^y,^''^°''c-0.
^'■xrES o* *■
Fishery Bulletin
Vol. 83, No. 1 January 1985
PEREZ FARFANTE, ISABEL. The rock shrimp genus Sicyonia (Crustacea:
Decapoda: Penaeoidea) in the eastern Pacific 1
NEILSON, JOHN D., GLEN H. GEEN, and BRIAN CHAN. Variability in dimen-
sions of salmonid otolith nuclei: implications for stock identification and micro-
structure interpretation 81
NEILSON, JOHN D., and GLEN H. GEEN. Effects of feeding regimes and diel
temperature cycles on otolith increment formation in juvenile chinook salmon,
Oncorhynchus tshawytscha 91
1 m(m m^^mcd Ubcralory [
LIBHABY
DEC 12 1985
Woods Hole, Mass.
Seattle, Washington
U.S. DEPARTMENT OF COMMERCE
Malcolm Baldrige, Secretary
NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION
John V. Byrne, Administrator
NATIONAL MARINE FISHERIES SERVICE
William G. Gordon, Assistant Administrator
Fishery Bulletin
The Fishery Bulletin carries original research reports and te(^nical notes on investigations in fishery science, engineering, and
economics. The Bulletin of the United States Fish Commission wks begun in 1881; it became the Bulletin of the Bureau of Fisheries
in 1904 and the Fishery Bulletin of the Fish and Wildlife Service in 1941. Separates were issued as documents through volume 46; the
last document was No. 1103. Beginning with volume 47 in 1931 and continuing through volume 62 in 1963, each separate appeared as
a numbered bulletin. A new system began in 1963 with volume 63 in which papers are bound together in a single issue of the bulletin
instead of being issued individually. Beginning with volume 70, nvunber 1, January 1972, the Fishery Bulletin became a periodical,
issued quarterly. In this form, it is available by subscription from the Superintendent of Documents, U.S. Government Printing
Office, Washington, DC 20402. It is also available free in limited numbers to libraries, research institutions. State and Federal
agencies, and in exchange for other scientific publications.
SCIENTIFIC EDITOR, Fishery Bulletin
Dr. William J. Richards
Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service, NOAA
Miami, FL 33149-1099
Editorial Committee
Dr Bruce B. Collette
National Marine Fisheries Service
Dr. Edward D. Houde
Chesapeake Biological Laboratory
Dr Merton C. Ingham
National Marine Fisheries Service
Dr. Reuben Lasker
National Marine Fisheries Service
Dr Donald C. Malins
National Marine Fisheries Service
Dr. Jerome J. Pella
National Marine Fisheries Service
Dr. Jay C. Quasi
National Marine Fisheries Service
Dr. Carl J. Sindermann
National Marine Fisheries Service
Mary S. Fukuyama, Managing Editor
The Fishery Bulletin (ISSN 0090-0656) is published quarterly by the Scientific Publications Office, National Marine Fisheries
Service, NOAA, 7600 Sand Point Way NE, BIN C15700, Seattle, WA 98115. Second class postage is paid at Seattle, Wash., and
additional offices. POSTMASTER send address changes for subscriptions to Superintendent of Documents, U.S. Government
Printing Office, Washington, IX; 20402.
Although the contents have not been copyrighted and may be reprinted entirely, reference to source is appreciated.
The Secretary of Commerce has determined that the publication of this periodical is necessary in the transaction of the public
business required by law of this Department. Use of funds for printing of this periodical has been approved by the Director of the
Office of Management and Budget through 1 April 1985.
Fishery Bulletin
CONTENTS
Vol. 83, No. 1 January 1985
PtREZ FARFANTE, ISABEL. The rock shrimp genus Sicyonia (Crustacea:
Decapoda: Penaeoidea) in the eastern Pacific 1
NEILSON, JOHN D., GLEN H. GEEN, and BRIAN CHAN. Variability in dimen-
sions of salmonid otolith nuclei: implications for stock identification and micro-
structure interpretation 81
NEILSON, JOHN D., and GLEN H. GEEN. Effects of feeding regimes and diel
temperature cycles on otolith increment formation in juvenile chinook salmon,
Oncorhynchus tshawytscha 91
jVlsrine Biste^isal Ufeoratory |
LIBRARY
DEC 12 19B5
Woods Hole, Mas
s.
Seattle, Washington
1985
For sale by the Superintendent of Documents, U.S. Government Printing Office, Washing-
ton DC 20402 — Subscription price per year: $21.00 domestic and $26.25 foreign. Cost per
single issue: $7.00 domestic and $8.75 foreign.
The National Marine Fisheries Service (NMFS) does not approve, recommend or
endorse any proprietary product or proprietary material mentioned in this pub-
lication. No reference shall be made to NMFS, or to this publication furnished by
NMFS, in any advertising or sales promotion which would indicate or imply that
NMFS approves, recommends or endorses any proprietary product or proprietary
material mentioned herein, or which has as its purpose an intent to cause directly
or indirectly the advertised product to be used or purchased because of this NMFS
publication.
THE ROCK SHRIMP GENUS SICYONIA
(CRUSTACEA: DECAPODA: PENAEOIDEA) IN THE EASTERN PACIFIC
Isabel Perez Farfante^
ABSTRACT
The genus Sicyonia is redefined and the 12 species occurring between Monterey Bay, California, and off
Pisco, Peru, are treated in detail. A key to species is followed by illustrated species accounts including
descriptions, ranges of intraspecific variation with analyses of morphometric data (rostrum to carapace
ratio graphically represented for 10 species), and color notes. The size ranges at which males and the
minimum sizes at which females attain adulthood are summarized, and ecological notes together with
maps illustrating the ranges of the species (six of which have been extended beyond limits previously
reported) are included. Sicyonia disparri seems to be restricted to the south and gulf coasts of Baja
California and waters off Nayarit, Mexico; S. affinis to waters off Costa Rica, Panama, and Colombia;
and S. penicillata occurs on the ocean side of Baja California Sur, Mexico, and from the Gulf of
California to Costa Rica. Sicyonia ingentis ranges from Monterey Bay to Nayarit, including the Gulf of
California. Sicyonia disedwardsi and S. martini occur along the ocean side of Baja California Sur, in
the Gulf of California, and southward to Panama, and four others, S. aliaffinis,S. disdorsalis,S. mixta,
and S. picta, frequent the same waters, but also reach as far south as Peru. Sicyonia laevigata and S.
brevirostris are found on both sides of the Continent, the former at the southern end of the Gulf of
California and from off Costa Rica to the Golfo de Panama in the Pacific, and from North Carolina to
Santa Catarina, Brazil, in the Atlantic. Sicyonia brevirostris has been recorded from the Golfo de
Tehuantepec and from Virginia southward through the Gulf of Mexico to Yucatan, and also from the
Bahamas and Cuba. In addition, there is an unverified literature record from Guyana. The treatment of
each species is concluded with a comparison of its diagnostic features with those of the most closely
allied congeners and a note on its present or potential economic value.
Until a few years ago, members of the genus
Sicyonia, "rock shrimps", were discarded from the
large commercial catches of panaeoid shrimps
made in tropical and subtropical waters of the
eastern Pacific and western Atlantic. It was com-
monly thought that because of their hard, stony
exoskeleton, they would be rejected by both con-
sumers and the processing industry; however, in-
creased demand for shrimp encouraged the
fishermen and dealers to bring the larger species
to market, and now production is not only readily
absorbed, but some prefer rock shrimps to the
thinner shelled species.
The exploitation and comparatively recent rec-
ognition of the commercial potential of Sicyonia,
the most distinctive group within the superfamily
Penaeoidea, have motivated this review of mem-
bers of the genus found in the American Pacific
(the western Atlantic species have already been
the object of a number of studies, e.g., Chace 1972;
Huff and Cobb 1979). For the most part, the infor-
Systematics Laboratory, National Marine Fisheries Service,
NOAA, National Museum of Natural History, Washington, DC
20560.
mation available is limited to the original descrip-
tions of the species, which are scattered in works
published between 1871 and 1945, and to a limited
number of locality records. Of the 12 species occur-
ring in the region, 4 had been recognized prior to
the close of the century. No other species were
reported from these waters until Burkenroad
made his invaluable studies (1934-45) which re-
sulted in the recognition of five new species plus
two others previously known to occur only in the
western Atlantic. Recently, Perez Farfante and
Boothe (1981) described the 12th member of the
genus frequenting the eastern Pacific. Two works
have been helpful in the identification of the
American Sicyonia: one by Anderson and Lindner
(1945) which provided a key to the then known
species; the other by Arana Espina and Mendez G.
(1978) in which was presented an illustrated key,
diagnoses, and ranges of the species found in
Peruvian and Ecuadorean waters, and an analysis
of morphometric relations, with data on the
growth and molting pattern of one of the species.
The extensive collections (515 lots containing
4,672 specimens) of Sicyonia available from Mon-
terey Bay, Calif., to off Pisco, Peru, and the oppor-
Manuscript accepted April 1984.
FISHERY BULLETIN: VOL. 83, NO. 1, 1985.
l'^<f
FISHERY BULLETIN: VOL. 83, NO. 1
tunity to examine all except two of the extant
type-specimens of the species have made a critical
study of the genus in the eastern Pacific possible.
The present work includes a definition of the genus
and a key to the species occurring in the region. A
complete synonymy and usually complete list of
references, vernacular names, and a diagnosis
precede the detailed description of each species,
which includes a discussion of the extensive varia-
tion exhibited as well as meristic and morphomet-
ric data. In addition, relation of the length of the
rostrum to the length of the carapace is graphed
for 10 species. Color notes, size range at which
males reach adulthood, and minimum size
at which females have been observed to be im-
pregnated are given. Geographic and bathymetric
ranges are delimited, and ecological data are pro-
vided. Analyses of the diagnostic features utilized
in the recognition of species and a discussion of
their phylogenetic relationships are also pre-
sented. Distributional maps as well as illustra-
tions of entire animals, genitalia, and a few other
morphological features are included along with a
bibliography which is as complete as possible. A
statement of their economic importance follows
the treatment of the pertinent species, and a list of
the specimens examined, with their localities, is
appended to each of the 12 species.
The distributional studies have resulted in ex-
tensions of both geographic and bathymetric
ranges of several species; e.g., of the seven species
known to occur both in the Gulf of California and
on the ocean side of the peninsula, five have not
been previously reported from the latter, and one,
which had been recorded only as far north as Point
Conception, Calif., was found to reach Monterey
Bay (Perez Farfante and Boothe 1981). Of the 12
species that have been reported from the region, 10
(or 11, in the unlikely event that the presence of S.
affinis is confirmed) occur in the Gulf of California;
of those occurring in the gulf, S. disparri appears
to be virtually confined to it and only S. ingentis
extends northward beyond Mexico, along the coast
of the United States. Eight of the 10 species range
southward to Central America, and of them 4
reach as far as Peru and S. aliaffinis also occurs off
Islas Galapagos. Sicyonia brevirostris has been
reported exclusively from the Golfo de Tehuan-
tepec, and S. affinis is known with certainty only
from Costa Rica to Colombia.
Seven of the species, S. laevigata, S. mixta, S.
disedwardsi, S. penicillata, S. aliaffinis, S. mar-
tini, and S. picta, appear to have disjunct ranges.
None has been recorded from stretches variable in
extension within the limits cited herein, and all of
the gaps encompass areas off southern Mexico.
Perhaps the discontinuities are due to limited
exploratory investigations; however, one species,
S. disdorsalis, has been found to occur virtually
continuously from the Gulf of California to Peru.
Nevertheless, speculations attempting to explain
the apparent gaps in the ranges of these species
should await the confirmation of their existence.
Except for records of the occurrence of S. picta at
333 m (Faxon 1893) and 369-400 m (Arana Espina
and Mendez G. 1978) and S. brevirostris at 329 m
(Williams 1965), no other species were previously
known from depths greater than about 200 m; here
six others are reported between about 250 and 300
m, depths considerably greater than their previ-
ously known maximum occurrence.
Distributions of members of the genus Sicyonia
in the eastern Pacific appear to differ strikingly
from those of most species of the closely related
family Penaeidae in that region. Whereas some
species of Sicyonia are restricted to comparatively
small areas (one confined to the southern and gulf
coasts of Baja California and waters immediately
south), others range from the Gulf of California to
the northern or to the central coasts of Peru. Most
of the eastern Pacific species, like their western
Atlantic congeners, reveal a marked preference for
firm or coarse bottoms.
PRESENTATION OF DATA
Many characters used in the descriptions are
depicted in Figures 1-7. To provide an appreciation
of the structure of the eye and the nomenclature
employed in its description I have chosen that of S.
disedwardsi. To illustrate the first article of the
antennular peduncle and anterior gnathal append-
ages, S. ingentis was selected. The petasmata
have been drawn from specimens stained with fast
green. For convenience, both the armature of ster-
nite XI and the shape of the posterior thoracic
ridge are presented with the description of the
thelycum. Scales accompanying the illustrations
are in millimeters. The length of the rostrum (rl)
recorded herein is the linear distance from the
apex to the orbital margin; length of the carapace
(cl) is the distance between the orbital margin and
the midposterior margin of the carapace; and the
total length (tl) is the distance from the apex of the
rostrum to the posterior end of the telson. The
geographic distribution of each of the species pre-
sented on the maps is based on material personally
examined and on published records believed to be
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
reliable. The names of the countries cited are in
English as are the Gulf of California and the Gulf
of Mexico; otherwise, all geographic features and
localities are in the language of the country in
which they occur
Material examined during this study are in the
collections of the following institutions.
AHF Allan Hancock Foundation, Los An-
geles, California, USA
AMNH American Museum of Natural His-
tory, New York, New York, USA
CAS California Academy of Sciences, San
Francisco, California, USA
IMARPE Instituto del Mar del Peru, Callao,
Peru
INP Instituto Nacional de Pesca, Sec-
retaria de Pesca, Mexico D.F.,
Mexico
MCZ Museum of Comparative Zoology,
Harvard University, Cambridge,
Massachusetts, USA
MP Museum National d'Histoire Natu-
relle, Paris, France
SIO Scripps Institution of Oceanography,
La Jolla, California, USA
UCR Universidad de Costa Rica, San Jose,
Costa Rica
UP Universidad de Panama, Panama
USNM National Museum of Natural History,
Smithsonian Institution, Washing-
ton, D.C., USA
YPM Peabody Museum of Natural History,
Yale University, New Haven, Con-
necticut, USA
ZMB Zoologisches Museum der Hum-
boldt-Universitat, Berlin, East
Germany.
Genus Sicyonia H. Milne Edwards 1830
Sicyonia H. Milne Edwards 1830:339 [type-
species, by monotypy: Sicyonia sculpta H. Milne
Edwards 1830:340 (= Cancer carinatus Brian-
nich 1768:102)]. H. Milne Edwards 1837:408.
De Haan 1849:187. Heller 1863:290. Bate
1888:292. A. Milne Edwards and Bouvier
1909:243. Balss 1914:14. Burkenroad 1945:1.
Barnard 1950:635. Holthuis 1952:339.
Hall 1956:87. Zariquiey Alvarez 1968:57.
[Name validated and placed on the Official
List of Generic Names in Zoology as Name No.
922 under Plenary Powers of the International
Commission on Zoological Nomenclature, Opin-
ion 382, 1956:45; Hemming 1958:126.] Gender:
feminine.
Ruvulus de Natale 1850:20 (published as synonym
of Sicyonia H. Milne Edwards 1830) [type-
species, by monotypy for Sicyonia H. Milne Ed-
wards: Sicyonia sculpta H. Milne Edwards
1830]. Holthuis 1952:339. Hall 1956:87.
Gender: masculine.
Synhimantites Boeck 1864:189 [type-species, by
monotypy: Synhimantites typicus Boeck
1864:189]. Burkenroad 1945:1. Holthuis
1952:339. Gender: masculine.
Eusicyonia Stebbing 1914:25 (substitute name for
Sicyonia H. Milne Edwards 1830) [type-species,
by monotypy for Sicyonia H. Milne Edwards
1830: Sicyonia sculpta H. Milne Edwards 1830].
Balss 1925:232. Burkenroad 1934a:70,
1934b:116, 1945:1. Kubo 1949:437. Holthuis
1952:339. Hall 1956:87. Gender: feminine.
Diagnosis. — Body with integument rigid, micro-
scopically setose-punctate. Rostrum short, not
overreaching distal margin of antennular pedun-
cle, more often falling short of it, and armed with
dorsal, and usually apical teeth, lacking ventral
ones (Fig. 1). Carapace with postrostral carina
bearing epigastric tooth and variable number of
teeth more posteriorly; orbital, postorbital, and
pterygostomian spines lacking; antennal spine
present or absent; hepatic spine well developed;
cervical sulcus indistinct; hepatic sulcus usually
shallow; hepatic carina weak or indistinct; bran-
chiocardiac carina strong to barely distinct (Fig.
2). Abdomen marked by transverse sulci bordered
by closely set setae; dorsomedian carina extending
for entire length; carina on first somite usually
produced in large anterior tooth, that on second
incised or entire, and that on sixth terminating in
strong tooth; sixth somite bearing cicatrix. Telson
armed with pair of marginal, fixed, subterminal
spines. Optic calathus articulated directly to basal
article of eyestalk, intermediate article [ = Young's
(1959) optic stalk] not apparent; ocular stylet pro-
jecting from anterolateral margin of ocular plate
(Fig. 3). Antennular peduncle about 0.6 cl; pro-
sartema (Fig. 4F-p) rudimentary; stylocerite long,
produced as sharp spine; antennular flagella
short, not exceeding 0.5 cl, mesial flagellum taper-
ing gradually from base, lateral one broad from
base to near tip, then tapering rapidly to apex.
Mandibular palp (Fig. 4A ) three-jointed, proximal
article small and short, distal article large, much
larger than penultimate one, and roughly
FISHERY BULLETIN: VOL. 83, NO. 1
P6REZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
Rostrum
Dorsal tooth\
Apical teethv
Adrostral carina-
Orbital margin-
Antennal spine-
Hepatic spine
Pterygostomian
region
Dorsum
/Epigastric tooth
Postrostral carina
Branchiostegite
Figure 2. — Lateral view of carapace oi Sicyonia showing terms used in descriptions.
Figure 3. — Sicyonia disedwardsi Stimpson, 2 30 mm cl, Golfo
de Panama, Panama. Eye, dorsal view: b, basal article; c,
cornea; o, optic calathus; p, ocular plate; s, ocular stylet. Scale
= 1 mm.
trapezoidal; first maxilla (Fig. 4S) with broad palp
unjointed and not produced distally; second
maxilla (Fig. 4C) with basipodite lacking proxi-
mal gnathal lobule; first maxilliped with flagel-
lum quite short (Fig. 4D); second maxilliped as
illustrated (Fig. 4E). Exopods lacking on second
and third maxillipeds and all pereopods. First
pereopod unarmed or with mesial spine on basis
and ischium. Endopods of pleopods absent except
for highly modified ones on first (petasma) and
second (bearing appendix masculina) pleopods.
Petasma (Fig. 5A) depressed, with dorsolateral
and heavily cornified ventrolateral lobules pro-
duced in distal projections, that of former funnel-
like, and with ventromesial slit; distal part of
dorsomedian lobule bearing short distal plate
resembling cusp in ventral aspect. Appendix mas-
culina (Fig. 5B ) projecting from free distal part of
ridge on dorsomedian margin of endopod, small,
roughly bellshaped, but with membranous termi-
nal wall. Male gonopores situated on sternite XIV.
Thelycum (Fig. 6) with plate of sternite XIV
single, flat or raised in paired, weak or prominent,
lateral bulges. Paired seminal receptacles (Fig. 7)
FISHERY BULLETIN: VOL. 83, NO. 1
Figure 4. — Sicyonia ingentis (Burkenroad 1938), ? 38 mm cl, off Bahia de San Quintin, Baja California Norte, Mexico. A,
Mandible. B, First maxilla. C, Second maxilla. D, First maxilliped — 6, branchial rudiment (arthrobranchia). £, Second maxil-
liped. F, First article of antennular peduncle — d, distolateral spine; p, rudimentary prosartema; s, stylocerite. Scales: A, C-E = 3
mm; B = \ mm; F = Z mm.
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
C
'$
o
X.
•X g
0)
n.
T3
n
O
&
y-
01
0)
>
o.
"H
t^
o
o
CJ
Q
s
<
c
o
CO
o
c
"a
CO
Sm
e
X
«,
c
r!
01
^
ex
,o
o.
CO
^-*
^*-<
n
U
0>
«'
"•>
m
m
o
1)
(-1
-i
(i>
CO
n
o
J
t-H
r
o
CO
T3
CO
0)
O
13
<1)
CO
s
c
CO
CO
to
U
"o
^
F
(U
E
>
CO
CO
^3
^
n>
Tt"
>
CO
05
T-H
03
"^
CO
r
^
o
P
-t^
q)
a.
-i«:
u
CJ
1
l/J
m
_C
«
T3
S-
0)
CO
"C
«
c
n
^
73
lO
w
OS
D
O
£1
FISHERY BULLETIN: VOL. 83, NO. 1
Figure 6. — Thelycum of Sicyonia showing
terms used in descriptions.
Posterior
thoracic ridge
^Sternite XI
Sternite XII
iSternite XIII
^Median plate
ii^uerior component
Sternite XIV
Plat^ of sternite XIV
Figure 7. — Sicyonia disedwardsi, 9 30 mm cl,
Golfo de Panama, Panama. Dorsal view of sperm
receptacles. Scale = 1 mm.
^'■**^
consisting of trilobed membranous sacs: large,
longitudinally disposed, mesial lobe, extending to
posterior margin of sternite XIV, and two small
anterior lobes, one directed anteriorly and the
other laterally; receptacles opening by transverse
slits at anterolateral margins of plate of sternite
XIV. Median plate of sternite XIII (supported by
buttress of sternite XII) large, triangular or
flask-shaped, tapering anteriorly in long, sharp
8
spine; plate bearing well-defined lateral constric-
tions setting off posterior component. Sternite XI
armed posteriorly with paired spines of variable
size. Branchial components consisting of pleu-
robranchia on somite IX; single arthrobranchia on
somite VII (lamellar rudiment; Fig. 4D-b); an-
terior and posterior arthrobranchiae on somites
VIII through XIII, anterior member of VIII very
small and that of XIII vestigial; and podobranchia
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
on second maxilliped. Epipod on first and second
maxillipeds and on first through third pereopods.
[Modified from Burkenroad (1934a, b) and Kubo
(1949).]
The species of this genus (about 55), the only one
encompassed in the family Sicyoniidae, occur in
tropical, subtropical, and temperate waters. They
are marine, some invading brackish waters, and
abundant at shallow to moderate depths; a number
of them also range across the continental shelf
onto the upper slope, reaching depths of several
hundred meters.
Members of Sicyonia exhibit a wide range of
intraspecific variation. The number and position of
the dorsal and apical rostral teeth and the ar-
rangement of teeth on the postrostral carina vary
as do the depth, extension, and form (continuous or
interrupted) of the abdominal sulci. Although the
number of the latter almost always provide a reli-
able diagnostic character for specific identifica-
tion, the posterior pleural sulcus may be present or
absent in some species. Furthermore, in females
the contour and sculpture of the thelycal plate of
sternite XIV and the shape of the posterior margin
of that of XIII also vary as pointed out in the
accounts for most of the species. In contrast, the
petasma of each of the members of the genus is
virtually invariable and thus useful for specific
recognition, and the appendix masculina is almost
constant in shape in all of the species.
In the females, sternite XI is armed with a pair
of spines which vary considerably in length, rang-
ing from quite small, as in all members oi Sicyonia
occurring in the eastern Pacific, to extremely long,
as in the western Atlantic iS. olgae Perez Farfante
1980. The posterior thoracic ridge varies but
within a range that does not prevent its having at
least limited diagnostic value.
Species of Sicyonia also exhibit various mor-
phological changes with increasing size. The
shape of the anteroventral margin of the pleuron
of the first abdominal somite may change gradu-
ally from straight in juveniles to pronouncedly
concave in adults, and the anteroventral ex-
tremities of the pleura of the first three or four
abdominal somites, from rounded to sharply
acute. The pleural armature, too, undergoes mod-
ifications with age; as Burkenroad (1934a) stated,
"A rounded angle usually precedes an unarmed
but acute angle, and this a veritable tooth, in the
course of individual development"; likewise, the
abdominal sculpture is altered, the sulci usually
becoming deeper as the animal grows. The forego-
ing statements indicate that abdominal features
which are diagnostic for the identification of
adults have scant systematic usefulness in iden-
tify ing juveniles.
Another characteristic of the genus is the wide
range in size among the species; whereas some are
small (the eastern Pacific S. disparri reaches a
maximum total length of about 44 mm), others are
quite large iS. ingentis and S. brevirostris attain a
total length of about 133 and 153 mm, respec-
tively).
In the genus Sicyonia there are two series of
species the contrasting characters of which would
appear to justify their separation into two genera.
The members of one series (occurring on both sides
of the Atlantic, in the Mediterranean and Indo-
Pacific, and represented in the eastern Pacific by
S. disparri and S. laevigata) lack or occasionally
exhibit a very minute antennal spine, are armed
with basial and ischial spines on the first pair of
pereopods, bear an incision or a notch on the dor-
somedian carina of the second abdominal somite,
and usually display a conspicuous notch on the
lateral margin of the petasma. The members of the
other series (restricted to American waters) have a
well-developed, buttressed, antennal spine, lack
basial and ischial spines on the first pair of
pereopods, have no incision on the carina of the
second abdominal somite, and never bear a notch
on the lateral margin of the petasma. These two
series, representing extremes of the range of vari-
ation in members of the genus, were first recog-
nized by Burkenroad (1934a) as Division I and
Division II, respectively. Both in 1934a and 1945,
he stated that there are species or series of species
in which some of these characters are inter-
changed. Certain species (all from the Indo-
Pacific) that lack an antennal spine and in which
the first pair of pereopods are armed exhibit an
entire carina on the second abdominal somite (the
first two are characters of Division I, and the last of
Division II). At least one species (also occurring in
the Indo-Pacific) lacks an antennal spine and has
armed first pereopods (both characters of Division
I) but bears an unnotched carina (a feature of
Division II). Another species (the eastern Pacific
S. mixta) that possesses an antennal spine and has
armed first pereopods exhibits a clearly distinct
depression on the carina of the second abdominal
somite which seems to correspond to the notch
characteristic of Division I.
Burkenroad (1934a) also divided his Division II
into species-groups, each named for one of the
species belonging to it. They were characterized by
the number, size, and position of the teeth on the
FISHERY BULLETIN: VOL. 83, NO. 1
postrostral carina. The complex intergradation of
the characters that have been used to recognize
these "Divisions" and "groups" of Sicyonia seems
to demonstrate that there are no superspecific dis-
junctions that will justify their being accorded
subgeneric or generic rank. In the present work,
occasionally, reference is made to these subdivi-
sions.
Key to the American Pacific species of
Sicyonia
la. First abdominal somite lacking tooth on
dorsomedian carina S. mixta
lb. First abdominal somite bearing anterior
tooth on dorsomedian carina 2
2a. Antennal spine absent or exceedingly
weak and without buttress; second abdom-
inal somite with perpendicular incision
in anterior half of dorsal carina; first
pereopod with short distomesial spine on
basis and ischium 3
2b. Antennal spine well developed and but-
tressed; second abdominal somite not
incised; first pereopod with basis and
ischium unarmed 4
3a. Postrostral carina armed with 3 sub-
equal teeth, anterior (epigastric) one as
large, or almost as large, as posterior 2
teeth; anteromedian sulcus of first abdom-
inal somite well marked to near ventral
margin of pleuron; posteroventral extrem-
ity of fourth abdominal somite dis-
tinctly angular S. disparri
3b. Postrostral carina armed with 3 unequal
teeth, anterior one conspicuously smaller
than posterior 2 teeth; anteromedian sul-
cus of first abdominal somite short, often
obscure, ending well above ventral mar-
gin of pleuron; posteroventral extremity
of fourth abdominal somite never distinct-
ly angular S. laevigata
4a. Postrostral carina with 2 or 3 teeth pos-
terior to level of hepatic spine 5
4b. Postrostral carina with 1 tooth posterior
to level of hepatic spine 7
5a. Postrostral carina almost always with 3
teeth posterior to level of hepatic spine,
occasionally anterior one of these at level
of or slightly anterior to hepatic spine
S. brevirostris
5b. Postrostral carina with 2 teeth posterior
to level of hepatic spine, never with tooth
at level or slightly anterior to hepatic
spine 6
6a. Rostrum bearing 2 dorsal teeth;
petasma with distal projections short and
stout; thelycum with plate of sternite XIV
raised in low (sometimes indistinct)
bulges and with posterior component of
median plate traversed by weak suture;
branchiostegite with large ocellus consist-
ing of well-defined yellow center sur-
rounded by purplish brown ring
S. disedwardsi
6b. Rostrum usually bearing 1 dorsal tooth
(rarely 2); petasma with distal projections
extremely long and slender; thelycum
with plate of sternite XIV raised in strong
bulges and with posterior component of
median plate traversed by deep groove;
branchiostegite with moderately large,
purplish brown spot sometimes bearing
poorly defined but diffuse yellow center
S. penicillata
7a. Postrostral carina behind posterior tooth
high, conspicuously elevated in arched
crest 8
7b. Postrostral carina behind posterior tooth
low, not elevated in high crest 11
8a. Fifth abdominal somite without tooth or
sharp angle at posterior end of dorsome-
dian carina; anteroventral extremity of
pleuron of fourth abdominal somite broad-
ly obtuse and unarmed S. affinis
8b. Fifth abdominal somite with tooth or
sharp angle at posterior end of dorsome-
dian carina; anteroventral extremity of
pleuron of fourth abdominal somite sharp-
ly angular or armed with spine 9
9a. Rostrum long, conspicuously surpassing
distal margin of eye; anteroventral angle
of second through fourth abdominal
somites unarmed, lacking spine; petasma
with projection of dorsolateral lobule dis-
tinctly bifurcate apically S. martini
9b. Rostrum short, falling short of, or infre-
quently barely surpassing distal margin
of eye; anteroventral angle of second
10
PfiREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
through fourth abdominal somites armed
with curved spine; petasma with projec-
tions of dorsolateral lobule simple 10
10a. Rostrum armed with 2 dorsal teeth; ab-
domen heavily tuberculate; anteromedian
pleural sulcus of first abdominal somite
well marked to near ventral margin of
pleuron; anteromedian pleural sulcus of
second and third somites reaching dor-
sally posteromedian pleural sulcus; bran-
chiostegite with horizontally disposed
9-shaped, brown mark S. aliaffinis
10b. Rostrum armed with 3 or 4 dorsal teeth;
abdomen with very few tubercles; an-
teromedian pleural sulcus of first abdom-
inal somite well marked only dorsally; an-
teromedian pleural sulcus of second and
third somites not reaching dorsally pos-
teromedian pleural sulcus; branchioste-
gite with ocellate mark, consisting of red
center surrounded by yellow ring
S. picta
11a. Dorsomedian carina of first abdominal
somite produced in tooth considerably
larger than posterior tooth on carapace,
that of fifth truncate or produced in spine
at posterior end; petasma with distal pro-
jections of dorsolateral lobules turned
mesially and lacking terminal filament;
thelycum with posterior component of
median plate flat or slightly raised pos-
terolaterally, not bearing short bosses cut
by transverse suture S. disdorsalis
lib. Dorsomedian carina on first abdominal
somite produced in tooth smaller or only
slightly larger than posterior tooth on
carapace, that of fifth sloping gradually to
posterior end; petasma with distal projec-
tions of dorsolateral lobules divergent and
produced in short filament; thelycum with
posterior component of median plate bear-
ing paired short lateral bosses cut by
transverse suture S. ingentis
Sicyonia laevigata Stimpson 1871
Figures 8-12
Sicyonia laevigata Stimpson 1871: 131 [type not
extant; type-locality: Charleston, S.C.].
Kingsley 1878:69, 1880:426. Rathbun 1901:
103 [part]. De Man 1911:11. Bouvier 1918:6.
Hay and Shore 1918:379, pi. 25, fig. 1. Rath-
bun 1920:319. Burkenroad 1945:5. Lunz
1945:4, fig. 1. Pearse and Williams 1951:
143. Wass 1955:142. Menzel 1956:41. Hut-
ton et al. 1959:6. Wells 1961:248. Williams
1965:33. Fausto Filho 1966a:32, 1966b:47,
fig. 8. Eldred et al. 1965:32. Joyce and El-
dred 1966:24. Fausto Filho 1968:73. Rouse
1969:136. Bayer et al. 1970:41. Lyons et
al. 1971:28. Garcia Pinto 1971:5. Chace
1972:11. Camp et al. 1977:23. Rodriguez
de la Cruz 1977:11. Huff and Cobb 1979:67,
fig. 38a-d. Rodriguez 1980:70. Perez
Farfante 1980:773. Greening and Living-
ston 1982:151. Coen and Heck 1983:206.
Williams 1984:47.
Sicyonia sculpta var. americana De Man 1907:450.
Sicyonia carinata De Man 1907:451. [Not Cancer
carinatus Briinnich 1768 = Sicyonia carinata.]
Sicyonia carinata var. americana De Man 1911:10.
Eusicyonia laevigata. Burkenroad 1934a:76, fig.
21, 26, 32, 1934b:117. Schmitt 1935:132.
Burkenroad 1938:80. Lunz 1945:4, fig. 1.
Sicyonia carinata americana. Burkenroad
1934a:76.
Vernacular names: rock shrimp, hardback, coral
shrimp (United States); camaron de piedra,
cacahuete (Mexico); camaron conchiduro
(Mexico, Panama); camarao-da-pedra (Brazil).
Diagnosis. — Antennal spine absent or barely dis-
tinct and lacking buttress. Second abdominal so-
mite with perpendicular incision on dorsomedian
carina. First pereopod armed with short spine on
basis and ischium. Postrostral carina bearing
three unequal teeth, epigastric one considerably
smaller than posterior two teeth. Anteromedian
sulcus of first abdominal somite, if distinct, short,
ending well above margin of pleuron; posteroven-
tral extremity of fourth abdominal somite not dis-
tinctly angular. Petasma with distal projection of
dorsolateral lobule almost straight but with apical
part curved dorsally. Thelycum with plate of ster-
nite XIV produced in elongate anterolateral
lobules, their anteromesial borders strongly di-
vergent.
Description. — Body moderately robust (Fig. 8)
and lacking tubercles. Carapace with patches of
short setae on dorsum, as well as ventral and an-
terior to posterodorsal part of branchiocardiac
carina; extremely long setae flanking base of, and
between, teeth of postrostral carina.
Rostrum long, reaching as far as distal end of
11
FISHERY BULLETIN: VOL. 83, NO. 1
Figure 8. — Sicyonia laevigata, 9 9 mm cl, Punta Paitilla, Panama. Lateral view. Scale = 5 mm.
antennular peduncle, its length (0.40-0.77 cl) in-
creasing linearly with carapace length (Fig. 9);
relatively deep, usually with dorsal and ventral
margins straight and subparallel; subhorizontal
or upturned to as much as 35°; armed with two
(25%), three (72%), or four (3%) dorsal teeth and
two (5%), three (33%), or four (62%) apical teeth,
additional rudimentary one present between two
ventral ones; ventralmost tooth, largest of apical
cluster, subterminal, directed anteriorly or curved
upward, and distinctly removed from adjacent one.
Position of first dorsal tooth ranging between 0.09
and 0.30 (mean 0.18) rl from level of orbital mar-
gin, and that of second tooth between 0.42 and 0.60
(mean 0.45) rl; third tooth, when present, between
0.76 rl and tip of rostrum (mean 0.87); and fourth,
rarely present, located at tip. Two, occasionally
one or three, minute but rather heavy movable
spinules (often absent in adults) flanking ventral
margin of rostrum, just posterior to apical teeth.
Adrostral carina, subparallel to ventral margin of
rostrum, extending to base of apical cluster.
Carapace with postrostral carina, barely dis-
tinct between teeth, bearing three unequal,
acutely produced teeth: 1) epigastric tooth,
situated between 0.06 and 0.16 (mean 0.12) cl from
orbital margin, subequal to or only slightly larger
than first rostral and conspicuously smaller than
more posterior teeth; 2) middle tooth, placed be-
tween 0.35 and 0.50 (mean 0.45) cl from orbital
margin; and 3) posterior tooth positioned be-
tween 0.68 and 0.80 (mean 0.72) cl from orbital
margin, well in advance of posterior margin of
carapace. Antennal spine absent or barely per-
ceptible, antennal angle 90° to broadly obtuse,
lacking buttress; hepatic spine long, sharply
pointed, projecting from low buttress, and situated
* 4
6 9
carapace length (mm)
12
15
Figure 9. — Sicyonia laevigata. Relationship between rostrum
length and carapace length (regression equation, >> = -0.39153
+ 0.64127X).
between 0.22 and 0.30 (mean 0.25) cl posterior to
orbital margin. Postocular sulcus short; hepatic
sulcus shallow, subhorizontal; hepatic carina lack-
ing; branchiocardiac carina barely evident.
Ocular calathus broad and bearing conspicuous
tuft of setae on dorsolateral extremity; ratio of
length of lateral margin to width (across base of
cornea) 0.54-0.65 (mean 0.60) and ratio length of
lateral margin to cl 0.11-0.15 (mean 0.13).
Antennular peduncle with stylocerite produced
in acute spine reaching 0.65-0.75 of distance be-
tween lateral base of first antennular article and
mesial base of distolateral spine; latter extending
only to about proximal 0.40 of second antennular
article. Antennular flagella short, mesial one,
about 0.7 as long as lateral; latter, about 0.4 cl.
Scaphocerite almost reaching or slightly sur-
12
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
passing distal end of third antennular article; lat-
eral rib produced in long, slender spine slightly
overreaching lamella. Antennal flagellum as
much as 3 times as long as carapace.
Third maxilliped much stouter than pereopods.
Basis and ischium of first pereopod armed with
short but well-developed sharp spine projecting
from distomesial margin.
Abdomen with dorsomedian carina low an-
teriorly, increasing in height posteriorly; carina on
first somite produced in rather small, anteriorly
directed tooth, smaller than posterior tooth on
carapace; carina on second somite conspicuously
incised (just dorsal to juncture of tergal sulci) and
that on sixth terminating in short, sharp tooth.
Antero ventral extremity of pleuron of first three
somites rounded; pleuron of fourth with postero-
ventral extremity angular or subangular, always
unarmed; postero ventral extremity of fifth and
sixth somites produced in very small, caudally
directed, sharp tooth.
First somite with short anteromedian pleural
sulcus (usually well marked but sometimes
obscure dorsally, obsolete, or represented by shal-
low depression ventrally) and long, united pos-
terior tergal-posteromedian pleural sulci. Second
and third somites marked by 1) long anterior ter-
gal (extending to base of pleuron) and short pos-
terior tergal sulci; 2) anteromedian pleural sulcus,
extending to near ventral margin on second somite
but restricted to dorsal part on third, in both so-
mites delimiting anterior shallow depression set-
ting off weak prominence dorsally; and 3) pos-
teromedian pleural sulcus, its dorsal extremity
curving anteriorly ventral to (not joining) pos-
terior tergal sulcus. Fourth and fifth somites with
anterior tergal sulcus (that of fourth obliterated
about midlength), merging with united posterior
tergal-posteromedian pleural sulci. Sixth somite
marked by weak, arched posteromedian pleural
sulcus and bearing shallow longitudinal depres-
sion between low dorsolateral ridge and elongate
cicatrix.
Telson with pair of short but strong fixed spines
and two longitudinal rows of movable spinules on
each side of median sulcus. Rami of uropod reach-
ing or barely overreaching apex of telson.
Petasma (Fig. lOA, B) with rigid distal projec-
tion of dorsolateral lobule bulbous proximally, al-
most straight but with terminal part strongly
curved dorsally; fleshy distal projection of ven-
trolateral lobule directed distolaterally, broad
basally, and with slender but blunt terminal part
curved proximally. Lateral margin of petasma
Figure lO. —Sicyonia laevigata, 6 5.7 mm cl, Isla Taboga, Panama. A, Petasma, dorsal view; fi, ventral view; C, right appendix
masculina, dorsolateral view. Scale = 0.5 mm.
13
FISHERY BULLETIN: VOL. 83, NO. 1
Figure 11. — Sicyonia laevigata. Thelyca. A,? 7 mm cl, Isla San Lucas, Costa Rica; B, J 9 mm cl, Punta Paitilla, Panama. Scales
= 0.5 mm.
slightly to conspicuously notched near midlength.
Petasmal endopods coupled in males with
carapace length as little as 2.9 mm, about 13 mm
tl, petasma joined in all larger males.
Appendix masculina as illustrated in Figure
IOC.
Thelycum (Fig. ILA, B) with plate of sternite
XIV produced in elongate, subalate anterolateral
lobules, their anteromesial borders strongly di-
vergent; plate flat except for deep, broad, antero-
median depression, limited posteriorly by raised
margin of posterior thoracic ridge. Median plate of
sternite XIII narrow, lanceolate, tapering gently
into sharp spine reaching as far as midlength of
coxae of extended second pereopods; plate con-
stricted and excavate at level of fourth pereopods;
posterior component of plate with posterior mar-
gin entire to deeply emarginate and traversed by
weak suture. Paired conspicuous spines projecting
anteroventrally from posterior margin of sternite
XI. Posterior thoracic ridge insensibly fused later-
ally with plate of sternite XIV.
The smallest impregnated female observed has
a carapace length of 5 mm, about 18 mm tl.
Co/or.— Huff and Cobb (1979) presented a detailed
14
account of the color pattern of this species based
on specimens collected on Florida's west central
shelf
Maximum size. — Males 7.3 mm cl, about 34 mm tl;
females 15 mm cl, about 53 mm tl.
Geographic and bathymetric ranges. — In the
American Pacific, S. laevigata is known from
Mazatlan (lat. 23°13'N, long. 106°25'W), Mexico
(Rodriguez de la Cruz 1977); Isla San Lucas
(9°56'N, 84°54'W), Golfo de Nicoya, Costa Rica;
and the Golfo de Panama, in the latter as far as
Punta Paitilla (8°58'N, 79°31'W), Panama. In the
western Atlantic this species ranges from off Cape
Hatteras (35°08'30"N, 75°10'00"W), N.C., south-
ward and into the Gulf of Mexico to northwest
Florida, and off Yucatan. Also, it occurs through
the Antilles and around the Caribbean coast of
Mexico, Central America, and South America, and
along the Atlantic coast of South America to Anse
de Zimbros (27°13'S, 48°31'W), Santa Catarina,
Brazil (Fig. 12).
In the Pacific, this shrimp has been taken from
tide pools to a depth of 4-9 m, but in the Atlantic it
occurs from the shore to as deep as 90 m. It occurs
PfeREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
on corals or other firm, rocky or shelly substrates,
but occasionally, as reported by Wass (1955), on
soft mud.
On the basis of their samplings and the observa-
tions made by Lyons et al. (1971), Huff and Cobb
(1979) concluded that S. laevigata "shows some
preference for grass habitats in estuarine and
nearshore environments, associating with coarse
substrates further offshore where seagrasses are
absent."
This species has been found at salinities be-
tween 22 and 37%o (Lyons et al. 1971 and Menzel
1956, respectively) and temperatures between 17°
and 32°C (Lyons et al. 1971 and Camp et al. 1977,
respectively).
Discussion. — Sicyonia laevigata is most similar to
the Pacific S. disparri and the western Atlantic S.
parri, but it may be readily distinguished from
them by the following features. The epigastric
tooth in S. laevigata is smaller than, instead of
almost as large as, the other teeth on the postros-
tral carina. Also in S. laevigata this tooth is al-
ways situated anterior to the hepatic spine, be-
tween 0.06 and 0.16 (mean 0.12) cl from the orbital
margin, whereas in S. disparri it is often located
opposite or posterior to the hepatic spine but, if
anterior, usually farther from the orbital margin,
between 0.12 and 0.25 (mean 0.17) cl. The an-
teromedian pleural sulcus of the first abdominal
somite in S. laevigata is short, commonly well
defined (sometimes obscure) dorsally, but obsolete,
cr represented by a shallow depression ventrally;
in contrast, in S. disparri and S. parri it is long,
extending to near the ventral margin of the
pleuron, although sometimes it is interrupted dor-
sal to midlength. In S. laevigata the posterior
pleural sulci are lacking, as they usually are in S.
disparri, whereas in S. parri they are present.
Furthermore, in the petasma of S. laevigata the
distal projection of the dorsolateral lobule is di-
rected distally, its tip curved dorsally, whereas in
S. disparri and S. parri it is strongly curved
mesially — but in the latter the tip is bent slightly
dorsally. It should be pointed out that S. parri , like
the other two species, lacks an antennal spine,
possesses a spine on the basis and ischium of the
first pereopod, and bears a dorsal incision on the
dorsomedian carina of the second abdominal so-
mite.
Remarks. — In 1980, 1 stated that the dorsal mar-
gin of the rostrum of S. laevigata is armed with
three teeth, an opinion that was contrary to that of
Figure 12. — CJeographic distribution of Sicyonia
laevigata, S. disparri, and S. mixta.
15
FISHERY BULLETIN: VOL. 83, NO. 1
previous authors who noted that it bears only two;
1 was convinced at the time that they considered
the variably situated third tooth, when located
subterminally, an apical instead of a dorsal tooth.
The study of the extensive collection available to
me for the present project has indicated that this
species sometimes (25% of the specimens) bears
only two teeth, and occasionally four (3% of the
individuals).
It should be mentioned that the holotype of this
species was lost during the Chicago fire of 1871.
Material. — 73 specimens from 41 lots.
Eastern Pacific — 12 specimens from 6 lots.
Costa Rica — 15, USNM, Isla San Lucas, 5
January 1930, M. Valerio.
Panama— Id 19, AHF, Isla Taboga, 4-9 m, 2
May 1939. 39, SIO, Isla Taboga, 3 m, 30 March
1967, R. Rosenblatt. 19, USNM, Punta Paitilla,
intertidal, 1 July 1969, L. G. Abele and J. Gra-
ham. 19, USNM, Punta Paitilla, intertidal, 17
June 1969, J. Graham. 49, USNM, Punta Pai-
tilla, 8 m, 13 April 1972, C. E. Dawson and party
Western Atlantic — 61 specimens from 34 lots.
United States— North Carolina: 19, USNM,
off Cape Hatteras, 90 m, 17 October 1885, Alba-
tross stn 2596. 29 , USNM, off Morehead City, 14
July 1913, Fish Hawk. 39, USNM, Boque Sound
(off Morehead City), August 1912, Fish Hawk . 19 ,
USNM, Black Rocks (off New River), 13 m, 8 Au-
gust 1949, A. S. Pearse. South Carolina: 19,
USNM, mouth of Bulls Creek, 1891, Fish
Hawk . 16 , USNM, Charleston Harbor, 14.5 m, 13
March 1891, Fish Hawk stn 1659. 19 , USNM, off
S end of May River, Calibogue Sound, 18 m, 16
January 1891, Fish Hawk stn 1651. Flori-
da: 19, USNM, Biscayne Bay, 7 July 1960, B.
Petskin. 19 , MCZ, off Key West, J. R. Miller. 16
49, USNM, Marco, 2-5.5 m, H. Hemphill. 16,
USNM, Punta Rassa, 2 m, February 1884, H.
Hemphill. 19, USNM, Charlotte Harbor, March
1887, W H. Dall. 26 29, USNM, Sarasota Bay H.
Hemphill. 16, USNM, St Martin, 5.5 m, 15
January 1902, Fish Hawk stn 7222. 16 39,
USNM, off St Martin's Reef, 5 m, G. F Moser 26 ,
USNM, off NW end St Martin's Reef, 1887, G. R
Moser. 19, USNM, Aucilla, 9 m, 6 November
1901, Fish Hawk stn 7148.
Cuba— Id 19, USNM, off Cayo Levisa, 4-5.5 m,
2 June 1914, Tomas Barrera Exped stn 14.
Jamaica— Id, USNM, SE of Great Pedro Bluff,
27-29 m, 6 July 1970, Pillsbury stn 1223.
Haiti— 19, AMNH, Port-au-Prince, W Beebe.
Puerto Rico— 29, USNM, Mayagiiez, 23 m, 20
January 1899, Fish Hawk stn 6093. Id 39,
USNM, Mayagiiez Harbor, 19-20 January 1899,
Fish Hawk . 29 , USNM, off Humacao, 23 m. Fish
Hawk. 26 29, USNM, off Isla Culebra, 27 m, 8
February 1899, Fish Hawk stn 6093.
Virgin Islands— St. Thomas: 19 , USNM, 1884,
Albatross.
Mexico — Quintana Roo: Id, USNM, off Isla
Mujeres, 29.5 m, 11 June 1962, Oregon stn
3638. Id , USNM, SE of Isla Mujeres, 101-275 m,
9 September 1967, Gerda stn 880. 19, USNM,
Bahia de la Ascension, 17 April 1960, Smith-
sonian-Bredin Caribbean Exped stn 85-60.
Nicaragua — 29, USNM, off NE Nicaragua, 55
m, 8 June 1964, Oregon stn 4930. 29 , USNM, off
Prinzapolca, 27 m, 28 January 1971, Pillsbury stn
1335. 19, USNM, E of Isla del Venado, 24 m, 28
January 1971, Pillsbury stn 1330. Id 19 , USNM,
SE of Punta de Perlas, 27 m, 28 January 1981,
Pillsbury stn 1334.
Colombia— 19, USNM, Sabanilla, 1884, Alba-
tross. 19, USNM, off Tucuracas, 9 m, 30 July
1968, Pillsbury stn 778.
Brazil — Santa Catarina: 19, MP, Anse de
Zimbros, 5-0 m, 16 December 1961, Calypso stn
148.
Sicyonia disparri (Burkenroad 1934)
Figures 5, 12-17
Eusicyonia disparri Burkenroad 1934a:83, fig. 27
[holotype: 9, YPM 4392, Bahia San Luis Gon-
zaga, Baja California Norte, Mexico, 17 May
1926, Pawnee]. Burkenroad 1938:80.
Anderson and Lindner 1945:315.
Sicyonia disparri. Brusca 1980:256.
Vernacular names: rock shrimp (United States);
camaron conchiduro, camaron de piedra,
cacahuete (Mexico).
Diagnosis. — Antennal spine absent. Second ab-
dominal somite with perpendicular incision on
dorsomedian carina. First pereopod armed with
short spine on basis and ischium. Postrostral
carina bearing three subequal teeth, epigastric
one as large, or almost as large, as posterior two
teeth. Anteromedian sulcus of first abdominal so-
mite clearly distinct to near ventral margin of
pleuron; posteroventral extremity of fourth ab-
dominal somite markedly angular Petasma with
distal projection of dorsolateral lobule curved me-
16
PfeREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
sially to apex. Thelycum with plate of sternite XIV
produced in elongate anterolateral lobules, their
anteromesial borders strongly divergent.
Description. — Body moderately robust (Fig. 13)
and lacking tubercles. Carapace with short setae
scattered over surface and extremely long ones
between and flanking base of teeth on postrostral
carina.
larger adults) flanking ventral margin of rostrum
posterior to apical teeth. Adrostral carina, sub-
parallel and distinctly dorsal to ventral margin,
extending almost to base of apical cluster
Carapace with weak postrostral carina bearing
three subequal, acutely produced teeth: 1)
epigastric tooth, often larger than first rostral and
nearly as large as posterior teeth, situated be-
tween 0.12 and 0.25 (mean 0.17) cl from orbital
Figure 13. — Skyonia disparri, holotype 9 10.4 mm cl, Bahia San Luis Gonzaga, Baja California Norte, Mexico. Lateral
view. Scale = 5 mm.
Rostrum long, reaching as far as distal margin
of second antennular article, its length (0.40-0.70
cl) increasing linearly with carapace length (Fig.
14); relatively deep, with dorsal and ventral mar-
gins subparallel; upturned to angle between 15°
and 45°; armed with three dorsal teeth and two
(7%), three (34%), four (57%), or five (2%) apical
teeth, additional rudimentary one present be-
tween two ventral ones; ventralmost tooth largest
of apical cluster, subterminal, directed anteriorly
or curved upward, and distinctly removed from
adjacent tooth. Position of first dorsal tooth rang-
ing from slightly posterior to level of orbital mar-
gin, to as much as 0.30 (mean 0.18) rl anterior to it;
that of second tooth between 0.40 and 0.65 (mean
0.50) rl from orbital margin, and that of third
between 0.65 and 0.90 (mean 0.75) rl. Paired mi-
nute, movable spinules (sometimes absent in
3 6 9 12
carapace length (mm)
\5
Figure 14. — Sicyonia disparri. Relationship between rostrum
length and carapace length (regression equation, y = -0.03809
+ 0.51152X).
17
FISHERY BULLETIN: VOL. 83, NO. 1
margin, i.e., anterior, opposite, or posterior to
hepatic spine; 2) middle tooth, largest of three,
placed between 0.34 and 0.48 (mean 0.42) cl from
orbital margin; and 3) posterior tooth, positioned
well in advance of posterior margin of carapace,
between 0.64 and 0.73 (mean 0.70) cl from orbital
margin. Antennal spine absent, antennal angle
broadly obtuse or rounded; hepatic spine long,
sharply pointed, projecting from low buttress, and
positioned between 0.20 and 0.30 (mean 0.25) cl
posterior to orbital margin. Postocular sulcus
short; hepatic sulcus shallow, subhorizontal; hepa-
tic carina lacking; branchiocardiac carina at most
barely evident.
Eye (Fig. 15A) with ocular calathus broad and
bearing conspicuous tuft of setae on dorsolateral
extremity; ratio of length of lateral margin to
width (across base of cornea) 0.50-0.60 (mean 0.54)
and ratio length of lateral margin to carapace
length 0.08-0.13 (mean 0.11).
Antennular peduncle with stylocerite produced
in acute spine reaching 0.65-0.85 of distance be-
tween lateral base of first antennular article and
mesial base of distolateral spine; latter extending
to proximal 0.45 of second antennular article. An-
tennular flagella short, mesial one about 0.8 as
long as lateral; latter about 0.4 cl.
Scaphocerite reaching between midlength and
distal end of third antennular article; lateral rib
produced in long, slender spine conspicuously
overreaching lamella. Antennal flagellum as
much as 3 times as long as carapace.
Third maxilliped much stouter than pereopods.
Basis and ischium of first pereopod each armed
with well-developed sharp spine.
Figure 15.— Eyes. A, Sicyonia disparri, ? 9 mm cl, NW of
Mantanchen, Nayarit, Mexico. B,S. parri (Burkenroad), j 10.5
mm cl, east side of Cocoa Point, Barbuda. Dorsal views. Scale
= 1 mm.
Abdomen with dorsomedian carina low an-
teriorly, increasing in height posteriorly; carina
on first somite produced in rather small, an-
teriorly directed tooth, usually smaller than pos-
terior tooth on carapace; carina on second somite
conspicuously incised, and that on sixth terminat-
ing in short, sharp tooth.
Anteroventral extremity of pleura of first three
somites rounded; pleuron of fourth with postero-
ventral margin straight to concave, its postero-
ventral extremity distinctly angular, occasionally
armed with minute tooth; posteroventral extrem-
ity of fifth and sixth somites produced in very
small, caudally directed, sharp tooth.
First somite traversed by long, sometimes inter-
rupted, deep anteromedian pleural sulcus ending
well above ventral margin without meeting long,
united posterior tergal-posteromedian pleural
sulci. Second and third somites marked by 1) long
anterior tergal sulcus and relatively short pos-
terior tergal sulcus; 2) anteromedian pleural sul-
cus, extending almost to ventral margin on second
somite but restricted to dorsal part on third, in
both somites delimiting anterior shallow depres-
sion setting off rounded prominence dorsally; and
3) posteromedian pleural sulcus, its dorsal ex-
tremity curving anteriorly, ventral to (not joining)
posterior tergal sulcus. Fourth and fifth somites
with anterior tergal sulcus (that of fourth usually
obliterated at about midlength) fused with united
posterior tergal-posteromedian pleural sulci.
Sixth somite marked by strongly arched pos-
teromedian pleural sulcus and bearing shallow,
longitudinal depression between dorsolateral
ridge and elongate, often ill-defined cicatrix.
Telson with pair of short but well-developed
fixed spines and two longitudinal rows of movable
spinules on either side of densely setose median
sulcus — mesial row extending almost to base of
spine. Both rami of uropod almost reaching or
barely overreaching apex of telson.
Petasma (Figs. 5, 16A, B) with cornified distal
projection of dorsolateral lobule bulbous prox-
imodorsally, curved mesially, and minutely bifid
distally; fleshy distal projection of ventrolateral
lobule directed distolaterally, expanded basally
and with slender but blunt terminal part slightly
curved proximally. Lateral margin of petasma
conspicuously notched just proximal to mid-
length, forming shoulder immediately proximal
to notch.
Petasmal endopods coupled in males with
carapace length as little as 3 mm (about 13 mm tl)
but sometimes unjoined in individuals with
18
PEREZ FARFANTE: ROCK SHRIMP GE^^JS SICYONIA
Figure 16. — Sicyonia disparri,6 6 mm cl, Canal de San Lorenzo, Baja California Sur, Mexico. A , Petasma, dorsal view; B , ventral
view of same; C, right appendix masculina, dorsolateral view. Scale = 0.5 mm.
carapace length as much as 4.9 mm (about 21 mm
tl).
Appendix masculina as illustrated in Figure
16C.
Thelycum (Fig. 17) with plate of sternite XIV,
produced in conspicuous anterolateral lobules, flat
except for deep, broad, median depression. Median
plate of sternite XIII narrow, lanceolate, tapering
gently into long, sharp spine reaching as far as
proximal 0.25 of basis of extended second
pereopods; plate constricted and deeply excavate
at level of coxae of fourth pereopods; posterior
component of plate with shallow, broad postero-
median emargination and well-marked transverse
suture. Paired conspicuous spines projecting an-
teromesially from posterior margin of sternite XI.
Posterior thoracic ridge with sharp, concave an-
teromedian margin but areas immediately lateral
to concavity flush with plate of sternite XIV.
The smallest impregnated female encountered
has a carapace length of 5 mm, about 21 mm tl.
Maximum size. — Males 6.9 mm cl, about 30 mm tl;
females 11 mm cl, about 44 mm tl.
Figure 17. — Sicyonia disparri, holotype 5 10.4 mm cl, Bahia
San Luis Gonzaga, Baja California Norte, Mexico.
Thelycum. Scale = 1 mm.
Geographic and bathymetric ranges. — In the Gulf
of California, from Bahia San Luis Gonzaga
(29°48'N, 114°22'W), Baja California Norte, and
southward along the east coast of the peninsula, to
Isla Santa Magdalena (24°55'N, 112°15'W), Islas
Tres Marias, Nayarit, Mexico; also off Cabo San
19
FISHERY BULLETIN: VOL. 83, NO. 1
Lucas (22°52'23"N, 109°53'23"W), Baja California
Sur (Fig. 12). This species occurs at depths between
0.2 and 82 m, mostly at <24 m, and on sandy
bottoms: sand, sand and shell, sand and gravel,
and a mixture of sand mud, and coral. Among the
eastern Pacific rock shrimps, S. disparri appears
to have one of the most restricted distributions,
being virtually confined to the Gulf of California
and waters off Nayarit. Its presence south of the
Gulf of California is reported here for the first
time.
Discussion. — This shrimp is very similar to the
geminate western Atlantic S. parri both in mor-
phology and size. Burkenroad (1934a) first distin-
guished S. disparri by the absence of posterior
pleural sulci on the anterior two abdominal so-
mites and by the shorter, deeper, and more up-
turned rostrum. A few years later (1938), on the
basis of three additional specimens, he pointed out
other features in which S. disparri differed from
his two specimens of S. parri: the shape of the
posteroventral margin and extremity of the fourth
abdominal somite, the presence of one or two pairs
of movable spinules dorsal to the ventral margin of
the rostrum near its anterior end, and the presence
of four instead of three teeth on the dorsal margin
of the rostrum. He stated that these characters are
probably subject to variation and in so doing indi-
cated that they might not be diagnostic. He noted,
however, that the size and shape of the ocular
calathus and the size and disposition of the cornea
might prove to be diagnostic.
My examination of a relatively large collection
of S. disparri has demonstrated that among the
various features that Burkenroad (1934a, 1938)
suggested to distinguish this species from S. parri ,
three are diagnostic: 1) the disposition of the ros-
trum, which is upturned between 15° and 45° in
the former, is subhorizontal or inclined not more
than 13° in the latter; 2) the shape of the postero-
ventral extremity of the pleuron of the fourth ab-
dominal somite, which is angular in S. disparri
and rounded in S. parri; and 3) the shape of the
ocular calathus and the breath and disposition of
the cornea. In the Pacific shrimp the calathus is
broader than in the Atlantic species, the lateral
margin ranges from 0.50 to 0.60 (mean 0.54) its
width at the base of the cornea and the latter is
obliquely disposed. In S. parri the lateral margin
of the calathus (Fig. 15B) varies from 0.80 to 0.91
(mean 0.85) its width at the base of the cornea, and
the latter is almost horizontally disposed. I have
confirmed that the ratio of the lateral margin of
the calathus to the length of the carapace is usu-
ally smaller in .S. disparri than in S. parri, rang-
ing from 0.08 to 0.13 (mean 0.11) in the former and
from 0.13 to 0.17 (mean 0.13) in the latter, but
sometimes overlapping.
The absence of posterior pleural sulci is a
character that, although not infallible, serves al-
most always to separate S. disparri from S. parri,
lacking in all specimens of the former except in
two small individuals, in one of which traces of
them are present in the first three somites, and in
the other, in the second somite. In contrast, all
individuals of S. parri bear such sulci. As Burken-
road anticipated, the shape of the posteroventral
margin of the pleuron of the fourth somite, which
is usually concave in S. disparri and convex in S.
parri, is variable, sometimes straight in both
shrimps.
The length of the rostrum is not a reliable diag-
nostic character, as previously suggested, only
tending to be slightly longer in S. disparri than in
S. parri — the ratio rl/cl ranges from 0.43 to 0.59 in
the former and 0.36 to 0.55 in the latter. It does
tend to be deeper, but not consistently, in the
Pacific than in the Atlantic species.
Burkenroad (1938) also pointed out the presence
of a fourth tooth on the dorsal margin of the ros-
trum in four of his specimens of S. disparri, but he
considered this tooth to belong to the apical cluster
(as I have in the meristic data presented here)
when discussing differences in number of apical
teeth between his smaller male and the remaining
four shrimps. The number of apical teeth vary ii*
both species; however, more tend to be present in
S. disparri, 59% of the specimens possess more
than three teeth (57% four, 2% five), whereas in S.
parri 90% of them bear two or three (80% three,
10% two) and only 10% bear four teeth. In S. dis-
parri the rostrum seems always to be armed with
submarginal, movable spinules; their absence in a
few adults is probably due to loss by accident. But
among the specimens of S. parri I have examined,
only one from south of Joao Pessoa, Paraiba,
Brazil, bears a pair of such spinules. Another from
Varadero, Cuba, possesses a single, very minute
spinule located on the ventral margin of the ros-
trum, near the base of the ventralmost apical
tooth.
The shape of the posteroventral margin of the
pleuron of the fourth abdominal somite is vari-
able, as Burkenroad predicted for S. disparri,
sometimes straight in both species, but, as stated
above, the posteroventral extremity is always an-
gular in S. disparri and rounded in S. parri. In the
20
PfiREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
holotype of the former this extremity is sharply
angular but unarmed, contrary to what was stated
in the original description of the species; however, I
have examined a few specimens in which the angle
is produced in a small spine.
Sicyonia disparri is also quite similar to S.
laevigata but the epigastric tooth is larger than
that in the latter, usually almost as large as the
other two teeth on the postrostral carina, and is
located closer to the level of the hepatic spine, i.e.,
farther from the orbital margin, 0.12-0.25 (mean
0.17) cl from it rather than 0.6-0.16 (mean 0.12) cl.
The anteromedian pleural sulcus of the first ab-
dominal somite is always well defined in S. dis-
parri whereas it is absent or, infrequently,
rudimentary in S. laevigata; and the posteroven-
tral extremity of the fourth abdominal somite in
S. disparri is angular rather than rounded. Fur-
thermore, whereas the distal projection of the dor-
solateral lobule of the petasma is conspicuously
curved mesially in S. disparri, it is directed
distally and curved dorsally at its tip in S. laevi-
gata.
The discussion of S. parri is based on 34 speci-
mens, including the holotype (YPM 4395) and one
male from the Bermudas, which represents the
second record of the species from this area. Bur-
kenroad (1938) reported it from the Bermudas, but
his record has not been cited by subsequent au-
thors, including me in my 1980 paper on the west-
ern Atlantic Sicyonia.
Material. — 62 specimens from 20 lots.
Mexico — Baja California Norte: 9, holotype,
YPM 4392, Bahia San Luis Gonzaga, 17 May 1926,
Pawnee. 19, paratype, YPM, Bahia San Luis
Gonzaga, 17 May 1926, Pawnee. 19, AHF, off Isla
Partida, 82 m, 8 March 1936. Baja California
Sur: Id 19, YPM, Bahia Santa Ines, 55 m, 11
April 1936, Zaca stn 142D-1. 66 49, AHF, 1.6 km
WSW of Punta Perico, Isla Carmen, 13-20 m, 21
March 1949, Velero TV. 16 , AHF, Bahia Salinas,
Isla Carmen, 13 m, 20 March 1940, Velero IV. 19 ,
SIO, Bahia Salinas, Isla Carmen, 0.3 m, 13 July
1965, B. W. Walker. 19, CAS, Bahia Balandra,
Isla Carmen, 22 May 1921, F Baker 16, AHF,
Bahia Agua Verde, 18 m, 12 February 1940, Velero
III. 66 89 , SIO, NW of Isla Santa Cruz, 0-3 m, 10
July 1960, B. W. Walker. 26 29, SIO, Isla San
Jose, 3-5 m, 29 March 1967. Id 29 , AHF, Canal de
San Lorenzo, 11-24 m, 14 February 1940. 4d 99,
USNM, off Isla del Espiritu Santo, 15 m, 30 April
1888, Albatross stn 2824. 29, SIO, off Punta
Lobos, 18 m, 26 June 1961, R. Rosenblatt. Id 19 ,
USNM, Bahia La Ventana, 24-27 m, 20 April 1939,
Stranger stn 38. 19, SIO, Ensenada de los Muer-
tos, 9 m, 20 June 1961, R. Rosenblatt. Id , YPM,
off Punta Arena, "Arena Bank," 64 m, Zaca stn
136D-30. Id , SIO, E of Cabo San Lucas, 0-6 m, 12
June 1961, R. Rosenblatt. Nayarit: 19, AHF,
1.6-3 km NW of Mantanchen, 21 December
1961. 19 , AHF, Isla Santa Magdalena, Islas Tres
Marias, 5.5-9 m, 9 May 1939.
Sicyonia mixta Burkenroad, 1946
Figures 12, 18-20
Sicyonia mixta Burkenroad, 1946:3, fig. 1-4
[holotype, d, NR (Stockholm) 2527; type-
locality: "St. Joseph (probably San Jose, Lower
California). Swedish Eugenie Expedition
#818"]. Rodriguez de la Cruz, 1977:11.
Diagnosis. — Antennal spine well developed, pro-
jecting from short but strong buttress. First ab-
dominal somite with dorsomedian carina
uniquely lacking anterior tooth; second abdominal
somite with anterior depression on dorsomedian
carina limited posteriorly by subvertical wall.
First pereopod with basis and ischium unarmed.
Rostrum very short, not surpassing midlength of
eye, bifid and bearing one dorsal tooth. Petasma
with distal projection of dorsolateral lobule
straight, but with tip curved dorsally; distal pro-
jection of ventrolateral lobule bifid, arms curved
inwardly. Thelycum with plate of sternite XIV
convex laterally and with deep median depression.
Description. — Body moderately robust (Fig. 18)
and lacking tubercles. Carapace with long setae on
dorsum, arc anterior to hepatic spine, and patch
accompanying hepatic sulcus ventrally
Rostrum very short, not surpassing midlength
of eye, its length 0.13-0.16 cl; straight; armed with
only one dorsal tooth situated almost at midlength
of rostrum, and two minute apical teeth (tip bifid);
ventral apical tooth located at same level or dis-
tinctly anterior to dorsal apical tooth. Conspicu-
ous adrostral carina, close and subparallel to ven-
tral margin, extending to base of ventral apical
tooth.
Carapace with low postrostral carina ending
markedly anterior to posterior margin of carapace
and bearing three teeth: 1) epigastric tooth, small-
est of three but larger than dorsal rostral tooth,
placed well in advance of hepatic spine, between
0.05 and 0.08 cl from orbital margin; 2) middle
tooth, as large as or slightly larger than posterior
21
FISHERY BULLETIN: VOL. 83, NO. 1
Figure 18. — Sicyonia mixta Burkenroad, 1946, 6 12 mm cl, off Cabo San Lucas, Baja California Sur, Mexico. Lateral
view. Scale = 5 mm.
one, but about twice as high as anterior, situated
posterior to hepatic spine, between 0.30 and 0.33 cl
from orbital margin; and 3) posterior tooth, be-
tween 0.60 and 0.63 cl. Tuft of setae present at
anterior base of each tooth. Antennal spine well
developed, projecting from short buttress; hepatic
spine long, sharp, borne on prominent buttress
arising from swollen hepatic region; branchiocar-
diac carina barely distinct, only for short distance
behind latter region. Postocular sulcus short and
deep anteriorly, continuing posteriorly as well-
defined groove; hepatic sulcus well marked, long,
extending caudally to about level of apex of pos-
terior tooth.
Antennular peduncle with stylocerite produced
in long, acute spine, its length almost or quite
equal to distance between lateral base of first an-
tennular article and mesial base of distolateral
spine; latter sharp, long, reaching as far as distal
margin of second antennular article; flagella rela-
tively elongate, mesial one about 0.20 cl, shorter
than lateral, latter about 0.30 cl.
Scaphocerite reaching or surpassing antennular
peduncle, sometimes by as much as 0.10 its own
length; lateral rib produced distally in long, sharp
spine overreaching lamella; antennal flagella in-
complete in all specimens examined.
22
Third maxilliped stouter than pereopods. Basis
and ischium of first pereopod unarmed.
Abdomen with dorsomedian carina extending
from first through sixth somites, carina weak on
first and second, increasing progressively in
height through sixth; carina on first somite lack-
ing anterior tooth; on second interrupted by
well-marked depression limited posteriorly by
abrupt elevation, situated at level of juncture of
tergal sulci; on fifth descending gradually instead
of truncate posteriorly; and on sixth ending in
large, acute, posterior tooth.
Pleuron of first abdominal somite with antero-
ventral margin slightly concave, anteroventral ex-
tremity rounded and unarmed; posteroventral ex-
tremity of first four somites also rounded, that of
fifth usually bearing minute spine, and that of
sixth always produced in small spine.
First somite with very short but deep anterome-
dian pleural sulcus and relatively weak (similar to
most remaining sulci) but long posterior tergal
(extending 0.60-0.66 height of somite). Second and
third somites bearing short anterior and quite
long posterior tergal sulci. Fourth somite with
long posterior tergal sulcus, but anterior tergal
almost indistinct. Fifth somite with barely dis-
tinct anterior tergal and relatively short posterior
pfiREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
FIGURE 19.
-Sicyonia mixta , 6 12 mm cl, off Cabo San Lucas, Baja California Sur, Mexico. A , Petasma, dorsal view; B , ventral
view of same; C, right appendix masculina, dorsolateral view. Scale = 1 mm.
tergal, and sixth bearing weak anterior tergal and
arched posteromedian pleural sulci.
Telson with paired fixed spines extremely mi-
nute (in the only specimen examined by me in
which they are present). Rami of uropod, subequal
in length, falling slightly short of apex of telson.
Petasma (Fig. 19A, B ) with rigid distal projec-
tion of dorsolateral lobule bearing rounded prox-
imodorsal prominence, extending almost straight
distally but with tip curved dorsally Distal projec-
tion of ventrolateral lobule bifid (arms curved),
inclined laterally, and falling considerably short of
adjacent projection.
Appendix masculina as illustrated in Figure
19C.
Thelycum (Fig. 20) with plate of sternite XIV,
delimited by rounded lateral margins, raised in
paired bulges sloping towards deep median de-
pression. Median plate of sternite XIII roughly
flaskshaped in outline, tapering into long, slender
spine reaching proximal extremity of basis of an-
teriorly extended second pereopods; posterior
component of plate with arched posterior borders
flanking shallow to deep, broad median emargina-
tion, and traversed by strongly incised suture.
Sternite XI armed posteriorly with paired, mod-
erately long, acute spines. Posterior thoracic ridge
with sharp, concave, anteromedian margin over-
FIGURE 20. —Sicyonia mixta, 9 13 mm cl, off Isla T^boga, Golfo
de Panama, Panama. Thelycum. Scale = 1 mm.
23
FISHERY BULLETIN: VOL. 83, NO. 1
lapping plate of sternite XIV but areas im-
mediately lateral to it flush with preceding plate.
Color. — The specimen examined by me from Peru
exhibits a dark colored mask in the shape of a "2"
(the base situated anteriorly), disposed hori-
zontally from the posterolateral part of the
carapace onto the anterodorsal part of the first
abdominal pleuron.
Maximum size. — Male 12.7 mmcl, about 43.5 mm
tl; female 20 mm cl, 65.5 mm tl.
Geographic and hathymetric ranges. — In addition
to the undetermined type-locality, "St. Joseph"
(most probably San Jose, Baja California), it has
been found in Bahia Aimejas (24°29'18"N,
111°47'24"W) and off Cabo San Lucas, both on the
ocean side of Baja California Sur, in Bahia de la
Paz, on the eastern side of the latter, off Isla
Taboga in the Golfo de Panama, and off Puerto de
Eten (6°22'S, 80°47'W), Peru (Fig. 12). Sicyonia
mixta occupies shallow water at depths between 11
and 24 m.
The discovery of S. mixta first in the Golfo de
Panama and more recently northwest of Puerto de
Eten, Peru, was surprising and represented a con-
siderable extension of the range of the species.
F*reviously, it was known only from the waters of
Baja California, where the three male types were
collected and where, in Bahia de la Paz, five
females and a male were found (Rodriguez de la
Cruz 1977). The specimen from off Puerto de Eten
(a female 20 mm cl, 26.5 mm tl ) was collected by M.
Niquen from the RV Humboldt on 27 April 1983,
and is deposited in the IMARPE.
Discussion. — As Burkenroad (1946) stated, S.
mixta is unique in lacking a tooth on the anterior
end of the dorsomedian carina of the first abdomi-
nal somite. Also this shrimp exhibits two of the
basic characters of the species that Burkenroad
(1934a) grouped in his Division II (the presence of
a well -developed or clearly distinct antennal spine
and the absence of basial and ischial spines on the
first pereopod) at the same time that the dorsome-
dian carina of the second abdominal somite, al-
though not incised, is abruptly depressed an-
teriorly. This depression seems to represent the
deep incision or notch typical of the species of his
Division I.
Among the American species (excluding those
grouped in Division I), S. mixta, S. disedwardsi,
S. penicillata, and two western Atlantic species
24
— S. typica (Boeck 1864) and sometimes S. olgae
Perez Farfante, 1980 — possess three dorsal teeth
on the postrostral carina, two of which are situ-
ated posterior to the hepatic spine. In S. mixta,
however, the posterior tooth arises on the post-
rostral carina considerably in advance of the pos-
terior margin of the carapace, and the carina ends
markedly anterior to the margin; in the other
species the tooth arises nearer the margin where
the carina ends. Sicyonia mixta also differs strik-
ingly from the other four in the general sculp-
ture of the abdomen; whereas in S. mixta it is not
tuberculate and lacks all pleviral sulci except the
anteromedian on the first somite and the postero-
median on the sixth, in these congeners the ab-
domen is strongly tuberculate, exhibits deeper
sulci, and possesses pleural sulci and all sixth so-
mites. The bifurcate shape of the terminal part
of the distal projection of the ventrolateral lob-
ule of the petasma is another character that dis-
tinguishes S. mixta from the just mentioned rela-
tives.
The relationships of this species are rather
puzzling. Except for the distinctly depressed dor-
somedian carina of the second abdominal somite,
it does not share any other characters of impor-
tance with the species of Division I, represented by
S. disparri, S. laevigata, and S. parri. Actually, it
appears to be much closer to the group represented
in the eastern Pacific by S. disedwardsi and S.
penicillata, for in addition to possessing an anten-
nal spine and lacking spines on the basis and is-
chium of the first pereopod, like them, it is armed
with two teeth on the postrostral carina posterior
to the hepatic spine. It seems to me that S. mixta
has had, although remotely, a common origin with
the above-mentioned group.
Remarks. — Because females of this shrimp have
not been known previously, the above description
of the thelycum is the first available for this
species. In addition to the females cited from the
Golfo de Panama and off northern Peru, two other
new records are presented here: one represented
by a male from off Cabo San Lucas, Baja Califor-
nia Sur, and the other by a female from Bahia
Aimejas, Gulf of California. These four specimens,
the types, and the six reported by Rodriguez de la
Cruz (1977) are the only ones that have been re-
corded for this shrimp.
The holotype of this species and the paratype, in
the Naturhistorisches Museum (Vienna), are the
only extant types of the Sicyonia treated here that
were not examined by me.
PfeREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
Material. — 5 specimens from 5 lots.
Mexico— Id paratype, ZMB 6097, "California.
Forrer" (?Ferrer). Baja California Sur: 16,
SIO, Bahia Almejas, 11-24 m, 30 November 1961, F.
H. Berry. IS , CAS, off Cabo San Lucas, 6 August
1932, Zaca stn D-21R.
Panama— 19, USNM, off Isla Taboga, Golfo de
Panama, 10 March 1969, H. A. Clarke and A.
Rodaniche.
Peru— 19, IMARPE, off Puerto de Eten, 27
April 1983, M. Niquen, Humboldt, stn 8304, haul
175.
Sicyonia hrevirostris Stimpson 1871
Figures 21-25
Sicyona cristata. de Saussure 1857:306. [Not
Hippolyte cristata De Haan 1844:194 = Sicyonia
cristata (De Haan 1844).]
Sicyonia hrevirostris Stimpson 1871:132 [syntypes
not extant; type-locality: S. Florida coast].
Kingsley 1878:69. Faxon 1896:162. De Man
1911:10. Pesta 1915:118. Hay and Shore
1918:380, pi. 25, fig. 4. Hedgpeth 1953:160.
Hildebrand 1954:268, 1955:220. Menzel 1956:
41. Lunz 1957:4. Anderson 1958:1, fig. 5.
Eldred 1959:5. Gunter and McCaughn 1959:
1194. Anderson 1962:1, fig. 15. Kutkuhn
1962:2. Chapa Saldaha 1964:4. Joyce 1965:
132. Cerame-Vivas and Gray 1966:263.
Joyce 1968:254, unnumbered fig. Rouse
1969:136. Bayer et al. 1970:41. Zyznar
1970:87. Brusher et al. 1972:75. Cain
1972:79. Franks etal. 1972:54. Allen 1973:1.
Cobb et al. 1973:7, fig. 3, 4A-C. Day et al.
1973:36. Bryan and Cody 1975:1. Brusher
and Ogren 1976:158. Hooks et al. 1976:103.
Kennedy et al. 1977:1. Perez Farfante
1978: Sicyoniidae. Huff and Cobb 1979:51.
Wenner and Boesch 1979:130. Holthuis
1980:58. Perez Farfante 1980:772. Soto
1980a:68, 1980b:84. Castille and Lawrence
1981:519. Wenner and Read 1981:4. Arre-
guin Sanchez 1981:21. Perez Farfante 1982:
370. Wenner and Read 1982:181. Williams
1984:43.
Eusicyonia edwardsi. Hay and Shore 1918, pi. 25,
fig. 2. [Not Sicyonia edwardsii Miers 1881:367
= Sicyonia typica Boeck 1864.]
Eusicyonia hrevirostris. Burkenroad 1934a: 84,
1934b:117, 1939:57. Lunz 1945:4. Anderson
et al. 1949:16. Anderson 1956:2. McConnell
1960:52.
Vernacular names: rock shrimp, hardback
(United States); camaron de piedra, camaron
conchiduro, camaron de roca (Mexico). FAO
names (Holthuis, 1980): rock shrimp (English);
camaron de piedra (Spanish); boucot ovetger-
nade (French).
Cobb et al. (1973) and Huff and Cobb (1979)
presented extensive bibliographic references to
this species, many of which are omitted from the
above synonymy.
Diagnosis. — Antennal spine well developed and
projecting from strong buttress. Second abdominal
somite with dorsomedian carina lacking incision.
First pereopod with basis and ischium unarmed.
Postrostral carina bearing three teeth posterior to
level of hepatic spine, rarely anterior one of these
at level of or slightly anterior to hepatic spine.
Rostrum armed with two dorsal teeth (rarely
three). Petasma with distal projection of dorsolat-
eral lobule relatively short, its apical part curved
dorsally. Thelycum with plate of sternite XIV al-
most flat or slightly raised laterally in paired low
bulges; posterior component traversed by well-
marked suture. Branchiostegite lacking large spot
or ocellus.
Description. — Body robust (Fig. 21). Carapace
with dorsum covered by densely set, short setae;
also patches of setae present anterior and ventral
to hepatic spine, subjacent to hepatic sulcus and to
branchiocardiac carina, and band of smaller setae
on ventral part of branchiostegite. Patches also
present on terga of abdominal somites. Abdomen
heavily or moderately tuberculate, tubercles
small, more numerous on first four somites.
Rostrum short, in young not overreaching distal
end of second antennular article, in adults falling
considerably short of distal margin of eye, its
length increasing linearly with carapace length
(Fig. 22), to about 16 mm cl, then growing little,
rarely surpassing 6 mm (proportional length de-
creasing with increasing size from as much as 0.49
to as little as 0.15 cl); subhorizontal or upturned as
much as 85°, tapering from base to tip, and armed
with two (very rarely three) dorsal and two or
three (four in one) apical teeth; latter subequal or
ventral one extending farther anteriorly than dor-
sal and often upturned; when two teeth present,
knob usually between them. Adrostral carina
strong, bordering ventral margin and reaching
end of rostrum.
Carapace with postrostral carina high, bearing
25
FISHERY BULLETIN; VOL. 83, NO. 1
Figure 21. — Sicyonia brevirostris Stimpson,(5 18.1 mm cl, off Puerto Madero, Chiapas, Mexico. Lateral view. Scale
= 5 mm.
Figure 22. — Sicyonia brevirostris. Relationship be-
tween rostrum length and carapace length (regression
equation for specimens with carapace length less than
about 16 mm, V = 0.52372 + 0.33342;t:; regression equa-
tion for those larger, >> = 5.06145 + 0.01211x).
T*
c
^ 4
E
3
•
•
■
•
•
•
•• •
•
•
• •
•
•
•
/:\-
•
%r*: ••.
•
•
;
•.
•
• •
•
•
/
/
•
••
/?
16 24 32
carapace length (mm)
40
four teeth: 1) epigastric tooth only slightly larger
than first rostral, situated from anterior to orbital
margin to as much as 0.1 cl posterior to it; and 2)
three large teeth usually placed posterior to level
of hepatic spine, anterior one (level with hepatic
spine in only three specimens examined) smallest,
situated between 0.20 and 0.28 (mean 0.25) cl from
26
orbital margin, middle tooth between 0.52 and
0.60 (mean 0.55) cl, and posterior one between 0.74
and 0.79 (mean 0.75) cl. Antennal spine moder-
ately long, projecting from strong buttress; hepa-
tic spine, longer than antennal, acutely pointed
and arising from moderately raised area between
0.20 and 0.25 (mean 0.23) cl from orbital margin.
P6REZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
Postocular sulcus with anterior part deep, con-
tinuing posteriorly as shallow groove; hepatic sul-
cus well marked; hepatic carina weak; bran-
chiocardiac carina conspicuous, extending to or
almost to transverse ridge near posterior margin
of carapace.
Antennular peduncle with stylocerite produced
in long, sharp spine, its length 0.85-0.90 distance
between lateral base of first antennular article and
mesial base of distolateral spine; latter extending
as far as distal end of proximal 0.80 of second
antennular article; antennular flagella short, me-
sial antennular flagellum shorter than lateral,
0.15-0.20 as long as carapace, lateral flagellum
0.19-0.23 as long.
Scaphocerite reaching or slightly overreaching
distal margin of antennular peduncle; lateral rib
ending distally in long, acute spine distinctly
overreaching margin of lamella. Antennal flagel-
lum about twice as long as carapace.
Third maxilliped stouter than pereopods. Basis
and ischium of first pereopod unarmed.
Abdomen with high dorsomedian carina ex-
tending from first through sixth somites: on first
produced in strong anterior tooth, on fourth usu-
ally sloping posteriorly but sometimes abruptly
truncate, and on fifth and sixth terminating in
sharp tooth, latter longer.
Anterolateral margin of pleuron of first abdom-
inal somite concave, anteroventral extremity of
first through fourth somites ending in spine, that
of first directed anterodorsally, those of second
through fourth curved posterolaterally; postero-
ventral extremity of fourth through sixth somites
bearing posteriorly directed, acute spine, that of
fifth largest. Pleural spination of first four somites
represented by tubercles in juveniles, becoming
longer with increasing length of carapace.
First abdominal somite with long anteromedian
pleural sulcus ending dorsally at anterior margin
of tergum and converging with long posterome-
dian pleural sulcus ventrally; posterior tergal sul-
cus long or short, well marked or weak; posterior
pleural sulcus well defined. Second and third so-
mites with long anterior and posterior tergal sulci;
anteromedian pleural sulcus continuous with an-
teroventral depression setting off prominence dor-
sally and ridge posteriorly; posterior pleural sul-
cus as on first somite. Fourth and fifth somites
with anterior tergal joining curved, united pos-
terior tergal-posteromedian pleural sulci dorsally;
fourth also with shallow but clearly distinct
caudodorsal depression, placed close to posterior
margin. Sixth somite marked with faint anterior
tergal and arched posteromedian pleural sulci,
also bearing longitudinal ridge along base of dor-
somedian carina and lateral depression (thickly
covered with setae) dorsal to interrupted cicatrix.
All sulci weak in juveniles, becoming deeper with
age.
Telson with pair of short, often abraded, fixed
subterminal spines. Rami of uropod subequal in
length, reaching or slightly overreaching apex of
telson.
Petasma (Fig. 23A, B) with rigid distal projec-
tion of dorsolateral lobule raised proximodorsally
in rounded prominence, strongly curved dorsome-
sially, its distal part compressed, rounded ven-
trally, produced dorsally in short, subacute salient;
mesial base of projection bearing short, dentiform
prominence. Distal projection of ventrolateral
lobule with firm terminal part curved laterally,
convex dorsally, plane ventrally, and tapering to
ventrally directed apex.
Petasmal endopods coupled in males as small as
6.3 mm cl, about 22 mm tl, but in individuals with
as much as 13 mm cl, about 48 mm tl, they may not
be joined.
Appendix masculina as illustrated in Figure
23C.
Thelycum (Fig. 24) with plate of sternite XIV
produced in anterolateral lobules, almost flat or
raised in paired low bulges sloping toward an-
teriorly deep median depression. Median plate of
sternite XIII sagittiform, tapering gradually into
long, slender spine reaching as far as proximal
0.25 of basis of extended second pereopods; plate
strongly excavate and bearing shallow, lateral in-
cisions at level of fourth pereopods; posterior com-
ponent with deep, broad posteromedian emargina-
tion separating paired subtriangular processes
limited anteriorly by well-marked transverse su-
ture. Paired spines projecting anteroventral ly
from posterior margin of sternite XI, spines broad
basally, often spiculiform apically. Posterior
thoracic ridge narrow, with concave anteromedian
margin well marked.
The smallest impregnated females encountered
have a carapace length of 10 mm, about 44 mm tl.
Color. — The coloration of this shrimp was de-
scribed in detail from live specimens from the Gulf
of Mexico by Burkenroad (1939). Williams (1965)
presented notes on the color of materials of North
Carolina, and Cobb et al. (1973) recorded observa-
tions on individuals from the Yucatan shelf. In the
latter, the dorsal part of the body is more reddish
than in specimens from the northern Gulf of
27
FISHERY BULLETIN: VOL. 83, NO. 1
«
Figure 23. — Sicyonia brevirostris , 18.1 mm cl, off Puerto Madero, Chiapas, Mexico. A, Petasma, dorsal view;
B, ventral view of same; C, right appendix masculina, dorsolateral view. Scales = 1 mm.
FIGURE 2A.— Sicyonia brevirostris, 9 26.3 mm cl, off Cape Lookout,
North Carolina, USA. Thelycum. Scale = 2 mm.
28
P6REZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
Mexico, which Burkenroad described as having
the dorsum brown and the sides white, and also
differs from shrimp occurring in North Carolina,
in which the ground color is off-white.
Maximum size. — According to Holthuis (1980),
153 mm tl. Largest individuals examined by me:
males 32 mm cl, about 125 mm tl; females 37 mm
cl, about 130 mm tl. The only specimen from the
Pacific, a male from off Puerto Madero, Chiapas,
Mexico, measures 18.1 mm cl, 70 mm tl (latter from
Burkenroad 1934a).
Geographic and bathymetric ranges. — In the east-
ern Pacific, off southern Mexico, from Colima
(Chapa Saldaha 1964) to Chiapas (Fig. 25). In the
western Atlantic, from Norfolk, Va., along the
coast of the United States and the Bahamas to the
southern coast of Cuba, and around the Gulf of
Mexico from the Florida Keys to off Isla Contoy,
Yucatan; perhaps also off Guyana (McConnell
1960). In the western Atlantic it occurs from shal-
low water to 329 m (Williams 1965), usually be-
tween 10 and 110 m, and rarely at depths >190 m.
Exploitable populations are found between 34 and
55 m (Huff and Cobb 1979).
This species prefers sand and shell-sand sub-
strates, but occasionally it is found on mud bot-
toms (Hildebrand 1954, 1955; Menzel 1956; Wil-
liams 1965; Cobb et al. 1973; Kennedy et al. 1977;
Huff and Cobb 1979). The depths and substrates
with which it was associated in the eastern Pacific
were not recorded.
Discussion. — Sicyonia brevirostris is rather
closely related to the western Atlantic S. typica
and the eastern Pacific S. disedwardsi . It differs
from both in possessing three, instead of two, large
teeth on the postrostral carina posterior to the
level of the hepatic spine and a caudodorsal de-
pression on the fourth abdominal somite. It differs
further from S. disedwardsi in 1) exhibiting
well-marked posterior pleural sulci on the first
three abdominal somites, which are lacking in the
latter shrimp or, if present, weak, often distinct on
only one or two somites; 2) having the distal pro-
jection of the dorsolateral lobule of the petasma
turned dorsomesially, compressed distally, and
produced apically in a short, subacute, dorsally
directed salient — in contrast, in S. disedwardsi
the projection is turned mesially and then dor-
solaterally, its apical extremity produced in a rela-
tively elongate, acutely pointed, laterally directed
salient which often bears a crest; and 3) lacking
an ocellus on the posterior part of the branchioste-
gite rather than bearing a large, brightly colored
one such as that in S. disedwardsi.
Sicyonia brevirostris occupies water of high sa-
20
10
100
Figure 25. — Geographic distribution of Sicyonia brevirostris.
29
FISHERY BULLETIN: VOL. 83, NO. 1
Unity; recorded off east Florida and off west cen-
tral Florida in salinities between 32.00 and
36.75%o and 31.22 and 36.71%o (Kennedy et al. 1977
and Huff and Cobb 1979, respectively) and off Mis-
sissippi between 27.8 and 34.6%.. (Franks et al.
1972). Only once, in the Chatham River, Fla., has
it been recorded in an estuarine environment, at a
salinity of 24%o (Rouse 1969). The specimens on
which this record is based consisted of larvae and
small juveniles, and might have been misiden-
tified, perhaps belonging to one of the other con-
geners found in that area. This shrimp, unlike
other penaeoids, does not depend upon estuarine
waters during its life cycle (Eldred 1959; Joyce
1965).
Many investigators (Lunz 1957; Joyce 1965;
Brusher et al. 1972; Cobb et al. 1973; Brusher and
Ogren 1976; Camp et al. 1977; Kennedy et al. 1977;
Huff and Cobb 1979; Wenner and Read 1981) note
that this species is predominantly nocturnal. Cobb
et al. (1973) suggested that it burrows into the
substratum during the day, thereby avoiding pre-
dation and capture by trawls.
Notes on biology and abundance. — Whereas the
other American rock shrimps have been largely
neglected, because of its considerable economic
value, large size, and ready availability S. bre-
virostris has been the subject of a number of inves-
tigations. Cobb et al. (1973) and Kennedy et al.
(1977) studied the reproductive cycle (including
ovarian development in detail) of west central and
east Florida populations, respectively They con-
cluded, as did Huff and Cobb (1979) who investi-
gated the former population, that spawning and
recruitment seem to occur throughout the year,
with a peak of spawning from October to February
off the west coast of Florida and during winter and
early spring off the northeast coast. Cobb et al.
(1973) suggested that a decrease in the daily
photoperiod was responsible for the onset of
spawning.
Morphometric studies by Kennedy et al. (1977)
demonstrated that increase in total length occurs
at the same rate in males as in females until they
reach 20 mm cl, then the rate of increase of total
length in females become less. They also found
that the juveniles grow at an average rate of 2-3
mm cl per month whereas the adults grow at 0.5-
0.6 mm cl. It was also estimated by them that the
life span of this species is 20-22 mo. More re-
cently Arreguin Sanchez (1981) presented biologi-
cal fishery statistics (length/weight, growth, mor-
tality, etc.) for this species.
Density of this shrimp in various populations
fluctuates seasonally. Wenner and Read (1981,
1982) found that S. brevirostris is the dominant
species of decapod crustacean on the continental
shelf between Cape Fear, N.C., and Cape Canav-
eral, Fla., and that highest densities occurred in
one summer of their 2y2-yr study. Lunz (1957)
noted a bimodal seasonal abundance off South
Carolina, with peaks occurring from September
through December and again in May. Kennedy et
al. (1977) observed that peak abundance is reached
during the fall in the east Florida population. In
the Gulf of Mexico, off central Florida (Cobb et al.
1973; Huff and Cobb 1979), maximum abundance
was found to exist from late summer through the
fall. Off Apalachicola, Fla., (Allen 1973) highest
densities seem to occur from June to October; in
coastal water of Louisiana (on the basis of
maximum production) and Texas (Brusher et al.
1972), from June through January, and in Bahia
de Campeche (Hildebrand 1955) this species was
more abundant in February than in July. It thus
appears that throughout the range of this species
maximum abundance occurs from summer
through fall, and, in some areas, into early winter.
Kutkuhn (1962) calculated regression equations
for predicting "headless" from "whole" weights and
vice versa, and Cobb et al. (1973) presented equa-
tions for relating carapace length to total length
for males and females, as well as others for
carapace length and total weight for males and
females, and for both sexes combined. Huff and
Cobb (1979) also calculated the relationships of
carapace length to total length and carapace
length to weight for each sex.
Commercial importance . — Commercial fishing for
S. brevirostris began in the United States in 1970
(Allen 1973) and since then production has in-
creased noticeably, amounting to 3,351,000 lb,
with a value of $3,222,000 in 1982 (Table 1). The
fishing grounds are located off the southeast coast
from North Carolina to central Florida (the most
Table l. — Landings of Sicyonia brevirostris
by areas and their values for 1982.'
Area
Pounds (heads-off)
Dollars
Georgia
East Florida
West Florida
Texas
Total
369.000
1.980.000
1.001.000
1,000
3,351.000
353,000
1 ,869,000
999.000
1,000
3,222.000
'Data provided by tlie Southeast Fisheries Center
Statistical Survey Division, National Marine Fisheries
Service, NCAA, Miami, Fla
30
PfeREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
important ones by far being those off Cape Canav-
eral and Fort Pierce), and in the Gulf of Mexico off
the coast of Florida (those off Apalachicola and
Pensacola the most productive of the entire region)
and western Texas. The production of the Caroli-
nas was insignificant in 1982, last year for which
landings are available.
This species is also exploited in Mexico off Isla
Contoy, Quintana Roo, and in Bahia de Campeche.
Arreguin Sanchez (1981) estimated that until
1978-79 the fishery off Isla Contoy, under optimal
conditions, could have produced as much as 450 t
(992,070 lb) of heads-on shrimp.
Remarks. — This species was first recorded from
the eastern Pacific by Burkenroad (1934a). His
record was based on a single specimen reportedly
taken by the Pawnee off southern Mexico, in the
Gulf of Tehuantepec, at lat. 14°40'20"N, long.
92°40'30"W. Later, Chapa Saldaha (1964) recorded
five lots of this shrimp from the coast of Oaxaca,
Golfo de Tehuantepec, which were in the collec-
tions of the Institute Nacional de Investigaciones
Biologico-Pesqueras, Mexico. Unfortunately, these
specimens are no longer extant (Concepcion Ro-
driguez de la Cruz^). Presence of S. brevirostris has
not been confirmed by subsequent investigations
in the region, including that of Sosa Hernandez et
al. (1980), who conducted a survey of the decapod
crustaceans in the general area from which Bur-
kenroad's and Chapa Saldaha's materials were ob-
tained. Furthermore, representatives of the
species were not found in the large collections of
penaeoids from the Pacific coast of Mexico and
Central America examined by me. Because of the
large size of this shrimp (it may reach 153 mm), it
should have been retained by the commercial
shrimp trawls or other gear used off southern
Mexico. The surprising fact that it has not been
recorded from commercial catches since the ap-
pearance of Chapa Saldana's report nor from col-
lections resulting from exploratory work raises
the possibility that the specimens cited above
either bear incorrect data (as might be true of the
correctly identified specimen examined by Bur-
kenroad) or were misidentified.
McConnell (1960) reported this species from
Guyana, but because it has not been recorded in
studies (including my own) made of large collec-
tions of penaeoids obtained by research vessels and
"Concepcion Rodriguez de la Cruz, Institute National de
Pesca, Secretaria de Pesca, Mexico, D.F., Mexico, pers. commun..
May 1983.
shrimp trawlers in the waters of that country or in
any others south of Cuba, its presence there needs
confirmation.
This is the only species for which full biblio-
graphic references are not given. Because of its
abundance, accessibility, and economic value, the
literature on this shrimp is extensive. As stated
above, much of it is cited in the works of Cobb et al.
(1973) and Huff and Cobb (1979), consequently, I
am including those references in which synonyms
were created, articles not cited by them, others
which appeared subsequent to their contributions,
and all of those cited in the treatment below.
Material. — 281 specimens from 66 lots.
Eastern Pacific — 1 specimen.
Mexico — Chiapas: Id, YPM, off Puerto Madero,
9 April 1926, Pawnee.
Western Atlantic — 280 specimens from 64 lots.
United States — North Carolina: 45 29,
USNM, off Rodanthe, 49 m, 20 October 1884, Al-
batross stn 2296. 14(? 129 , USNM, off Cape Hat-
teras, 64 m, 21 June 1957, Combat stn 396. 19,
USNM, NE of Cape Hatteras, 55 m, 26 July 1969,
Oregon II stn 10697. 36 39, USNM, off Raleigh
Bay, 26 m, 30 July 1969, Oregon II stn 10738. 26
69, USNM, off Raleigh Bay, 33 m, 27 May 1962,
Silver Bay stn 4028. Id, USNM, SE of Cape
Lookout, 37 m, 12 March 1961, Silver Bay stn
2913. 39, USNM, off Cape Lookout, 43 m, 21
June 1957, Combat stn 397. Id 39, USNM,
Onslow Bay, 46 m, 2 August 1962, Silver Bay stn
4196. South Carolina: 2d , USNM, off Port
Royal Sound, 51-44 m, 25 June 1957, Combat stn
428. Id 19, USNM, off Hilton Head Island, 40-46
m, 7 October 1957, Combat stn 514. 39, USNM,
off Hilton Head Island, 64 m, 14 December 1961,
Silver Bay stn 3657. Georgia: 3d, USNM, off
Cape Romain, 1941, J. Oney 19, USNM, off
Sapelo Island, 42 m, January 1940, Pelican. 49,
USNM, NE of Savannah Beach, 40 m, 4 February
1940, Pelican . 6d 99 , USNM, off Jekyll Island, 73
m, 15 March 1940, Pelican. Florida: Id 29,
USNM, NE of Fernandina, 31 m, 2 October 1951,
Combat stn 505. Id 29, USNM, off Fernandina,
42 m, 10 March 1976, George M. Bowers stn
37. 3d 39, USNM, off Ponte Vedra Beach, 24 m,
23 April 1956, Pelican stn 32. 4d 19, USNM, off
St. Augustine, 329 m, 16 September 1956, Combat
stn 119. Id , USNM, off Matanzas Inlet, 183 m, 18
November 1965, Oregon stn 5741. 13d 229,
31
FISHERY BULLETIN: VOL. 83, NO. 1
USNM, off Flagler Beach, 40 m, 7 November 1963,
Silver Bay stn 5201. 25 89, USNM, off Edge-
water, 22 m, 1 December 1961, Silver Bay stn
3588. 16, USNM, off Cape Canaveral, 25
January 1962, Silver Bay stn 3704. 19, USNM,
off Cape Canaveral, 70 m, 16 January 1966, Ore-
gon stn 5860. 36, USNM, off Melbourne Beach,
40 m, 23 March 1956, Pelican stn 14. 56 59,
USNM, off Hutchinsons Island, 63 m, 11
November 1963, Silver Bay stn 5267. 26 69,
USNM, NE of St Lucie Inlet, 38-42 m, 21 May
1968, Gerda stn 1002. 26 29, USNM, off Key
Largo, 110-113 m, 26 January 1966, Gerda stn
769. 16, USNM, S of Islamorada, 49-40 m, 15
September 1965, Gerda stn 756. 26 59 , USNM, S
of Pine Island, 170-194 m, 25 February 1969,
Gerda stn 1023. 16 29, USNM, S of Marathon,
57-69 m, 26 February 1969, Gerda stn 1030. 16
19, USNM, NW of Marquesas Keys, 27 m, 28 May
1952, Oregon stn 562. 16 39, USNM, SE of Dry
Tortugas Islands, 59 m, 13 April 1965, Gerda stn
574. 16 89 , USNM, S of Dry Tortugas Islands, 68
m, 13 April 1954, Oregon stn 1004. 26 69 , USNM,
S of Dry Tortugas Islands, 64 m, 12 April 1965,
Gerda stn 566. 16 , USNM, SW of Dry Tortugas
Islands, 91 m, 8 March 1970, Gerda stn 1241. Id
49, USNM, NW of Dry Tortugas Islands, 55 m, 18
June 1956, Oregon stn 1553. Id, W of Dry Tor-
tugas Islands, 37 m, 7 March 1970, Gerda stn
1235. 16, USNM, off Appalachee Bay, 27 m, 9
March 1954, Oregon stn 905. 19, USNM, off St
George Island, 37-35 m, 26 July 1957, Silver Bay
stn 88. 29 , USNM, off St George Island, 68 m, 10
March 1954, Oregon stn 916. 19, USNM, S of
Apalachicola Bay, 64 m, 7 March 1954, Oregon stn
896. 16, USNM, off Grayton Beach, 43 m, 16
November 1952, Oregon stn 707. Alabama:
16, USNM, off Orange Beach, 37 m, 24 January
1957, Oregon stn 1651. 56 49, USNM, off
Dauphin Island, 70 m, 9 August 1950, Oregon stn
82. Louisiana: 16 , USNM, off Beeton Sound,
40 m, 21 August 1962, Oregon stn 3713. 19,
USNM, S of Mississippi Delta, 84 m, 12 September
1950, Oregon stn 101. 29, USNM, off Southwest
Pass, Mississippi Delta, 60 m, 14 September 1980,
Oregon stn 110. 16 19, USNM, off Ship Shoal
Lighthouse, 37-40 m, 12 September 1962, Oregon
stn 3186. 19 , USNM, off Pelican Island, 22 m, 8
March 1957, Oregon stn 1755. Texas: 66 62,
USNM, SE of Galveston, 20 m, 6 May 1938, Peli-
can. 59, USNM, S of Galveston, 18 m, 5 May
1938, Pelican. 69 , SW of Galveston, 16 m, 5 May
1938, Pelican. 19 , USNM, NE of Brownsville, 26
m, 5 February 1939, Pelican.
32
Mexico— Tabasco: 16 19, USNM, off Paraiso,
35 m, 16 May 1954, Oregon stn 1057. 19 , USNM,
off Laguna Machona, 64 m, 16 May 1954, Oregon
stn 1060. 19 , USNM, NW of Punta Frontera, 60
m, 8 June 1970, Oregon II stn 10981. 36 39,
USNM, NW of Punta Frontera, 66 m, 9 June 1970,
Oregon II stn 10982. Campeche: 26 , USNM, N
of Arrecifes Triangulos, 64 m, 17 August 1951,
Oregon stn 411. 16 , USNM, W of Cayos Areas, 66
m, 16 June 1970, Oregon II stn 11005. 16 , USNM,
E of Cayos Areas, 37 m, 11 December 1952, Oregon
stn 720. 19, USNM, NE of Cayos Areas, R.
Ramirez and M. Flores, 48 m, 30 April 1959. 36
19, USNM, NE of Cayos Areas, 42 m, 10 December
1952, Oregon stn 719. Id 29, USNM, 16 km, NE
of Ciudad del Carmen, R. Ramirez and M. Flores,
29-37 m, 29 April 1959. 19, USNM, off Cam-
peche, 13 m, 2 May 1959, R. Ramirez and M. Flores.
Sicyonia disedwardsi (Burkenroad 1934)
Figures 3, 7, 26-30
Eusicyonia disedwardsi Burkenroad 1934a:86, fig.
23, 29, 34 [holotype: d, YPM 4394; type-local-
ity: Bahia Concepcion, Baja California Sur, 3
May 1926, Pawnee]. Burkenroad 1938:82.
Anderson and Lindner 1945:317. Castro
1966:17.
Sicyonia disedwardsi. Brusca 1973:219. Rosales
Juarez 1976:41. Rodriguez de la Cruz
1977:11. Anonymous 1980:6. Brusca 1980:
256. Perez Farfante 1982:371.
Vernacular names: rock shrimp, target shrimp,
Japanese shrimp (United States); cacahuete,
camaron de piedra, camaron de roca, camaron
japones (Mexico); camaron conchiduro (Mexico,
Panama).
Diagnosis. — Antennal spine well developed and
buttressed. Second abdominal somite with dor-
somedian carina lacking incision. First pereopod
with basis and ischium unarmed. Postrostral
carina bearing two teeth posterior to level of
hepatic spine. Rostrum armed with two dorsal
teeth. Petasma with distal projection of dorso-
lateral lobule short, stout, curved dorsomesially
then laterally. Thelycum with plate of sternite
XIV raised in relatively low, sometimes indistinct
bulges; posterior component traversed by faint su-
ture. Branchiostegite with large ocellus consisting
of well-defined yellow center surrounded by
purplish brown ring.
P6REZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
Figure 26.— Sicyonia disedwardsi (Burkenroad 1934),? 34 mm cl, Golfo de Panama, Panama. Lateral view. Scale = 10 mm.
Description. — Body robust (Fig. 26). Carapace
studded with long setae anterior to hepatic spine
and in pterygostomian region; patches of densely
set shorter setae present on dorsum, in depression
anterior to posterodorsal part of branchiocardiac
carina, on branchiostegite, and subjacent to hepat-
ic sulcus; patches also on tergum of abdominal
somites and in depression just ventral to dorsal
ridge of sixth somite. Abdomen bearing numerous
tubercles on all somites (especially first three),
except few or none on sixth.
Rostrum short, reaching distal margin of eye at
most, its length increasing linearly with carapace
length (Fig. 27) to about 20 mm cl, then growing
little, not surpassing 6 mm (proportional length
decreasing with increasing size from as much as
0.43 to as little as 0.13 cl); subhorizontal or up-
turned to as much as 45° (in young), tapering con-
siderably from base to truncate, sometimes de-
curved tip; armed with two dorsal and two (96%) or
three (4%) apical teeth. Adrostral carina, situated
close to ventral margin, extending to end of ros-
trum.
Carapace with well-marked postrostral carina
bearing three teeth: 1) epigastric small, only
slightly larger than first rostral, situated from
slightly anterior to orbital margin to 0.07 cl be-
hind it; 2) middle tooth, larger than epigastric,
placed well posterior to hepatic spine, between
0.29 and 0.38 (mean 0.33) cl from orbital margin;
and 3) posterior tooth, larger than middle one,
acutely pointed (usually abraded in larger adults),
rising almost vertically before turning anteriorly
or, more often, strongly inclined anteriorly, and
situated between 0.68 and 0.80 (mean 0.72) cl from
orbital margin; tuft of setae present at anterior
base of all three teeth. Postrostral carina increas-
7 14 21
carapace length (mm)
Figure 27. — Sicyonia disedwardsi. Relationship between ros-
trum length and carapace length (regression equation for speci-
mens with about 20 mm cl or less, y = 0.74318 + 0.2174aac;
regression equation for those larger, y = 3.81074 + 0.04939x).
33
FISHERY BULLETIN; VOL. 83, NO. 1
ing in height from low anterior part (between
epigastric and middle teeth) to posterior tooth,
descending gradually from it to posterior margin
of carapace. Antennal spine relatively long, sharp,
and projecting from short buttress; hepatic spine
acutely pointed, arising from moderately raised
area, and placed between 0.19 and 0.26 (mean 0.22)
cl from orbital margin. Postocular sulcus short but
deep, continuing posteriorly as barely distinct
narrow groove; hepatic sulcus shallow; bran-
chiocardiac carina broad, long, extending lon-
gitudinally from hepatic region almost to posterior
margin of carapace where bifurcate: one branch
curving dorsally and other, short, disposed
ventrally.
Eye as illustrated in Figure 3. Ocular stylet
with terminal part often bent laterally in young,
but usually straight in larger individuals.
Antennular peduncle with stylocerite produced
in long spine, its length 0.80 to 0.90 distance be-
tween lateral base of first antennular article and
mesial base of distolateral spine; latter extending
as far as distal 0.3 of second antennular article;
antennular flagella short, maximum length 0.25-
0.35 cl, mesial flagellum slightly shorter than lat-
eral in young but subequal to or slightly longer in
larger adults.
Scaphocerite nearly or quite overreaching an-
tennular peduncle by as much as 0.15 its own
length; lateral rib ending distally in long, acute
spine conspicuously surpassing margin of lamella.
Antennal flagellum as much as 2.2 times as long
as carapace.
Third maxilliped stouter than pereopods. Basis
and ischium of first pereopod unarmed.
Abdomen with high dorsomedian carina ex-
tending from first through sixth somites, carina on
first produced in strong tooth, sometimes disposed
almost horizontally, but usually elevated as much
as 55°, tooth tapering to sharp apex, and consider-
ably larger than posterior one on carapace; carina
on fifth somite produced in small tooth and that on
sixth terminating in strong sharp one.
Anterior margin of pleuron of first abdominal
somite straight or very slightly concave; antero-
ventral extremity of pleuron of first through
fourth somites ending in spine, that of first usually
directed anteroventrally, spines on second through
fourth often curved posterolaterally; posteroven-
tral margin of first through third somites rounded,
that of fourth broadly angular, sometimes bearing
node or minute spine, and that of fifth and sixth
sharply angular and armed with small, caudally
directed spine. Pleural spination of first four so-
mites barely if at all distinct in juveniles, becom-
ing stronger with increasing length of carapace.
First somite traversed by deep, long anterome-
dian pleural sulcus (sometimes obsolete along
midlength), latter usually converging with united
posterior tergal-posteromedian pleural sulci ven-
FlGURE 28. — Sicyonia disedwardsi , S 23.5 mm cl, Golfo de Panama, Panama. A, Petasma, dorsal view;
B, ventral view of same; C, right appendix masculina, dorsolateral view. Scale = 1 mm.
34
P6REZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
trally, but its dorsal extremity often not reaching
anterior margin. Second and third somites with
anterior and often short posterior tergal sulci; an-
teromedian pleural sulcus frequently joining
posteromedian pleural sulcus (sometimes obso-
lete) dorsally, and continuous with anteroventral
depression setting off prominence dorsally and
ridge posteriorly. Traces of posterior pleural sulcus
occasionally present in one or more of first three
somites. Fourth and fifth somites with anterior
tergal joining curved, united posterior tergal-
posteromedian pleural sulci. Sixth somite with
shallow, arched posteromedian pleural sulcus;
longitudinal ridge along base of dorsomedian
carina delimited ventrally by weak depression
lying dorsal to ill-defined cicatrix.
Telson with pair of small but clearly distinct
fixed spines. Rami of uropod subequal in length
and falling slightly short of or overreaching apex
of telson by as much as 0.15 its own length.
Petasma (Fig. 28A, B) with rigid distal projec-
tion of dorsolateral lobule mesially inclined (in-
stead of erect), strongly curved dorsomesially then
laterally; distal part of projection slightly com-
pressed, often bearing crest, rounded ventrally
and produced laterally in elongate, acutely
pointed salient. Distal projection of ventrolateral
lobule with terminal part strongly curved later-
ally, bulbous dorsally, plane ventrally, with
pointed tip curved proximoventrally.
Petasmal endopods coupled in males with
carapace length as little as 5.5 mm (about 22.5 mm
tl), but sometimes unjoined in individuals with
carapace length as much as 10.5 mm (about 38.5
mm tl). These observations are similar to those
noted by Burkenroad (1938).
Appendix masculina as illustrated in Figure
28C.
Thelycum (Fig. 29) with plate of sternite XIV
raised in paired, low (sometimes indistinct), rela-
tively short bulges, sloping toward deep, broad,
median depression. Median plate of sternite XIII
sagittiform, tapering gradually into long, slender
spine reaching as far as proximal 0.25 of basis of
extended second pereopods; plate deeply excavate
and bearing arched lateral incisions at level of
fourth pereopods; posterior component with deep,
broad posteromedian emargination forming rela-
tively elongate, posterolateral processes marked
basally by rather faint transverse suture. Sternite
XI armed posteriorly with pair of small, broad
based spines. Posterior thoracic ridge either al-
most flush with plate of sternite XIV or with only
anteromedian margin raised (ventrally).
Sperm receptacles as illustrated in Figure 7 (il-
lustration based on specimen treated following
method by Monod and Cals (1970)).
The smallest impregnated female encountered
has a carapace of 12 mm, about 42 mm tl.
Color. — The only observation on color of fresh
material from the Gulf of California (Anonymous
1980) indicates that the typical large spot found in
the posterior part of the branchiostegite is
purplish brown with a yellow center. The con-
spicuous ocellate spot persists in preserved speci-
mens, appearing like a broad dark ring surround-
ing a light center.
Maximum size. — Male, 29.2 mm cl, about 102 mm
tl; female 34 mm cl, about 108 mm tl.
Geographic and bathy metric ranges. — Southwest
of Isla Santa Margarita (24°19'36"N, 111°46'24"W
- 24°19'48"N, 111°47'06"W) to Bahia San Lucas,
Figure 29. — Skyonia disedwardsi , 9 21.3 mm cl, off Punta
Gorda, Baja California Sur, Mexico. Thelycum. Scale = 2 mm.
35
FISHERY BULLETIN: VOL. 83, NO. 1
Baja California Sur, in the Gulf of California along
the central and southern parts of both coasts and
southward to Bahia Chamela (19°33'42"N,
105°07'24"W), Jalisco, Mexico. Also from Bahia de
Culebra (10°37'00"N, 85°40'00"W), Costa Rica, to
northwest of Punta Caracoles (7°45'00"N,
78°24'30"W), Darien, Panama (Fig. 30). It has
been found at depths between at least 18 (5-18) and
249 m, but seems to be most abundant at 30-60 m.
It occurs on bottoms of shell, mud, fine sand, and
rocks.
The occurrence of this shrimp along the west
coast of Baja California Sur has not been previ-
ously reported.
Discussion. — Sicyonia disedwardsi is most simi-
FlGURE 30. — Geographic distribution of Sicyonia disedwardsi
and S. penicillata.
lar to the western Atlantic S. typica. As stated
above, among the American members of the genus
lacking an incision or abrupt depression on the
middorsal carina of the second abdominal somite,
these two, together with S. penicillata and the
western Atlantic S. olgae bear two relatively large
teeth on the postrostral carina posterior to the
level of the hepatic spine. The genitalia of S. dis-
edwardsi and S. typica are so similar that they are
almost indistinguishable, but in the petasma of S.
typica the tip of the projection of the dorsolateral
lobule is not so strongly produced and is usually
directed dorsally rather than dorsolaterally. These
two species, however, differ in the number and
extension of abdominal sulci: in S. typica the first
three somites exhibit well-marked posterior
pleural sulci, which are absent or weak in S. dis-
edwardsi , and the dorsal extremity of the united
posterior tergal-posteromedian pleural sulci of the
first somite reaches the anterior margin of the
somite, whereas in S. disedwardsi the dorsal end
usually does not reach the margin. Also in S.
typica, the anteromedian pleural sulcus of the first
somite is unbroken and that of the second joins the
posteromedian, whereas in S. disedwardsi the
former is often interrupted and the median sulci
do not merge; in addition, the posterior tergal sulci
of the second and third somites are much longer
than in S. disedwardsi, in which they terminate
considerably dorsal to the base of the respective
pleuron. Furthermore, the rostrum of S. dised-
wardsi usually bears two teeth on the dorsal mar-
gin posterior to the apical teeth, whereas in S.
typica it is often armed with only one.
Sicyonia disedwardsi differs from S. penicillata
by the same features of the abdomen that distin-
guish it from S. typica, except that in S. penicillata
the posterior pleural sulci are more frequently
present and slightly better marked than in S. dis-
edwardsi. Too, the rostrum of S. penicillata, like
that of S. typica, commonly bears only one dorsal
tooth and is less elevated and usually shorter than
in individuals of same size of S. disedwardsi. The
two partly sympatric species can be separated
readily by the genitalia. The unusually long distal
projections of the dorsolateral and ventrolateral
lobules in S. penicillata are not exhibited by any
other of its congeners. Also, whereas in S. dised-
wardsi the thelycal plate of sternite XIV bears
paired low (sometimes indistinct) bulges, in S.
penicillata it is raised in strongly marked and
more striking ones; the posterior component of the
median plate of sternite XIII in S. disedwardsi
exhibits a broad and deep posteromedian emar-
36
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
gination flanked by elongate processes and is
traversed by a faint suture; in contrast, that of S.
penicillata possesses a shallow emargination,
often bearing a small anteromedian notch, and is
traversed by a deep groove.
Long after they have been taken from the water,
even after years in alcohol, specimens of this
species may be readily recognized by a large ocel-
lus, consisting of a well-defined yellow center sur-
rounded by a broad purplish ring, on the bran-
chiostegite. In S. penicillata, as in S. typica, the
branchiostegite does not bear a large marking.
Burkenroad (1938) indicated that all members of
S. disedwardsi may be distinguished from those of
S. penicillata by the shape of the ocular stylets
which in the former, according to him, diverge at
the tip; they are straight in the latter. I have found,
however, that although the stylets are laterally
inclined distally in most of the young of S. dised-
wardsi, they are straight in some young and in
many adults.
Commercial importance. — Sicyonia disedwardsi,
one of the stubbiest of the rock shrimp occurring in
the region, is usually taken with other penaeoids
by the shrimp fleets operating in various areas
from the Gulf of California to the Golfo de
Panama. Because of its size, it appears to have the
potential of providing a fishery as has the simi-
larly heavy S. brevirostris in the western Atlantic.
Material. — 242 specimens from 54 lots.
Mexico— Baja California Sur: 66 69, SIO, 3
km SW of Isla Santa Margarita, 48-57 m, 13
November 1964, Black Douglas . 5d 69 , SIO, SW
of Isla Santa Margarita, 29-40 m, 13 November
1964, Black Douglas. 26 19, SIO, NW of Punta
Marquez, 37 m, 4 December 1962, H. Perkins and
R. Wisner. 126 119, SIO, NW of Todos Santos, 38
m, 9 November 1964, Black Douglas. 36 19,
YPM, Bahia San Lucas, 15-29 m, 6 May 1936, Zaca
stn 135 D-1. 19 , YPM, Bahia San Lucas, 11-37 m,
6 May 1936, Zaca stn 135 D-9. 26 29, YPM, off
Punta Arena, 92 m, 30 April 1936, Zaca stn 136
D-24. 19, YPM, off Punta Arena, 82 m, 3 April
1936, Zaca stn 136 D-1. 4d 29, YPM, off Punta
Arena, 64 m, 1 May 1936, Zaca stn 136 D-30. 36
19, USNM, Bahia La Ventana, 24-27 m, 20 April
1939, Strange stn 38. 2619, SIO, off Punta
Gorda, 81-84 m, 2 July 1965, C. Hubbs. 46 39,
USNM, Canal de San Lorenzo to Isla del Espiritu
Santo, 4 April 1960, R. Mercado and G. Pre-
ciado. 26 29, SIO, Bahia de la Paz, 55-79 m, 6
July 1965, R. Rosenblatt. 36 99, SIO, Canal de
San Jose, 64 m, 8 July 1965, R. Rosenblatt. 46
109, SIO, Punta San Telmo, 10 July 1965, W
Baldwin. 86 69, SIO, off W of Isla Monserrate,
92-73 m, 12 July 1965, R. Rosenblatt. 26 , SIO,
Bahia Concepcion, 4 February 1940, D.
Rouch. Id , holotype, YPM, Bahia Concepcion, 3
May 1926, Pawnee. 26 29, USNM, 4-6 m, off
Punta Concepcion, 12 April 1964, F. Rosales
Juarez. 19, YPM, Bahia Santa Ines, 50 m, 13
April 1936, Zaca stn 143 D-1. 26 19 , YPM, Bahia
Santa Ines, 37 m, 10 April 1936, Zaca stn 141
D-4. 19, YPM, Bahia Santa Ines, 13-16 m, 10
April 1936, Zaca stn 141 D-1. 26 39 , YPM, Bahia
Santa Ines, 50 m, 11 April 1936, Zaca stn 142
D-1. 86, SIO, off Santa Rosalia, 35-26 m, 25
March 1960, R. Parker. 16 , SIO, S arm of Bahia
de los Angeles, 22-37 m, 26 April 1962, R.
Rosenblatt. 26 39, AHF, Puerto Refugio,
Isla Angel de la Guarda, 38 m, 27 January 1940.
Sonora: 16 19, USNM, off Estero de Lobos, 47
m, 3 April 1978, Toral Garcia. 19, USNM, 8
km off Guaymas, 26 m, April 1980, M. Hatziolos.
3d 59, INP, off Punta Rosa, 56 m, 2 April 1978,
Toral Garcia. 66 49, USNM, SE of Punta Rosa,
54 m, 1 April 1978, Toral Garcia. Sinaloa:
Id, USNM, off San Ignacio, 25 May 1962, R. Bush
M. 2d, SIO, Isla de Altamura, 22-31 m, 26
May 1965, El Golfo II stn 50-6. 19, AHF, off
Rio San Lorenzo, 11-24 m, 14 February 1940.
Nayarit: Id 59, AHF, off Isla Isabela, 27-46 m,
9 May 1939. Jalisco: Id, SIO, Bahia Cha-
mela, 27-18 m, 2 April 1973, Agassiz. Colima:
19, CAS, off Manzanillo, 17 July 1932, Zaca.
Costa Rica— Id, AHF, Bahia de Culebra, 5-18
m, 24 February 1934. 29, AHF, S of Bahia de
Culebra, 18 m, 25 February 1934. 19, SIO, Cabo
Blanco, 60 m, 18 April 1973, Agassiz. Id, SIO,
Cabo Blanco, 137-145 m, 19 April 1973, C. Hubbs
and S. Luke. 19 , UCR, near Cabo Blanco, 245 m,
28 April 1973, Enriqueta. Id, UCR, near Cabo
Blanco, 249 m, 28 April 1973, Enriqueta. Id,
UCR, near Puerto Quedos, 242 m, 26 April 1973,
Enriqueta . Id , AHF, 5 km off Isla Manuelita, 146
m, 3 June 1973, Velero IV. 19 , AHF, Golfo Dulce,
35-88 m, 26 March 1939, Velero IV.
Panama— 2d 29, USNM, Golfo de Panama,
Canopus stn 670. 5d 119, USNM, Golfo de
Panama, Canopus stn 126. 2d 29, UP, Ar-
chipielago de las Perlas, 11 December 1970, J. M.
del Rosario. Id 19, USNM, Isla San Jose, 64 m,
23 February 1973, fishermen. 3d 19 , USNM, S of
Isla del Rey 44-42 m, 7 May 1967, Pillsbury stn
551. 19, AHF, Islas Secas, 46-48 m, 27 March
1939. 19, AHF, off Bahia Honda, 55-64 m, 1
37
FISHERY BULLETIN: VOL. 83, NO. 1
March 1938. M 49, UP, between Punta Ave
Maria and Ensenada Guayabo, 14 December 1969,
staff Dep. Biol. Mar, UP 3d 19, USNM, 12 km
NW of Punta Caracoles, staff Dep. Biol. Mar., UP
Sicyonia pentcillata Lockington 1879
Figures 30-34
Sicyonia penicillata Lockington 1879:164 [syn-
types (not extant): "Bolinas Bay (?Bahia de
Ballenas), Lower California", 14 fm (fathom)
(25.6 m); Angeles Bay (Bahia de los Angeles),
Gulf of California, W. J. Fisher]. De Man
1911:112. Pesta 1915:118, fig. 7. Schmitt
1924:387. Brusca 1973:219. Rosales Juarez
1976:41. Rodriguez de la Cruz 1977:10.
Anonymous 1980:7. Brusca 1980:256.
Rodriguez de la Cruz 1981:1. Mathews 1981:
329.
Eusicyonia penicillata. Boone 1930:115 [part], pi.
36. Burkenroad 1934a:88, figs. 30, 31, 33,
1938:93. Steinbeck and Ricketts 1941:444.
Castro 1966:17 [part]. Word and Charwat
1976:22, 2 figs.
Eusicyonia sp. Castro 1966:16, 17 [part], fig. 4.
Vernacular names: rock shrimp, target shrimp,
Japanese shrimp (United States); cacahuete,
camaron de piedra, camaron de roca, camaron
japones (Mexico). FAO names: peanut rock
shrimp (English), camaron cacahuete
(Spanish), boucot cacahouette (French).
Diagnosis. — Antennal spine well developed and
buttressed. Second abdominal somite with dor-
somedian carina lacking incision. First pereopod
with basis and ischium unarmed. Postrostral
carina bearing two teeth posterior to level of he-
patic spine. Rostrum armed with two dorsal teeth
(rarely one). Petasma with distal projection of dor-
solateral lobule acicular, long and slender.
Thelycum with plate of sternite XIV raised in
strong bulges; posterior component traversed by
deep groove. Branchiostegite with moderately
large purplish brown spot bearing poorly defined
yellow center.
Description. — Body robust (Fig. 31). Carapace
studded with long setae anteroventral to hepat-
ic spine and pterygostomian region; patches of
densely set shorter setae present on dorsum, in
depression anterior to posterodorsal part of bran-
chiocardiac carina, on branchiostegite and along
hepatic sulcus; patches also on tergum of abdomi-
nal somites and in lateral depression of sixth so-
mite. Abdomen with numerous tubercles on first
three somites, fewer on last three.
Rostrum short, not surpassing distal margin of
eye, its length increasing linearly with carapace
length (Fig. 32) but proportionately longer in
young (0.30-0.12 cl); usually straight but occasion-
ally curved, subhorizontal or elevated as much as
45°; tapering, sometimes considerably, from base
to truncate tip; and armed with one dorsal (rarely
2) and two (96%) or three (4%) apical teeth. Adros-
FlGURE 31. — Sicyonia penicillata Lockington,
23 mm cl, west of Punta T^sca, Isla Santa Margarita, Baja California Sur, Mexico.
Lateral view. Scale = 5 mm.
38
PfcREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
tral carina, situated distinctly dorsal to ventral
margin, strong and extending to end of rostrum.
Carapace with well-marked postrostral carina
bearing three teeth: 1) epigastric tooth small, only
slightly larger than first rostral, situated opposite
(rarely) to <0.1 cl posterior to orbital margin; 2)
middle tooth, larger than epigastric, sharp, placed
well posterior to hepatic spine, between 0.33 and
0.40 (mean 0.36) cl from orbital margin; and 3)
posterior tooth, larger than middle tooth, acutely
pointed, rising almost vertically with only apical
part inclined anteriorly or so inclined throughout,
and situated between 0.70 and 0.77 (mean 0.74) cl
from orbital margin; tuft of setae present at an-
terior base of all three teeth. Postrostral carina
low anterior to middle tooth, high between middle
and posterior one, and descending gradually from
latter to posterior margin of carapace. Antennal
spine relatively long, sharp, and projecting from
short buttress; hepatic spine acutely pointed,
larger than antennal, arising from moderately
raised area between 0.20 and 0.26 (mean 0.22) cl
from orbital margin. Postocular sulcus short but
deep, continuing as shallow groove; hepatic sulcus
well marked; branchiocardiac carina usually low
(sometimes barely distinct) but occasionally quite
prominent and long, extending to bifurcation near
posterior margin of carapace, short branch curv-
ing dorsally and longer one ventrally.
Ocular stylet with terminal part straight or,
occasionally, turned laterally.
Antennular peduncle with stylocerite produced
in long spine nearly or quite reaching mesial base
7 14 21 28
carapace length (mm)
35
Figure 32. — Sicyonia penicillata. Relationship between ros-
trum length and carapace length (regression equation, y =
0.65537 + 0.13963;c).
of distolateral spine; latter slender and sharp, ex-
tending as far as proximal 0.70 of second antennu-
lar article; antennular flagella short, with
maximum length of 0.20-0.30 cl, in juveniles and
young adults mesial flagellum slightly shorter
than lateral one but in larger adults subequal to or
slightly longer.
Scaphocerite reaching distal margin of anten-
nular peduncle or overreaching it by no more than
0.10 of its own length; lateral rib ending distally in
sharp spine distinctly surpassing margin of
lamella. Antennal flagellum 2.4-2.7 times cl in
young, and as much as 2.0 times in larger adults.
Third maxilliped stouter than pereopods. Basis
and ischium of first pereopod unarmed.
Abdomen with high dorsomedian carina ex-
tending from first through sixth somites, carina on
first produced in strong, sharp, anterodorsally di-
rected tooth, slightly to considerably larger than
posterior tooth on carapace; carina on fifth somite
produced in conspicuous tooth, and that on sixth
terminating in strong acute one.
Anterior margin of pleuron of first abdominal
somite almost straight; anteroventral extremity of
pleuron of first through fourth somites ending in
spine, that of first directed anteroventral ly but
that of second usually curved posterolaterally, re-
sembling strong spines on third and fourth so-
mites; posteroventral margin of first through third
somites convex, on fourth broadly angular, and on
fifth and sixth sharply so and armed with small
caudally directed spine. Pleural spination of first
four somites barely, if at all, distinct in juveniles,
becoming stronger with increasing length of
carapace.
First somite marked by long, anteromedian
pleural sulcus converging with united posterior
tergal-posteromedian pleural sulci ventrally, dor-
sal extremity of tergal reaching anterior margin of
somite; posterior pleural sulcus weak, but usually
clearly distinct. Second and third somites with
anterior and posterior tergal sulci long, almost
reaching base of pleuron; anteromedian pleural
sulcus deep, continuous with anteroventral de-
pression setting off elongate prominence dorsally
and ridge posteriorly; posteromedian pleural sul-
cus also long, extending anterodorsally subparal-
lel to posterior tergal sulcus; shallow posterior
pleural sulcus commonly present in both somites.
Fourth and fifth somites with anterior tergal and
curved, united posterior tergal-posteromedian
pleural sulci merging dorsally. Sixth somite
marked by arched posteromedian pleural sulcus
and bearing longitudinal ridge along base of dor-
39
FISHERY BULLETIN: VOL. 83, NO. 1
somedian carina delimited ventrally by depres-
sion lying just dorsal to well-defined cicatrix.
Telson with pair of small but well-developed
fixed spines. Rami of uropod subequal in length
and falling slightly short of or overreaching apex
of telson by no more than 0.10 its own length.
Petasma (Fig. 33A , B ) with short distal plate of
dorsomedian lobule bearing distolaterally small,
scalelike process bent inwardly (posteroven-
trally). Projection of distolateral lobule acicular,
extremely long, about 0.75 as long as body of
lobule, with heavily sclerotized triangular plate
proximodorsally and flexible flagellum arising
from ventrolateral surface; flagellum long, reach-
ing between 0.60 and 0.75 length of projection
from level of apex of triangular plate. Projection of
ventrolateral lobule also long, about half length of
acicular projection, bladelike and flexible, except
for sclerotized tip curving proximally.
Petasmal endopods coupled in males with
carapace length as little as 5.5 mm, about 22
mm tl, but sometimes unjoined in individuals
with carapace length as much as 11 mm, about 39
mm tl.
Appendix masculina as illustrated in Figure
33C.
Thelycum (Fig. 34) with plate of sternite XIV
raised in paired, well-marked, elongate bulges
sloping toward deep, narrow, median depression.
Median plate of sternite XIII lanceolate, tapering
gradually into slender spine reaching as far as
proximal 0.20 of basis of extended second
pereopods; posterior component with relatively
shallow posteromedian emargination (occasion-
ally replaced by longitudinal incision) often form-
ing small notch anteriorly, and flanked by short,
rounded, posterolateral processes marked basally
by deep transverse suture. Sternite XI armed
posteriorly with pair of broad based, acute spines.
Posterior thoracic ridge with anteromedian mar-
gin sharp and raised (ventrally), its lateral mar-
gins usually well marked, occasionally flush with
plate of sternite XIV.
The smallest impregnated female encountered
has a carapace length of 8.5 mm, about 33 mm tl.
Color. — Available information based on speci-
mens that had been recently caught in the Gulf of
California is limited to a purplish brown spot,
with a yellow center not sharply defined, postero-
ventral to the hepatic spine; sometimes the entire
spot is purplish brown (Anonymous 1980). Lock-
FlGURE 33. — Sicyonia penicillata, 6 21.5 mm cl, west of Punta T^sca, Isla Santa Margarita, Baja California Sur, Mexico.
A, Petasma, dorsal view; B, ventral view of same; C, right appendix masculina, dorsolateral view. Scale = 1 mm.
40
P6REZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
Figure 34. — Sicyonia penicillata, 9 23 mm cl, west of Punta
Tasca, Isla Santa Margarita, Baja California Sur, Mexico.
Thelycum. Scale = 1 mm.
ington (1879) noted that "Color after two weeks
exposure to alcohol, bright red; with a dark red-
brown ocellated spot on each side of the carapace.
Antennae bluish." In many of the preserved speci-
mens that I have studied, the ocellus appears as a
dark circle.
Maximum size. — Males 32 mm cl, about 103 mm
tl; females 35 mm cl, about 110 mm tl.
Geographic and bathymetric ranges. — From
southwest of Punta Canoas (29°20'N, 115°02'W),
Baja California Norte, Mexico (Fig. 30), south-
ward to Bahia San Lucas, and in the Gulf of
California, from the northern end to Bahia Con-
cepcion on the west and northern Sinaloa on the
east; it seems to be absent from the southernmost
part of the Gulf. It has also been found off Pun-
tarenas (9'58'N, 84°50'W), Costa Rica (Boone
1930). This species occurs at depths between 0.60
and 180 m (latter by Boone 1930), mostly at 35-70
m. It has been recorded on sand (fine or coarse) and
mud substrates that are sometimes densely cov-
ered with algae.
Discussion. — The closest affinities of S. penicil-
lata seem to be with S. disedwardsi from which it
differs most conspicuously in features of the
petasma. The extremely long, slender, distal pro-
jections of both the dorsolateral (which bears a
lateral fiagellum) and ventrolateral lobules are far
different from the short, stout, and simple projec-
tions of the petasma of S. disedwardsi, as well as
from those of all other species of Sicyonia. These
two species also exhibit significant thelycal differ-
ences. In the thelycum of S. penicillata the lateral
bulges of the plate of sternite XIV are well defined;
the posteromedian emargination of the median
plate of sternite XIII is shallow (occasionally re-
placed by a longitudinal incision), often bears an
anterior notch, and is flanked by short posterolat-
eral processes marked basally by a conspicuous
transverse groove. In the thelycum of S. dised-
wardsi the bulges are low, often indistinct, the
posteromedian emargination of the median plate
of sternite XIII is broad and deep, lacks a notch,
and is flanked by relatively elongate posterolat-
eral processes which are delimited anteriorly by a
weak suture.
The following characters are also helpful but
somewhat less reliable for distinguishing between
the two species. In S. penicillata the rostrum is
armed with only one tooth (rarely two) on the
dorsal margin, instead of two as in S. disedwardsi;
the stylocerite reaches the mesial base of the disto-
lateral spine of the first antennular article,
whereas in the latter species it often falls short of
the base; the dorsal extremity of the united pos-
terior tergal-posteromedian pleural sulci of the
first abdominal somite reaches the anterior mar-
gin of the somite, whereas in S. disedwardsi often
it does not; and the clearly defined although shal-
low posterior pleural sulci are usually present on
the first three abdominal somites of S. penicillata
but are quite weak or, more often, lacking on some
or all of the latter
Fresh material of this shrimp may be identified
by a purplish brown spot on the branchiostegite,
sometimes bearing a yellow center with diffuse
border.
Burkenroad (1934a) presented a detailed discus-
sion of the differences between S. penicillata and
the western Atlantic S. typica (as Sicyonia ed-
wardsii Miers, 1881). These species, which share
among other characters three teeth on the post-
rostral carina and usually one dorsal and two api-
41
FISHERY BULLETIN: VOL. 83, NO. 1
cal rostral teeth, differ strikingly in other fea-
tures. In S. typica the sculpture of the abdomen is
stronger than that in the eastern Pacific shrimp,
exhibiting a long and deep posterior pleural sulcus
on the first four somites instead of ones that are
weak or even obsolete, and the telsonic spines are
quite inconspicuous, rather than being well devel-
oped as they are in S. penicillata .Also, in S. typica
the petasma lacks long slender distal projections
as well as accessory flagella, the thelycal plate of
sternite XIV is almost flat laterally instead of ele-
vated in strong bosses, and the posteromedian
emargination of the posterior component of the
median plate is quite broad rather than narrow or
even reduced to a longitudinal incision as it is in S.
penicillata.
Remarks. — The types of this species were de-
stroyed in the San Francisco earthquake and fire
of April 1906 as were all of Lockington's types
which had been deposited at the California Acad-
emy of Sciences (Dunn 1982). The locality of one of
the syntypes, the one Lockington described in de-
tail, "Bolinas Bay, Lower California," is uncertain.
The NIS Gazetteer (Office of Geography, Depart-
ment of the Interior, 1956) does not include any
place or geographic feature under "Bolinas". On
the west coast of Baja California Sur is Bahia de
Ballenas or "Ballenas Bay" (NIS Gazetteer, p. 50),
at 26°45'N, 113°26'W, and it is quite possible that
the name of this locality was misspelled on the
label accompanying the sjnitj^e or that Lock-
ington misread and transcribed it as "Bolinas
Bay". There is a bay by this name at 37°53'36"N,
122°39'54"W, in Marin County, California; how-
ever, I am inclined to think that Bahia de Ballenas
actually is the place where the specimen was ob-
tained because it is well within the range of the
species, whereas Bolinas Bay is not only outside
"Lower California" but also far beyond the known
northern limit of this shrimp — southwest of
Punta Canoas, Baja California Norte.
Commercial importance. — There is a fishery for
rock shrimp in the northern half of the Gulf of
California, and the catches are believed to consist
largely of S. penicillata a very abundant species in
that area. This fishery in 1979-80 produced
1,426,541 kg, but in 1981-82 (data recorded in
Guaymas by the Instituto Nacional de Pesca,
Mexico), the last year for which landings are
available, the production declined sharply to
187,786 kg; fishing for rock shrimp is only sea-
sonal, from February to June, with maximum
catches being obtained during March and April
(Concepcion Rodriguez de la Cruz see footnote 2).
Material. — 939 specimens from 56 lots.
Mexico— Baja California Norte: 29, SIO, SW
of Punta Canoas (29°20'N, 115°02'W), 40 m, 6 Sep-
tember 1952, K. S. Norris. 16 29, SIO, Bahia
Playa Maria, 11 m, 1 April 1952, K. S. Norris. 39 ,
SIO, Bahia Sebastian Vizcaino, surface, 17 Au-
gust 1952, Spencer F. Baird. 16 , YPM, E of Isla
Cedros, 1-73 m, Zaca stn 126D-3. 49 , SIO, Bahia
Sebastian Vizcaino, 0-2 m, 14 August 1952, K. S.
Norris. Baja California Sur: 3d , SIO, Bahia
Sebastian Vizcaino, 55 m, 11 August 1952, K.S.
Norris. 16 , SIO, E of entrance to Laguna Ojo de
Liebre, 2 m, 16 August 1952, K. S. Norris. 76 59,
SIO, Bahia Tortolo, 31 March 1962, H. C. Per-
kins. Id 29, SIO, E of Punta Asuncion, Bahia
Asuncion, 15 m, 24 March 1951, R. Wisner and K.
S. Norris. 66 99, SIO, Bahia Asuncion, 40-44 m,
17 November 1964, Black Douglas . 136 119 , SIO,
Bahia Asuncion, 68-64 m, 17 November 1964,
Black Douglas. 116 149, SIO, Laguna San Ig-
nacio, 1.5 m, 11/12 February 1950, C. Hubbs. 3d
89, SIO, Bahia de Ballenas, 18 m, 14 February
1948, Scripps. 43d 509, SIO, SE of Punta Abre-
ojos, 55-59 m, 17 November 1964, Black Doug-
las. 246 229, SIO, W of Punta Pequeha, 37-40 m,
16 November 1964, Black Douglas. 266 219 , SIO,
off Punta Pequeiia, 55-51 m, 16 November 1964,
Black Douglas. 46 109, SIO, WSW of Punta
Pequeha, 68-73 m, 16 November 1964, Black Doug-
las. 16 59, SIO, NW of Santo Domingo del
Pacifico, 45-40 m, 19 April 1969, D. Dock-
ins. 26d 399, SIO, 15 km WSW of Boca de las
Animas, 55-57 m, 16 November 1964, Black Doug-
las. 26 39, SIO, S of Boca de las Animas, 137 m,
29 January 1964, C. Hubbs. 13d 79 , SIO, between
Boca de Santo Domingo and Boca de Sole-
dad, 12 m, 5 February 1964, A. Stover and B.
Zahuranec. 19, USNM, Boca de Soledad, 26
April 1964, H. Chapa. 19, SIO, channel N of
Bahia Magdalena, 6 m, 30 January 1964, A. Stover
and B. Zahuranec. 48d 449, SIO, NW of Isla
Santa Magdalena, 73 m, 15 November 1964, Black
Douglas. 3d 39, SIO, Bahia Santa Maria, 0-36
m, 8 December 1962, H. C. Perkins. Id 19, SIO,
Bahia Magdalena, 42-44 m, 29 November 1962, F
H. Berry. 19, USNM, Bahia Magdalena, surface,
10 July 1953. 14d 99, SIO, Bahia Magdalena,
37-40 m, 24 August 1960, F H. Berry 8d 69,
YPM, Bahia Magdalena, 0.6-0.9 m, 1936, Zaca
[unnumbered stn]. 19, AHF, Bahia Magdalena,
between mainland and Punta Redonda, 15 m, 5
42
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
February 1974, H. G. Moser stn 13. 16, SIO, off
Bahia Magdalena, 88 m, 3 February 1964, C.
Hubbs. 5c? 69, SIO, Bahia Almejas, 21-24 m, 11
November 1964, Black Douglas. 506 509, SIO,
SW of Isla Santa Margarita, 29-40 m, 13 November
1964, Black Douglas . 406 409 , SIO, 3 km SW of
Isla Santa Margarita, 46-57 m, 13 November 1964,
Black Douglas. 186 89, SIO, SW of Isla Santa
Margarita, 75-80.5 m, 13 November 1964, Black
Douglas. 16 59, SIO, SW of Isla Santa Mar-
garita, 88-90 m, 13 November 1964, Black Doug-
las. 36 29, SIO, W of Punta Tasca, Isla Santa
Margarita, 7 July 1955, Andres stn 143. 19, SIO,
11 km NW of Punta Marquez, 55 m, F H. Ber-
ry 29 , SIO, 14.5 km WNM of Punta Marquez, 92
m, 4 December 1962, F H. Berry 16, YPM,
Bahia San Lucas, 11-37 m, 6 May 1936, Zaca stn
135D-11, 12. 16, SIO, Bahia Santa Ines, 40-82 m,
14 July 1965, C. Hubbs. 34c5 229, YPM, Bahia
Concepcion, 3 May 1926, Pawnee. 16 29, SIO, off
Santa Rosalia, 35-36 m, 25 March 1960, R. Parker
Baja California Norte: 16 59, SIO, S arm of
Bahia de los Angeles, 22-37 m, 26 April 1962, R.
Rosenblatt. b6 159, YPM, Bahia de los Angeles,
31-46 m, 13 May 1926, Pawnee. 16 69, SIO, off
San Felipe, 2 April 1973, C. Farwell. 4<5 29, YPM,
Bahia San Felipe, 19 May 1926, Pawnee. &6 59,
USNM, near northern end of Gulf of California,
9-18 m, February 1949, B. W. Walker. Sonora:
Id 19, USNM, Bahia de Adair, 46 m, 5 April
1968, Toral-Garcia. 26 39, USNM, Bahia de
Adair, 29 m, 5 April 1978, Toral-Garcia. 56 139,
USNM, off Bahia de San Jorge, 26 March 1967,
shrimp trawler. 26 19, INP, N of Guaymas, 26
April 1961, H. Chapa. 16, AHF, Bahia de
Guaymas, 4-6 m, 22 January 1940. 19, SIO,
Bahia de Guaymas, 22 March 1939, M. W
Johnson. 26 , SIO, Bahia de Guasimas, 32 km S
of Guaymas, April 1968, D. Hoese. Sinaloa: 16
19, USNM, off Sinaloa, H. Chapa.
Sicyonia affinis Faxon 1893
Figures 35-38
Sicyonia affinis Faxon 1893:209 [syntypes: 16 19,
MCZ 4637, off Isla del Coco, Costa Rica,
5°31'30"N, 86°52'30"W, 100 fm (183 m), 28 Feb-
ruary 1891, Albatross stn 3367; 16, USNM
21169, off Isla del Coco, Costa Rica, 5°32'45"N,
86°55'20"W, 52 fm (95 m), 28 February 1891,
Albatross stn 3369; 29, USNM 21170, W of Isla
de Malpelo, Colombia, 3°58'20"N, 81°36'00"W,
112 fm (205 m), 5 March 1891, Albatross stn
3378. 19 , MCZ 4638, W of Isla de Malpelo, Co-
lombia, 3°59'40"N, 81°35'00"W, 52 fm (95 m),
5 March 1891, Albatross stn 3379]. Faxon
1895:179, pi. 46, fig. 1, la-c. A. Milne Edwards
and Bouvier 1909:244. De Man 1911:112.
?Chapa Saldaha 1964:9. Chirichigno Fonseca
1970:7, fig. 5. ?Rodriguez de la Cruz 1977:
12. Arana Espina and Mendez G. 1978:23,
fig. 1-5. Mendez G. 1981:47, pi. 9, fig. 75-77.
Perez Farfante and Boothe 1981:424.
Eusicyonia affinis. Burkenroad 1934a:93,
1934b:126, 1938:84, fig. 24. Anderson and
Lindner 1945:317.
Sicyonia penicillata Boone 1930:115 [part]. [Not
Sicyonia penicillata Lockington 1879.]
Diagnosis. — Antennal spine well developed and
buttressed. Second abdominal somite with dor-
somedian carina lacking incision. First pereopod
with basis and ischium unarmed. Postrostral
carina bearing one tooth posterior to level of
hepatic spine and forming high crest behind pos-
terior tooth. Rostrum short, not overreaching
distal margin of eye. Abdomen lacking tubercles;
second and third somites lacking inverted
V-shaped ridges laterally; fifth somite with dor-
somedian carina lacking tooth or sharp angle at
posterior end. Petasma with distal projection of
dorsolateral lobule compressed distally its trun-
cate tip produced dorsally in simple, minute spine.
Thelycum with plate of sternite XIV without an-
teromedian tubercle and raised in paired low, but
well-defined bulges. Branchiostegite lacking large
mark.
Description. — Body relatively slender (Fig. 35)
and lacking tubercles. Carapace studded with
numerous short setae, those on anterior part of
dorsum forming dense patches. First five abdomi-
nal somites with paired broad patches of short
setae flanking dorsomedian carina; sixth with one
in dorsolateral depression.
Rostrum short, reaching only as far as distal
margin of eye, its length 0.25-0.35 cl; upturned to
angle between 10° and 40°; armed with two dorsal
teeth and three minute apical teeth; latter dis-
posed on truncate apex with ventralmost one
either terminal or subterminal; first dorsal tooth
located distinctly anterior to orbital margin, sec-
ond tooth situated at about anterior 0.25 cl of ros-
trum. Conspicuous adrostral carina, subparallel
and distinctly dorsal to ventral margin, extending
almost to end of rostrum.
Carapace with well-marked postrostral carina
bearing two teeth; epigastric tooth, situated
43
FISHERY BULLETIN: VOL. 83, NO. 1
Figure 35. — Sicyonia affinis Faxon, ? 17 mm cl, 4.4 km off Isla Manuelita, Costa Rica. Lateral view. Scale = 5 mm.
slightly anterior to level of hepatic spine at about
0.15 cl from orbital margin, small, subequal to, or
only slightly larger than first rostral tooth; and
large posterior tooth, considerably larger than
epigastric, hooklike, with apical portion acutely
pointed and slightly curved anteriorly; tooth
placed distinctly in advance of posterior margin of
carapace, betw^een 0.65 and 0.75 (mean 0.67) cl
from orbital margin. Postrostral carina low an-
teriorly forming high crest descending gently from
posterior tooth to posterior margin of carapace.
Tuft of setae present at anterior base of each tooth.
Antennal spine small, sharp, projecting from
weakly developed buttress; hepatic spine moder-
ately long and acutely pointed, situated at 0.20-
0.25 (mean 0.22) cl from orbital margin; hepatic
sulcus almost horizontal, accompanying incon-
spicuous carina; branchiocardiac carina broad,
low, longitudinally disposed except for posterior
part curving dorsally near posterior margin of
carapace.
Antennular peduncle with stylocerite long, al-
most reaching level of mesial base of distolateral
spine, its length about 0.95 distance between lat-
eral base of first antennular article and mesial
base of distolateral spine; latter reaching as far as
distal 0.25 of second antennular article, antennu-
lar flagella short, mesial one more slender and
longer, about 0.20 cl, than lateral, 0.16 cl.
Scaphocerite extending to distal end or slightly
overreaching antennular peduncle; lateral rib
produced distally in long, strong spine, surpassing
margin of lamella. Antennal flagellum incomplete
in specimens examined.
Third maxilliped stouter than pereopods. Basis
and ischium of first pereopod unarmed.
Abdomen with strongly marked dorsomedian
carina extending from first through sixth somites,
carina on first somite produced anteriorly in
strong tooth (slightly more elevated than posterior
tooth on carapace), its anterior margin subvertical
but apical extremity slightly curved anteriorly;
carina deeply cleft posteriorly on first five somites,
on fourth and fifth not truncate but sloping gradu-
ally to apex of cleft, and on that of sixth somite
produced in large, acute, posterior tooth.
First four somites with rounded or broadly an-
gular anteroventral extremity unarmed; fourth
somite with posteroventral extremity rounded and
lacking spine, and that of fifth and sixth somites
bearing minute spine.
First somite marked with short, weak, an-
teromedian pleural sulcus, its length slightly <0.2
distance from origin (emargination on anterior
margin) to ventral margin of pleuron; united pos-
terior tergal-posteromedian sulci relatively shal-
low. Second and third somites with weak anterior
and posterior tergal sulci joining anterodorsally;
44
P6REZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
anteromedian pleural sulcus short, extending
from slightly below midheight of somite to near
ventral margin; posteromedian pleural sulcus
with faint dorsal extension directed anteriorly at
about 0.33 height of somite from dorsomedian line
and just ventral to weak crescent- shaped ridge
(latter delimited dorsally by tergal sulcus). Fourth
somite with anterior tergal sulcus shallow and
posterior tergal and posteromedian pleural sulci
coalescent, extending from near base of dorsal
carina to curve anteriorly near ventral margin.
Fifth somite with united posterior tergal-
posteromedian pleural sulci ending well above
ventral margin. Sixth somite with strongly arched
posterior pleural sulcus and low longitudinal
ridge situated between base of middorsal carina
and setose depression lying dorsal to weak cica-
trix.
Telson with very weak median sulcus and bear-
ing pair of small, fixed subterminal spines. Both
rami of uropod extending as far as apex of telson or
surpassing it by as much as 0.2 of their own
lengths.
Petasma (Fig. 36A, B) with rigid distal projec-
tion of dorsolateral lobule curved mesially, raised
proximodorsally in rounded prominence, and
compressed distally; its truncate tip with ventral
extremity rounded and dorsal extremity acutely
produced in acute salient. Distal projection of ven-
trolateral lobule fleshy, with terminal part flat-
tened (dorsal surface not bulbous) and curving
dorsally.
Appendix masculina as illustrated in Figure
36C.
Thelycum (Fig. 37) with plate of sternite XIV,
delimited by arched or straight lateral edges,
rounded anteriorly, its surface raised in low, ovoid
bulges separated by broad, median depression.
Median plate of sternite XIII flask-shaped in out-
line, tapering gradually into long, slender spine
reaching between midlength of coxae and proxi-
mal extremity of bases of second pereopods; plate
incised and excavate at level of coxae of fourth
pereopods; posterior component of plate with shal-
low posteromedian emargination. Sternite XI
armed with paired short spines. Posterior thoracic
ridge with concave anteromedian margin slightly
overlapping plate of sternite XIV, ridge then flush
with, or separated by shallow, transverse depres-
sion from sternite XIV.
Color. — "...light greenish yellow, banded with
vermilion on the branchial regions and abdomen.
Appendages red, antennary flagellum trans-
versely banded with light and dark" (Faxon
1893).
Maximum size. — In the meager material avail-
FIGURE 36.— Sicyonia affinis,i 21.5 mm cl, 4.4 km off Isla Manuelita, Costa Rica. A , Petasma, dorsal view; B, ventral view of same;
C, right appendix masculina, dorsolateral view. Scales = 1 mm.
45
FISHERY BULLETIN: VOL. 83, NO. 1
Figure 37.— Sicyonia affinis, 9 17 mm cl, 4.4 km off Isla Ma-
nuelita, Costa Rica. Thelycum. Scale = 1 mm.
able, larger male 21.5 mm cl, about 46 mm tl;
largest female, 17 mm cl, about 62 mm tl.
Geographic and bathymetric ranges. — Known
with certainty only from a restricted area between
Isla Manuelita (5°34'N, 87°00'W), Costa Rica, and
Isla de Malpelo (3°58'20"N, 81°36'00"W), Colom-
bia (Fig. 38). Chirichigno Fonseca (1970) and
Arana Espina and Mendez G. (1978) cited Paita,
Peru, as the southern limit of the range of the
species. Chirichigno Fonseca did not present a list
of her material and Matilde Mendez G.^ found no
representative of the species in Peruvian collec-
tions, including those of the Instituto del Mar del
Peru (IMARPE) from which Chirichigno Fonseca
obtained most of her information. Chapa Saldaha
(1964) recorded the occurrence of this species in
the waters of Chiapas and Sinaloa, Mexico, but
again, more recent studies, including the present
one based on extensive material, failed to disclose
its presence north of Costa Rica. Further investi-
gations are necessary to ascertain the limits of the
range of this shrimp both south of Isla de Malpelo
and north of Isla Manuelita. Sicyonia affinis is one
of only four members of the genus that have been
recorded from the eastern Pacific off South
America.
This species has been found at depths between
79-77 and 205 m, on substrates of rocks or broken
shells.
Discussion . — Sicyonia affinis is one of the three
closely related American Pacific species belonging
to Burkenroad's (1934a) "affinis group" of his Divi-
sion II. He characterized this group (in which he
included S. affinis and S. aliaffinis, and to which
* S. affinis
* S. aliaffinis
* S . martini
'Matilde Mendez G., Instituto del Mar del Peru, Callao, Peru,
pers. commun., January 1984.
46
Figure 38. — Geographic distribution of Sicyonia affinis, S.
aliaffinis, and S. martini.
P6REZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
recently Perez Farfante and Boothe (1981) added
S. martini^ as possessing two teeth posterior to the
orbital margin, of which one, that posterior to the
level of the hepatic spine, is large. Like all mem-
bers of Division II, in S. affinis the antennal spine
is buttressed, but the buttress is barely distinct in
contrast to that in S. aliaffinis and S. martini in
which it is well developed. In S. affinis the first
rostral tooth is situated farther anteriorly, at
about the end of the anterior third of the rostral
length from the orbital margin, than in the other
two species in which it is placed opposite or im-
mediately anterior to the orbital margin.
In S. affinis the abdominal surface is punctate
but otherwise rather smooth, lacking tubercles,
conspicuous ridges, and deep sulci. Also, in S.
affinis the anteromedian sulcus of the first abdom-
inal somite is not only weak but short, whereas in
S. aliaffinis and S. martini it is deep (except ven-
trally in S. martini in which it is represented by a
shallow depression) and long, in S. aliaffinis al-
most reaching the ventral margin of the pleuron.
The anteromedian sulci of the second and third
somites in S. affinis are distinct only ventrally,
rather than dorsally as in S. martini, or along
most of the height of the somite, as in S. aliaffinis.
The posteromedian sulci of these somites in S.
affinis extend dorsally only to a point situated at
about 0.33 of the height of the somite from the
dorsal midline where they turn anteriorly and are
marked dorsally by weak longitudinal ridges;
these sulci are considerably shorter than the well-
incised ones in S. aliaffinis, which extend to about
the dorsal 0.25 of the height of the somite, and are
not accompanied dorsally by longitudinal ridges.
In S. martini the posteromedian sulci curve an-
teroventrally at their dorsal ends, defining strong
angular ridges.
As Burkenroad (1934a) pointed out, in iS. affinis
the dorsal carina of the fifth abdominal somite
does not end in a sharp angle or acute tooth as it
does in the other two species; instead its posterior
part slopes gradually to the apex of the caudal
cleft. In S. affinis the tip of the tooth on the first
abdominal somite is slightly curved anteriorly
whereas in S. martini it forms a conspicuous hook,
and in S. aliaffinis the entire tooth is straight and
projects anterodorsally Furthermore, the antero-
ventral extremities of the pleura of the first four
somites in S. affinis are unarmed whereas they
bear a small spine in S. aliaffinis , and in S. mar-
tini, although lacking spines, are strongly angular
instead of faintly so or rounded as they are in S.
affinis.
These three species can also be distinguished
readily by petasmal and thelycal characters. In S.
affinis the projection of the dorsolateral lobule of
the petasma, like that of S. aliaffinis, is truncate
or shallowly emarginate distally and produced in
a simple, dorsally directed, sharp salient, whereas
in S. martini the projection curves gently to a
conspicuously bifurcate, mesially directed tip; on
the other hand, in S. affinis, as in S. martini, the
projection of the ventrolateral lobule is fiattened
and curved or concave dorsally rather than being
strongly bulbous as it is in S. aliaffinis. In the
females of S. affinis and S. martini the thelycal
plate of sternite XIV bears a pair of low but well-
marked lateral bulges (longitudinally disposed in
the former and transversely so in the latter),
whereas in S. aliaffinis the plate is almost flat or
barely raised in ill-defined elevations. Moreover,
in both S. affinis and S. aliaffinis, the posterior
emargination of the median plate of sternite XIII
does not embrace a tubercle, as it does in S. mar-
tini.
Material. — 17 specimens from 6 lots.
Costa Rica— 3c5 59, AHF, 4.4 km off Isla Ma-
nuelita, 146 m, 3 June 1973, Velero IV stn
19044. 16 , syntype, USNM, off Isla del Coco, 95
m, 28 February 1891, Albatross stn 3369. 16 19,
syntypes, MCZ, off Isla del Coco, 183 m, 28 Feb-
ruary 1891, Albatross stn 3367.
Panama— 39, USNM, NE of Isla Iguana, 79-77
m, 4 May 1967, Pillsbury stn 515.
Colombia — 19, syntype, MCZ, W of Isla de Mal-
pelo, 95 m, 5 March 1891, Albatross stn 3379. 29 ,
syntypes, USNM, W of Isla de Malpelo, 205 m, 5
March 1891, Albatross stn 3378.
Sicyonia aliaffinis (Burkenroad 1934)
Figures 38-42
Eusicyonia aliaffinis Burkenroad, 1934a:92, fig. 24
[holotype 6, YPM 4393; type-locality: Pacific
coast of southern Mexico (NW of Puerto Ma-
dero), 14°48'40"N, 92°54'40"W, 19-30 fm (35-
55 m), 9 April 1926, Pawnee]. Burkenroad
1938:84, fig. 25, 27. Anderson and Lindner,
1945:317.
Eusicyonia sp. Castro, 1966:17 [in part, by im-
plication].
Sicyonia aliaffinis. Chapa Saldana 1964:
15. Bayer et al. 1970:A97. Chirichigno
Fonseca 1970:7, fig. 6. Del Solar 1972:
7. Rodriguez de la Cruz 1977:10. Arana
Espina and Mendez G. 1978:25, fig. 6-9.
47
FISHERY BULLETIN: VOL. 83, NO. 1
Anonymous 1980:7. Brusca 1980:256.
Sosa Hernandez et al. 1980:12. Mendez G.
1981:47, pi. 9, fig. 78-82. Perez Farfante and
Booths 1981:424. Perez Farfante 1982:370.
Vernacular names: rock shrimp, target shrimp,
Japanese shrimp (United States); camaron de
piedra, camaron de roca, camaron japones,
cacahuete (Mexico); camaron conchiduro
(Mexico, Panama); camaron de mar, camaron
cascaradura (Peru). FAO names: hardhusk
rock shrimp (English); camaron cascara dura
(Spanish); boucot noisette (French).
Diagnosis. — Antennal spine well developed and
buttressed. Second abdominal somite with dor-
somedian carina lacking incision. First pereopod
with basis and ischium unarmed. Postrostral
carina bearing one tooth posterior to level of he-
patic spine and raised in high crest behind pos-
terior tooth. Rostrum short, not overreaching dis-
tal margin of eye. Abdomen tuberculate; second
and third somites not bearing special inverted
V-shaped ridges laterally; fifth somite with dor-
somedian carina ending in sharp angle or tooth
posteriorly. Petasma with distal projection of dor-
solateral lobule compressed distally, its truncate
tip produced dorsally in simple, minute spine.
Thelycum with plate of sternite XIV lacking an-
teromedian tubercle and either flat or barely
raised in ill-defined bulges. Branchiostegite bear-
ing large, horizontally disposed 9-shaped color
pattern.
Description. — Body relatively short (Fig. 39).
Carapace with irregular patches of longer setae on
dorsum, in depression delimiting branchiocardiac
carina posterodorsally, and on areas anterior to
hepatic spine and ventral to hepatic sulcus; one
patch also present in dorsolateral depression of
sixth abdominal somite. Abdomen rather heavily
granulate on first three abdominal somites, usu-
ally slightly so on last somites.
Rostrum short, not overreaching distal margin
of eye, its length increasing linearly with carapace
length (Fig. 40) to about 16 mm cl, then increasing
little, not surpassing 6 mm (proportional length
decreasing with increasing size from as much as
0.43 to as little as 0.20 cl); subhorizontal or up-
turned to 30° in males and to 50° in females; armed
with two dorsal teeth and three (occasionally two)
apical ones, latter disposed on obliquely truncate
apex, upper tooth posterior to level of ventral one
(occasionally appearing to be third of dorsal
series); first dorsal tooth subequal to or, more often
slightly smaller than, epigastric and situated op-
posite or immediately anterior to orbital margin;
second tooth variably placed between anterior 0.17
and 0.40 (mean 0.30) rl. Conspicuous adrostral
carina, subparallel and near ventral margin, ex-
FlGURE 39. — Sicyonia aliaffinis (Burkenroad 1934), 9 26 mm cl, west of Puerto Madero, Golfo de Tehuantepec, Mexico. Lateral
view. Scale = 5 mm.
48
PfiREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
t)
•
1 6
J
•
• •
■^L-^
^^
•
/T
.I'''**
0»
c
t
• ,
^•«i
*• •
J.--
•
— 4
* .
/
. .••«
E
3
J^
\
k
• *>*
M
j^ •
o
2
yV% •
y^9
12 18 24
carapace length (mm)
30
Figure 40. — Sicyonia aliaffinis. Relationship between rostrum
length and carapace length (regression equation for specimens
with about 16 mm cl or less,^' = 0.83950 + 0.25635x; regression
equation for those larger, y = 2.34086 + 0.13665x).
tending from orbital margin almost to end of ros-
trum.
Carapace with strong postrostral carina bear-
ing two teeth: 1) epigastric tooth small, subequal
to or slightly larger than first rostral tooth,
situated opposite or anterior to level of hepatic
spine, between 0.15 and 0.22 (mean 0.18) cl from
orbital margin; and 2) posterior tooth, much
larger, as much as three times higher than epigas-
tric, hooklike, its apical portion acutely pointed
and strongly curved anteroventrad; tooth placed
well in advance of posterior margin of carapace,
between 0.66 and 0.76 (mean 0.71) cl from orbital
margin. Postrostral carina slightly elevated just
in front of posterior tooth and forming high crest
from latter descending gently to posterior margin
of carapace. Tuft of setae present at anterior base
of each tooth. Antennal spine sharp, projecting
from well-marked buttress; hepatic spine acute,
larger than antennal, arising from raised area,
and situated between 0.19 and 0.26 (mean 0.23) cl
from orbital margin. Postocular sulcus deep an-
teriorly, continuing posteriorly as low groove;
hepatic sulcus well marked; branchiocardiac
carina distinct but rather low, extending longitu-
dinally from hepatic region almost to posterior
margin of carapace, there bifurcating: one branch
curving dorsally and other disposed ventrally.
Antennular peduncle with stylocerite produced
in long spine, its length about 0.9 distance be-
tween lateral base of first antennular article and
mesial base of distolateral spine; latter extending
to about midlength of second article.
Scaphocerite almost reaching or slightly over-
reaching distal margin of antennular peduncle;
lateral rib produced distally in long, strong spine
surpassing distal margin of lamella. Antennal
flagellum as much as 2 times as long as carapace.
Abdomen with high dorsomedian carina ex-
tending from first through sixth somites, carina on
first somite produced in strong triangular tooth as
high as, or usually higher (as much as one-third)
than, posterior tooth on carapace, its anterior
margin straight, subvertical or sloping anterodor-
sally; carina on fourth somite obliquely truncate
posteriorly forming obtuse (rarely almost right
angle); that on fifth strongly truncate forming
acute posterior tooth; and that on sixth strongly
produced in large acute posterior tooth.
First four somites with angular anteroventral
extremity bearing small spine; fourth somite with
posteroventral extremity broadly angular, occa-
sionally armed with minute spine, and fifth and
sixth somites with posteroventral extremity bear-
ing small sharp spine, that of fifth slightly larger.
First somite marked with long anteromedian
pleural sulcus joining coalescent posterior
tergal-posteromedian pleural sulci near margin of
pleuron. Second and third somites with deep an-
terior and posterior tergal and long, well-incised
anteromedian (expanding ventrally) and pos-
teromedian pleural sulci, posteromedian ones ex-
tending dorsally to a point located at least at 0.25
of the height of the somite from the dorsal midline.
Fourth somite bearing anterior and posterior ter-
gal sulci, posterior one merging with deep, long
posteromedian sulcus. Fifth somite marked with
anterior tergal sulcus and united posterior
tergal-posteromedian pleural sulci. Sixth somite
with short anterior tergal sulcus, strongly arched
posterior pleural one, and setose, longitudinal de-
pression delimited dorsally by rib and ventrally by
usually strong cicatrix.
Telson with pair of small but well-developed
fixed spines. Rami of uropod subequal in length,
reaching or slightly overreaching apex of telson.
Petasma (Fig. 41) with rigid distal projection of
dorsolateral lobule curved mesially, raised prox-
imodorsally in rounded prominence, and com-
pressed distally; its truncate tip with ventral ex-
tremity rounded and dorsal extremity sharply
produced in minute spine. Fleshy distal projection
of ventrolateral lobule with firm, terminal part
directed laterally almost at right angle, dorsally
bulbous, ventrally flat, and tapering to pointed,
ventrally inclined apex.
Petasmal endopods coupled in males 8.2 mm cl,
49
FISHERY BULLETIN: VOL. 83, NO. 1
Figure 41. — Sicyonta aliaffinis ,6 16 mm cl, west of Puerto Madero, Golfo de Tehuantepec, Mexico. A , Petasma, dorsal view;
B, ventral view of same; C, right appendix masculina, dorsolateral view. Scale = 1 mm.
about 27 mm tl, but may not be joined in individu-
als as much as 11 mm cl, about 36 mm tl.
Appendix masculina as illustrated in Figure
41C.
Thelycum (Fig. 42) with plate of sternite XIV,
delimited anterolaterally by strongly convex mar-
gins, flat or very slightly raised in paired ill-
defined bulges flanking depressed median portion.
Median plate of sternite XIII flask-shaped in out-
line, tapering gradually into long, slender spine
reaching as far as distal margin of coxae of an-
teriorly extended second pereopods; posterior
component of plate with posterolateral margins
strongly arched and separated by median emargi-
nation variable in width. Sternite XI armed pos-
teriorly with paired short spine. Posterior thoracic
ridge with weakly concave or virtually straight
anteromedian portion slightly elevated, but areas
lateral to it merging indistinctly with plate of
sternite XIV.
The smallest impregnated female encountered
has a carapace of 5 mm, about 23 mm tl.
Color. — Specimens from Peruvian waters were
described by Arana Espina and Mendez G. (1978)
as follows: dorsum dark, petroleum green;
carapace lighter laterally, exhibiting various
shades of gray, green, or pink, and bearing striking
dark mark resembling longitudinally disposed "9"
on branchial region. Antennae with light and dark
Figure 42. — Sicyonia aliaffinis, * 25 mm cl, west of Puerto
Madero, Golfo de Tehuantepec, Mexico. Thelycum. Scale = 2
50
PfeREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
bands. Pereopods and pleopods pink. In addition,
spot — dark proximally, intense blue distally —
present on lateral ramus of uropods. Sosa Hernan-
dez et al. (1980) also presented color notes on
specimens from the Golfo de Tehuantepec: body
cream, suffused with reddish brown; carapace
bearing hook-shaped brown mark on each side;
lateral ramus of uropod with violet ventral spot;
antennae banded with violet with cream. In
Anonymous' (1980) work on the crustacean dec-
apods of the Gulf of California, the "9" is described
as purplish brown.
Maximum size. — Male, 22.0 mm cl, 86.6 mm tl;
female, 28.5 mm cl, 100.7 mm tl (both recorded by
Arana Espina and Mendez G. 1978). Largest indi-
viduals examined by me: male, 21.4 mm cl, about
71 mm tl; female, 28 mm cl, about 89 mm tl.
Geographic and bathymetric ranges. — Isla Santa
Margarita (24°20'00"N, 111°45'30"W - 24°20'
10"N, 111°46'40"W), Baja California Sur, Mexico,
to Cabo San Lucas, in the southern part of the Gulf
of California along both the east and west coasts,
and southward to Bahia Chamela (19°34'00"N,
105°07'24"W), Jalisco. Also from off Salina Cruz
(16°10'00"N, 95°00'00"W), Oaxaca, Mexico, to
Santa Maria (12°24'S), Peru, except off middle
Central America, Colombia, and most of Ecuador.
In the waters of Ecuador, it has been recorded from
the Golfo de Guayaquil and Islas Galapagos (Fig.
38). This species has been found at depths between
4-9 and 242 m, mostly at <85 m, on substrates of
sand and mud.
The report of the occurrence of this shrimp in
Santa Maria, Peru, (Velez J., J. Zeballos, and M.
Mendez G., in press) is the first from waters south
of Bahia Sechura (5°43.1'S, 81°05.0'W), the
southernmost record cited by Arana Espina and
Mendez G. (1978). These specimens from Santa
Maria were collected at a depth of 10.5 m by A.
Robles on 28 June 1983.
Discussion. — The closest relative of S. aliaffinis is
iS. affinis. The former, however, reaches a larger
size (about 29 mm cl) than S. affinis, the largest
known specimen of which has only a 17 mm
cl. Sicyonia aliaffinis also differs from S. affinis
in having a strongly buttressed antennal spine
and in the position of the first dorsal rostral tooth,
which is situated opposite or barely anterior to the
orbital margin instead of at about the anterior end
of the basal third of the rostrum.
Differences in the abdominal characters are
even more striking. In S. aliaffinis the abdomen is
granulose, heavily so on the first three somites,
and the transverse sulci are deeply incised
whereas in S. affinis it is glabrous and bears weak
sulci, some of which are incomplete, adding to the
smooth appearance of the abdomen. In S. aliaffinis
the anteromedian sulcus of the first somite is long,
and although it becomes shallow ventral ly, it ex-
tends to near the ventral margin of the pleuron; in
S. affinis, in contrast, it is short, ending consider-
ably above the ventral margin of the pleuron. The
anteromedian sulci of the second and third somites
in iS. aliaffinis are long instead of short, recogniz-
able only on the ventral half of the somites; the
posteromedian sulci of these somites in S.
aliaffinis extend dorsally to a point at least at 0.25
of the height of the somite from the dorsal midline
and do not turn anteriorly, whereas in S. affinis
they extend only to about 0.35 from the dorsal
midline and turn anteriorly, delimiting ventrally a
weak longitudinal ridge which is absent in S.
aliaffinis. Also in iS. aliaffinis, the anterior tooth of
the first somite is acute but not curved at the tip as
it is in the other species, and the dorsal carina of
the fifth somite ends in a sharp angle or more often
in a tooth, whereas in S. affinis it slopes gradually
to the base of the caudal cleft. The anteroventral
extremities of the first through fourth pleura in S.
aliaffinis bear a small spine rather than being
unarmed.
Features of the external genitalia also allow a
ready separation of these two species. In S.
aliaffinis, the distal projection of the ventrolateral
lobule of the petasma is bulbous dorsally; in con-
trast, that of S. affinis is comparatively thin. The
thelycal plate of sternite XIV is flat or very faintly
raised laterally in ill-defined elevations in S.
aliaffinis, whereas in S. affinis it bears a pair of
low but well-marked ovoid or subellipticai bulges.
In addition to the morphological characters dis-
cussed above, S. aliaffinis exhibits a striking
9-shaped color pattern on the branchial region
which distinguishes it from all of its congeners
occurring in the American Pacific.
Discussing the diagnostic characters of S.
aliaffinis, Burkenroad (1934a) stated that "The
carina of the second somite is, although not
notched above the juncture of the tergal sulci,
shallowly emarginate at this point." I have ob-
served that this carina may be entire or slightly
depressed either at the point where Burkenroad
noted it or more posteriorly; consequently, in this
shrimp the contour of the carina is insignificant.
51
FISHERY BULLETIN: VOL. 83, NO. 1
Remarks. — Arana Espina and Mendez G. (1978)
graphed the size distribution of each sex in sam-
ples of this shrimp from the Golfo de Guayaquil.
They included correlations between carapace
length and total length, total weight, and abdomi-
nal weight. They determined that the relative
growth rate in males is higher than that in
females, and that within the size range of the
shrimp studied, eight molts occurred with an in-
crease of 7.25% at each molt.
Although Castro (1966) did not cite S. aliaffinis
by name, he stated that among the specimens of
"Eusicyonia" collected off Puerto Pehasco and near
Isla de San Jorge, Sonora, Mexico, there were some
bearing a 9-like shaped spot, which undoubtedly
indicates that they belonged to this species.
Commercial im,portance . — Sicyonia aliaffinis,
like the other six relatively large species of the
genus occurring in the American Pacific, is fre-
quently taken together with other penaeoids of
greater economic value. In the Gulf of California it
is present in the commercial catches made on the
eastern side. In some other areas along its range,
e.g., the Golfo de Guayaquil (Arana Espina and
Mendez G. 1978), it is found in quantities that
might support development of a fishery.
Material. — 251 specimens from 27 lots.
Mexico— Baja California Sur: 2c5 19, SIO, SW of
Isla Santa Margarita, 29-40 m, 13 November 1964,
Black Douglas . 16 , SIO, NW of Todos Santos, 38
m, 9 November 1964, Black Douglas. IS, YPM,
Bahia San Lucas, 24 m, 7 May 1936, Zaca stn
135D-26. Id 19, USNM, W of Estero de los Al-
godones, 47 m, 3 April 1978, Toral Garcia. Id,
YPM, Bahia Santa Ines, 37 m, 10 April 1936, Zaca
stn 141-D4. Nayarit: 57d 389 , SIO, NE of Isla
Maria Madre, 51 m, 31 March 1973, Agassiz. 15d
89, SIO, NE of Isla Maria Madre, 55 m, 31 March
1973, Agassiz. Jalisco: 19, USNM, Puerto
Vallarta, 13 April 1937. 29 , SIO, N part of Bahia
Chamela, 15-18 m, 2 April 1973, Agassiz. Oaxa-
ca: 13d 139, USNM, E of SaUna Cruz, Golfo de
Tehuantepec, 18 m, 10 July 1963, 1. Mayes A. 2d
19, SIO, Golfo de Tehuantepec, 55 m, 6 June 1965,
T. Matsui. 19, USNM, Laguna Lagartero,
Ixhuatan, 25 July 1963, G. Solorzano.
Chiapas: 2d 19, USNM, Puerto Arista, 14
January 1964, I. Mayes A. 8d 89 , SIO, Golfo de
Tehuantepec, 46-48 m, 10 April 1973, Agas-
siz. 3d 29 , SIO, Golfo de Tehuantepec, 73 m, 10-11
July 1963, D. Dockins. Id, holotype, YPM, off
"southern Mexico" [NW of Puerto Madero], 35-55
m, 9 April 1926, Pawnee. 17d 389, SIO, W of
Puerto Madero, Golfo de Tehuantepec, 55 m, 10
April 1973, Agassiz.
Guatemala — Id, AHF, off San Jose light, 42 m,
23 March 1939.
Costa Rica— Id , USNM, near Quepos, 242 m, 26
April 1973, Enriqueta.
Panama— Id, AHF, Isla Taboga, 4-9 m, 2 May
1939. Id, USNM, Bahia Santelino, 1.6 km N of
Punta de Cocos, Archipielago de las Perlas, 9 Feb-
ruary 1939. 19 , USNM, S of Isla del Rey 44-42 m,
7 May 1967, Pillshury stn 551. 19 ,USNM, SW of
Bahia San Miguel, 55 m, 7 May 1967, Pillsbury stn
549. 2d 19, USNM, 12 km NW of Punta
Caracoles, Darien, 84 m, L. G. Abele.
Ecuador— 19, USNM, S of Isla Seymour,
Galapagos, 7-13 m, 9 March 1938, F E. Lewis. 19 ,
USNM, off Playas, Golfo de Guayaquil, 16 m, 1976,
P Arana Espina.
Peru— Id, USNM, off Caleta Cruz, 10-14 m,
1970, E. Valdivia.
Sicyonia martini Perez Farfante and Boothe
1981
Figures 38, 43-46
Eusicyonia species, Burkenroad 1938:81, fig. 26,
28-30.
Sicyonia martini Perez Farfante and Boothe
1981:424, fig. 1-4 [holotype 9, USNM 180235;
type-locality: SW of Punta Ana Maria, Golfo de
Panama, 7°50'30"N, 78°49'00"W, 58 m,
Pillsbury stn 556].
Vernacular names: rock shrimp (United States);
camaron de piedra, camaron de roca (Mexico);
camaron conchiduro (Mexico, Panama).
Diagnosis. — Antennal spine well developed and
buttressed. Second abdominal somite with dor-
somedian carina lacking incision. First pereopod
with basis and ischium unarmed. Postrostral ca-
rina bearing one tooth posterior to level of hepat-
ic spine and raised in high crest behind posterior
tooth. Rostrum long, conspicuously overreaching
distal margin of eye. Abdomen tuberculate; second
and third somites bearing unusual inverted
V-shaped ridges laterally; fifth somite with dor-
somedian carina sharply truncate posteriorly.
Petasma with distal projection of dorsolateral
lobule tapering distally to minutely bifurcate tip,
arms sharp. Thelycum with plate of sternite XIV
bearing anteromedian tubercle. Branchiostegite
without 9-shaped color pattern.
52
PfeREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
Figure 43.—Sicyonia martini Perez Farfante and Boothe (1981), paratypec? 19 mm cl, off Puerto Escondido, Golfo de Panama.
Lateral view. Scale = 5 mm.
Description. — Body relatively slender (Fig. 43).
Carapace with sparse long setae intermingled
with elongate patches of shorter ones situated on
dorsum, ventral to hepatic sulcus, posterior to
pterygostomian region, and on posterodorsal part
of branchiostegite; patches also present on abdom-
inal terga. Abdomen tuberculate, tubercles
numerous on first five somites, few on sixth.
Rostrum comparatively long, conspicuously
surpassing eye, reaching as far as distal 0.33 of
second antennular article, its length, 0.40-0.54 cl,
increasing linearly with carapace length (Fig. 44);
armed with two or three dorsal teeth and cluster of
apical teeth, both groups varying in disposition
and number in males and females. In males, ros-
trum horizontal or directed upward at slight angle
of no more than 10°, but weakly decurved at tip,
with three dorsal teeth evenly spaced; first rostral
tooth situated immediately anterior to orbital
margin, last usually separated from upper apical
tooth by interval (about 0.33 rl) slightly greater
than that between dorsal teeth; apical cluster con-
sisting of three or four teeth (76% and 24% , respec-
tively), with subterminal ventral tooth situated
not far from adjacent apical tooth. In females, ros-
trum strongly elevated at angle of 40°-50°, its ven-
tral margin straight or, more often, strongly con-
vex along midlength, and with two dorsal teeth;
first rostral tooth placed distinctly anterior to orbi-
10
E
E
6 •
c
_«
E
3 4
10 15 20
carapace length (mm)
25
Figure 44. — Sicyonia martini. Relationship between rostrum
length and carapace length (regression equation, j = 0.76705 +
0.39436X).
tal margin; interval between second tooth and
upper apical tooth slightly shorter than that be-
tween first and second; apical cluster consisting of
three, four, or five teeth (1, 87, and 12%, respec-
tively), ventral one subterminal, distinctly re-
moved from adjacent apical tooth; teeth of apical
53
FISHERY BULLETIN: VOL. 83, NO. 1
cluster either turned ventrally, or less frequently
directed forward. Adrostral carina strong, some-
times sharp, reaching between level of last apical
tooth and base of ventral apical one.
Carapace with postrostral carina well-marked,
bearing two teeth: 1) epigastric tooth, small, sub-
equal to first rostral tooth, situated opposite or
only slightly anterior to hepatic spine; and 2) pos-
terior tooth, placed between 0.63 and 0.73 (mean
0.69) cl from orbital margin, large, about three
times as high as epigastric tooth, hooklike at tip;
postrostral carina low anteriorly, slightly elevated
below apex of posterior tooth, and forming crest
from latter descending gently toward ridge on
posterior margin of carapace; each tooth preceded
by tuft of long setae. Antennal spine small, project-
ing from rather long buttress; hepatic spine
acutely pointed, much longer than antennal, aris-
ing from moderately raised area, and situated be-
tween 0.14 and 0.20 (mean 0.18) cl from orbital
margin. Postocular sulcus short but deep an-
teriorly, continuing posteriorly as weak groove;
hepatic sulcus deep, subhorizontal, accompanying
inconspicuous carina. Branchiocardiac carina low
but clearly distinct, long, extending from base of
hepatic region to near posterior margin of
carapace, then curving dorsal ly toward base of
posterior tooth.
Antennular peduncle with stylocerite produced
in spine distally, extending about 0.8 distance be-
tween lateral base of first antennular article and
mesial base of distolateral spine; distolateral
spine strong, reaching as far as midlength of sec-
ond article; antennular flagella short, mesial one
slightly shorter than lateral.
Scaphocerite almost reaching (occasionally
overreaching) distal end of antennular pedun-
cle; length of antennal flagellum as much as 2.5
times cl.
Third maxilliped slightly stouter than
pereopods. Basis and ischium of first pereopod un-
armed.
Abdomen with high dorsomedian carina ex-
tending from first through sixth somites; carina on
first somite produced in large, apically hooked,
triangular anterior tooth, more elevated than
posterior tooth on carapace; carina of fifth somite
abruptly truncate posteriorly; and that of sixth
produced in large, acute posterior tooth.
Anteroventral margin of pleuron of first abdom-
inal somite barely to distinctly concave; antero-
ventral angle 90°-100°, that of third and fourth 90°
or less, with vertex slightly produced anteroven-
trally; pleuron of fifth roughly pentagonal, an-
54
teroventral and posteroventral angles with ver-
tices slightly produced, posteroventral one often
armed with small spine; posteroventral angle of
pleuron of fifth and sixth somites armed with
spine, that of fifth larger.
First somite with anteromedian sulcus well de-
fined only dorsally but continuing ventrally as
shallow depression joining deep posterior tergal-
posteromedian pleural sulcus, ridge often extend-
ing posteriorly from ventral portion of anterome-
dian pleural sulcus to fused posterior sulci. Second
and third somites with relatively short, anterior
and posterior tergal sulci; short anteromedian
pleural sulcus merging ventrally with conspicu-
ous broad depression, latter terminating near an-
teroventral margin of corresponding pleuron;
posteromedian pleural sulcus extending dorsally
to about 0.3 height of somite measuring from mid-
dorsal line, there curving anteriorly; special in-
verted V-shaped ridge Ijdng between tergal and
pleural sulci. Fourth somite with anterior tergal
and long, united posterior tergal-posteromedian
pleural sulci; anteroventral part of latter curving
dorsally; often short longitudinal ridge present at
about 0.3 height of somite from middorsal line.
Fifth somite with anterior tergal sulcus continu-
ous with united posterior tergal-posteromedian
pleural sulci, anteroventral portion of latter fad-
ing as shallow depression; cicatrix extending post-
eriorly from ventral end of anterior tergal sulcus.
Sixth somite with arched posterior pleural sulcus
and with shallow setose depression situated dorsal
to long but interrupted strong cicatrix.
Telson with pair of small, fixed, subterminal
spines. Both rami of uropod reaching, or almost
reaching apex of telson.
Petasma (Fig. 45 A, B) with rigid distal projec-
tion of dorsolateral lobule strongly curved me-
sially, raised proximodorsally in subhemispheric
prominence, and ending in bifurcate apex, both
tips sharp. Fleshy distal projection of ventrolat-
eral lobule falling short of adjacent one, and with
terminal part truncate and curved dorsally.
Petasmal endopods coupled in males as small as
5.8 mm cl, about 23 mm tl, but may not be joined in
individuals as large as 9 mm cl, about 32 mm tl.
Appendix masculina as illustrated in Figure
45C.
Thelycum (Fig. 46A, B) with plate of sternite
XIV forming slightly to broadly rounded lateral
flanges partly surrounding and merging with
roughly semicircular, low mesial bulges; latter
separated by median depression bearing oval or,
occasionally, subhemispheric anterior tubercle (if
P6REZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
Figure 45. — Sicyonia martini, paratyped 13.7 mm cl, south of Archipielago de las Perlas, Golfo de Panama. A, Petasma,
dorsal view; B, ventral view of same; C, right appendix masculina, dorsolateral view. Scale = 1 mm.
Figure 46. — Sicyonia martini. A , holotype? 21 mm cl, southwest of Punta Ana Mari a, Golfo de Panama; B ,9 16.5 mm cl,
Banco Gorda de Afuera, Baja California Sur Thelyca. Scales = 1 mm.
55
FISHERY BULLETIN: VOL. 83, NO. 1
oval, long axis disposed either longitudinally or
transversely). Median plate of sternite XIII
flaskshaped in outline, tapering into long, slender
spine reaching between anterior and posterior ex-
tremities of coxa of anteriorly extended second
pereopods; plate constricted, its ventral surface
strongly excavate at level of coxae of fourth
pereopods; posterior component of plate, with
rounded posterolateral margins and broad shal-
low, median emargination. Paired, broad based
spines projecting anteriorly from posterior margin
of sternite XI. Posterior thoracic ridge narrow,
with concave, sharp anteromedian margin but
merging laterally with preceeding plate.
The smallest impregnated females encountered
have a carapace of 8 mm, about 31 mm tl.
Color. — Specimens preserved in Formalin'* buff
with purplish blue markings: antenna, lateral
ridge of scaphocerite, postrostral and abdominal
carina, and dorsal ribs of telson transversely
banded; anterior margin and posterior ridge of
carapace, anterior margin of pleuron of first ab-
dominal somite, and posterior margin of all ab-
dominal somites with series of small spots; tip of
teeth on rostrum, carapace, and first abdominal
somite also purplish blue; lateral ramus of uropod
with subterminal spot on lateral ridge and large
mesial blotch at same level.
Maximum size. — Males 15.6 mm cl, 60.5 mm tl;
females 22.5 mm cl, 87.2 mm tl.
Geographic and bathymetric ranges. — From
southwest of Isla Santa Margarita (24°19'48"
N, lir47'06"W - 24°19'36"N, lir47'06"W),
Baja California Sur, Mexico, to southern tip of
Baja California Sur and throughout the Gulf of
California southward to off Punta Lizardo
(18°06'00"N, 102°5718"W), Michoacan; also from
E of Puerto Angel (15°41'00"N, 96°07'30"W),
Oaxaca, Mexico, to SW of Punta Ana Maria
( 7°50'30"N, 78°49'00"W - 7°50'48"N, 78°48'00"W),
Panama (Fig. 38). It has been found at depths
between 9 and 242 m, on substrates of sand, rock,
mud, and coralline debris.
D/scuss/on. — Although closely allied to S. affinis
and S. aliaffinis, S. martini can be distinguished
readily from both of them by the length, shape, and
armature of the rostrum; the shape of the tooth on
Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
56
the first abdominal somite; the sculpture of the ab-
domen; and features of the petasma and thelycum.
In S. martini the rostrum is quite long, surpass-
es the eyes, and almost reaches the distal margin
of the second antennular article. In males, the
rostrum is straight or upturned at an angle of no
more than 10°, and armed with three dorsal teeth
and three or four apical teeth, the ventral one of
which is occasionally subterminal. In females, the
rostrum is strongly elevated (40°-50°), with its
ventral margin usually markedly convex in the
middle and concave posterior to the base of the
subterminal tooth, and bears two dorsal teeth and
three to five apical teeth, the ventral one of which
lies distinctly posterior to the adjacent tooth. In S.
affinis and S. aliaffinis the rostrum is shorter than
in S. martini, reaching at most the distal margin
of the eye; in both males and females it is upturned
at an angle of about 30°, thus more elevated than
in males of S. martini but less so than in females,
and its ventral margin is usually straight or, occa-
sionally, slightly convex basally. Also, in these two
species the rostrum is armed with only two dorsal
teeth, and the ventral of the two or three apical
teeth (four or five have not been observed) is ter-
minal, instead of subterminal as it is in all females
and some males of S. martini.
The tooth on the first abdominal somite is pro-
portionately higher in S. martini than in the other
two species; its dorsal margin is sigmoid and it
ends in a strong, recurved, hooklike tip. In S.
affinis and S. aliaffinis the dorsal margin of the
tooth is gently curved in an arc, and the tooth is
inclined more anteriorly than in S. martini; in S.
affinis it ends in a slightly curved tip, and in S.
aliaffinis the tip is triangular rather than hook-
like. Also, the abdominal sculpture of S. martini is
much stronger than that of its two closest congen-
ers, and exhibits unusual, longitudinally disposed,
inverted V-shaped ridges at the ventral end of the
dorsal third of the second and third somites, which
are absent in the other two species.
In S. martini, the projection of the dorsolateral
lobule of the petasma is bifurcate apically, the tips
sharp. In S. affinis and S. aliaffinis, the projection
is compressed distally with the ventral extremity
rounded, the dorsal extremity sharply produced in
a simple spine, and the distal margin (im-
mediately ventral to the spine) truncate or
slightly emarginate. Furthermore, the projection
of the ventrolateral lobule of the petasma of S.
martini, like that of S. affinis but in contrast to
that of S. aliaffinis, is flattened distally rather
than thickened (dorsally) into a subovoid pro-
PfeREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
tuberance. The females of S. martini differ from
those of all the other Sicyonia occurring in the
region by possessing a conspicuous tubercle on the
anteromedian extremity of the plate of sternite
XIV.
In addition to the distinguishing characters
cited above, S. martini exhibits other features that
differ from those of S. affinis. The dorsomedian
carina of the fifth abdominal somite is abruptly
truncate; the abdomen is coarsely tuberculate and
the tergal sulci on the third through fifth somites
are deep. Sicyonia martini also differs from S.
affinis in the barely to distinctly concave (instead
of convex) anterior margin of the pleuron of the
first somite; the anteroventral extremity of the
four anterior pleura which are markedly angular,
forming angles of about 90° or less, rather than
being rounded or broadly angular; and the outline
of the fourth abdominal pleuron which is subpen-
tagonal and often bears a spine on the posteroven-
tral angle, whereas in S. affinis it is subcircular
and always unarmed.
Sicyonia martini differs further from S.
aliaffinis by the presence on the first abdominal
somite of a short but conspicuous longitudinal
ridge extending posteriorly from the ventral end of
the anteromedian pleural sulcus. The anterome-
dian and posteromedian pleural sulci of the second
and third abdominal somites are shorter than in
S. aliaffinis, extending dorsally only to about a
third of the height of the somite from the middor-
sal line rather than to a fourth, and the pos-
teromedian ones are curved anteriorly at their
dorsal extremities. Finally, S. martini lacks the
conspicuous purplish-brown mark (resembling a
longitudinally disposed "9" located posterior to the
hepatic sulcus and just ventral to the branchiocar-
diac carina) present in S. aliaffinis.
Material. — 193 specimens from 41 lots.
For list of records see Perez Farfante and Boothe
1981.
Sicyonia picta Faxon 1893
Figures 47-52
Sicyonia picta Faxon 1893:210 [syntypes: 4c? 29,
MCZ 4639, and 25 29, USNM 21172, off Golfo de
Panama (7°40'00"N, 79°17'50"W), 127 fm (232
m), 8 March 1891, Albatross stn 3387; 16 , USNM
21171, off Punta Mariato (7°12'20"N,
80°55'00"W), Panama, 182 fm (333 m), 23 Feb-
ruary 1891, Albatross stn 3355]. Faxon
1895:180, pi. 46, fig. 2, 2a-c. H. Milne Edwards
and Bouvier 1909:244. De Man 1911:
112. Bayer et al. 1970:A97. Arana Espina
and Mendez G. 1978:27, fig. 10-13. Brusca
1980:256. Mendez G. 1981:47, pi. 10, Fig.
83-86. Perez Farfante 1982:372.
Eusicyonia picta. Burkenroad 1934a:95, fig. 35,
1934b: 126, 1938:87. Anderson and Lindner
1945:318.
Vernacular names: rock shrimp, target shrimp,
Japanese shrimp (United States); cacahuete,
camaron de piedra, camaron de roca, camaron
japones (Mexico). FAQ names: peanut rock
shrimp (English), camaron cacahuete
(Spanish), boucot cacahouette (French).
Diagnosis. — Antennal spine well developed and
buttressed. Second abdominal somite with dor-
somedian carina lacking incision. First pereopod
with basis and ischium unarmed. Postrostral
carina bearing one tooth posterior to level of he-
patic spine and raised in high, arched crest behind
posterior tooth. Abdomen with tooth on dorsome-
dian carina of first somite conspicuously larger
than posterior tooth on carapace. Petasma with
distal projection of dorsolateral lobule slightly
curved mesially, its compressed tip produced dor-
sally in strong, hooklike spine. Thelycum with
plate of sternite XIV flat or slightly elevated lat-
erally; posterior component of median plate flat or
slightly raised laterally. Branchiostegite with
ocellus consisting of red center svirrounded by yel-
low ring.
Description. — Body relatively slender (Fig. 47).
Carapace sparsely studded with long setae and
bearing patches of shorter setae on dorsum; patch
also present anteroventral to hepatic sulcus,
another elongate obliquely disposed on bran-
chiostegite, and others on lateral depression and
anteroventral part of sixth abdominal somite. Ab-
domen with few small tubercles on first three so-
mites, most on row behind posterior sulci.
Rostrum short, usually not overreaching distal
margin of eye, its length increasing linearly with
carapace length (Fig. 48), but proportionately
longer in young (0.40-0.25 cl); in males (Fig. 49fi),
weakly arched, subhorizontal or upturned, usu-
ally not more than 25° but occasionally 30°, deep
basally, gently narrowing to slender, short tip (Fig.
49A); in females, nearly straight, raised 25°-40°,
deep along almost entire length, slightly narrower
and truncate apically; in both sexes armed with
two to four dorsal teeth and two or three apical
57
FISHERY BULLETIN: VOL, 83, NO. 1
Figure 47. —Sicyonia picta Faxon 1893. Syntype 5 19 mm cl, off Golfo de Panama. Lateral view. Scale = 5 mm.
ones (3 + 3, bmc; 4+3, 19%; 4+2, 22%; 3 + 2, 0.5%;
2 + 3, 0.5% ), dorsal teeth in females often crowded
anteriorly with apical ones, about evenly spaced
along margin in males. Adrostral carina, subpar-
allel and close to ventral margin, extending to base
of apical teeth.
Carapace with well-marked postrostral carina
bearing two teeth: 1) epigastric tooth small, sub-
equal to or only slightly larger than first rostral
tooth, situated distinctly anterior to hepatic spine,
between 0.13 and 0.16 (mean 0.15) cl from orbital
margin; and 2) posterior tooth, much larger, four
or five times higher, than epigastric, hooklike, its
apical portion acutely pointed and strongly curved
anteroventrally, situated far posterior to hepatic
spine but well in advance of posterior margin of
carapace, between 0.60 and 0.68 (mean 0.64) cl
from orbital margin. Postrostral carina low an-
teriorly, slightly elevated just in front of posterior
tooth, and forming high crest descending gently
from latter to posterior margin of carapace. Tuft of
setae present at anterior base of each tooth. An-
tennal spine sharp, projecting from short, low
buttress; hepatic spine considerably larger than
antennal, arising from moderately raised area,
and situated between 0.18 and 0.24 (mean 0.22) cl
from orbital margin. Postocular sulcus deep an-
teriorly, continuing posteriorly as low groove;
58
B
• ■
?*
•
•
^
X
1-
•
^
•
^
0»
c
y^
•
£. 4
•
V^
•
E
•^
• •
3
A^
•
1
S^ •
M
• J
• •
0
V*
w
^
kr?
2
V
10 15 20
carapace length (mm)
25
Figure A&.— Sicyonia picta. Relationship between rostrum
length and carapace length (regression equation, y = 0.51173 +
0.26668X).
hepatic sulcus deep; hepatic carina indistinct;
branchiocardiac carina recognizable only pos-
teriorly, extending for short distance subparallel
to slope of posterior tooth, then curving dorsally
to posterior margin of carapace.
Antennular peduncle with stylocerite produced
in long spine, its length 0.75-0.85 distance be-
tween lateral base of first antennular article and
I
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
mesial base of distolateral spine; latter, slender
and sharp, extending to about midlength of second
antennular article; antennular fiagella short, me-
sial one slightly shorter, 0.20-0.30 cl, than lateral,
0.25-0.35 cl.
Scaphocerite extending to midlength of third
antennular article or slightly overreaching it. An-
tennal flagellum about twice as much as twice
length of carapace.
Third maxilliped slightly stouter than
pereopods. Basis and ischium of first pereopod un-
armed.
Abdomen with dorsomedian carina extending
from first through sixth somites, carina on first
produced in strong, anterodorsally directed tooth
tapering to sharp apex and considerably larger
than posterior tooth on carapace; carina on fifth
produced in conspicuous sharp tooth and that on
sixth terminating in strong, acute one.
Anteroventral margin of pleuron of first abdom-
inal somite concave; posteroventral margin of first
through fourth somites rounded; anteroventral
extremity of pleuron of first through fourth so-
mites ending in spine, that of first directed ven-
trolaterally, those of second through fourth curved
posterolate rally. Pleuron of fifth and sixth somites
bearing posteroventral, caudally directed, rela-
tively small spine, that of fifth slightly larger than
that on sixth.
First abdominal somite traversed by anterome-
dian pleural sulcus, deep dorsally and disappear-
ing at about 0.30 height of somite before reappear-
ing ventrally as broad shallow depression merging
with united posterior tergal-posteromedian
pleural sulci. Second and third somites with an-
terior tergal and posterior tergal sulci joining an-
terodorsally; anteromedian pleural sulcus short
(not reaching dorsally posteromedian pleural) but
deep and merging with shallow anteroventral
depression, latter setting off subelliptical promi-
nence dorsally and low ridge posteriorly; pos-
teromedian pleural sulcus long, extending
anterodorsally ventral to (not joining) posterior
tergal. Fourth and fifth somites with anterior ter-
gal sulcus and curved, united posterior tergal-
posteromedian pleural sulci merging. Sixth so-
mite with arched posteromedian pleural sulcus
and longitudinal rib situated along base of mid-
dorsal carina and delimited ventrally by deep de-
pression lying just dorsal to weak cicatrix.
Telson with median sulcus deep anteriorly, in-
creasingly shallow posteriorly, its terminal por-
tion elongate and sharp, and bearing pair of small
fixed subterminal spines. Rami of uropod sub-
equal in length, falling slightly short of or barely
overreaching apex of telson.
Petasma (Fig. 50A, B) with rigid distal projec-
tion of dorsolateral lobule only slightly curved me-
sially, raised proximodorsally in rounded promi-
nence and compressed distally, its tip with ventral
extremity rounded and dorsal extremity produced
in strong, sharp spine directed dorsally. Fleshy
distal projection of ventrolateral lobule curving
laterally, roughly sickle shaped in outline, with
apex directed proximoventrally.
Petasmal endopods coupled in males as small as
6.7 mm cl, about 27 mm tl, but may not be joined in
individuals as much as 9 mm cl, about 34 mm tl.
Figure 49.— Skyonia picta. A, c? 16 mm cl, NW of Isla
Monserrate, Baja California Sur, Mexico. Lateral view of
carapace. Scale = 5 mm. B, syntjrpe 6 15.5 mm cl. Golfo
de Panama. Lateral view of dorsal part of cara-
pace. Scale = 2 mm.
59
FISHERY BULLETIN: VOL. 83, NO. 1
\gP
Figure 50. — Sicyonia picta, syntype 6 15.5 mm cl, off Golfo de Panama. A, Petasma dorsal view; fi, ventral view of same;
C, right appendix masculina, dorsolateral view. Scales = 1 mm.
Appendix masculina as illustrated in Figure
50C.
Thelycum (Fig. 51) with plate of sternite XIV
flat or slightly elevated laterally, inclined toward
broad median depression, and bordered anteriorly
and laterally by narrow, sometimes thickened,
flange. Median plate of sternite XIII flask-shaped
in outline or subtriangular, tapering anteriorly
into long, slender spine reaching between proxi-
mal end and midlength of basis of anteriorly ex-
tended second pereopods; plate at level of fourth
pereopods excavate and constricted by pair of shal-
low, widely separated lateral incisions; posterior
component of median plate, often convex laterally,
with rather deep median emargination. Paired
short spines projecting from posterior margin of
sternite XI. Posterior thoracic ridge narrow, with
well-marked anteromedian margin but flush with
lateral parts of plate of sternite XIV.
The smallest impregnated females encountered
have a carapace of 7 mm, about 28 mm tl.
Color. — Mendez G. (1981) described recently
caught specimens as follows: body light red or
orange red, with white areas on ventral part of
abdominal somites; carapace marked by conspicu-
ous ocellus consisting of red center surrounded by
yellow ring. Diffuse dark spot on lateral ramus of
60
Figure 51.— Sicyonia picta, syntype 9 28 mm cl, off Golfo de
Panama. Thelycum. Scale = 1 mm.
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
uropod situated distomesially according to her
figure 84. Antennae with alternating light and
dark red bands. In Formalin, body turns darker
red with ring around ocellus, garnet. Faxon (1893,
1895) noted that in specimens preserved in alcohol
there is a dark ring on the posterior part of the
branchial region and traces of color are present on
margins of rostrum, dorsal carinae, and append-
ages. In most specimens preserved in either
agent examined by me, the color pattern described
above is still distinguishable.
Maximum size. — Males 17.5 mm cl, about 70 mm
tl; females 24 mm cl, 87.9 mm tl (Faxon 1893 and
Arana Espina and Mendez G. 1978; corroborated
by me).
Geographic and bathymetric ranges. — Bahia
Magdalena (24°33'00"N, 112°00'30"W) to south-
ern tip of Baja California Sur, Mexico, throughout
the Gulf of California and southward to northeast
of Isla Maria Madre (22°00'N, 106°16'W), Nayarit,
Mexico; also from Champerico (13°55'36"N,
92°02'30"W), Guatemala, to Islas Lobos de Afuera
(06°45'S, 80°45'W), Peru (Fig. 52). It occurs at
depths between 16 and 400 m (shallowest cited by
Arana Espina and Mendez G. 1978), but most of
the recorded depths are <150 m. It occupies a large
variety of bottom types: sand, shell, sand and shell,
sand and mud, shell and mud, rock and mud,
green, grey and brown mud, broken gravel and
shells, and a mixture of mud, rocks, and coralline
detritus.
Discussion. — Sicyonia picta is most similar to S.
disdorsalis; both are of moderate size and in addi-
tion bear a small epigastric tooth, a large posterior
tooth on the postrostral carina, and a strongly
developed one on the first abdominal somite. These
shrimps can be readily separated by their color
pattern and a number of morphological characters.
In S. disdorsalis an ocellus is lacking on the pos-
terior part of the branchiostegite, the rostrum is
slender throughout its entire length, and less ele-
vated than in S. picta, its inclination not exceed-
ing 20°; the epigastric and posterior teeth on the
postrostral carina are situated closer to the orbital
margin, between 0.06 and 0.12 (mean 0.10) cl and
0.55 and 0.65 (mean 0.60) cl, respectively; and the
posterior tooth rises from a uniformly low post-
rostral carina.
The two species also differ in sculpture of the
abdomen. In S. disdorsalis the first abdominal
somite is traversed by a short anteromedian sul-
cus which is not represented ventrally by a depres-
sion; the posterior tergal and posteromedian
pleural sulci of the second and third somites are
coalescent; the anteroventral extremities of the
second through fourth are unarmed or are pro-
duced in a small, ventrally projecting spine; and
the posteroventral extremities of first through
fourth somites are angular, that of the fourth bear-
ing a well-developed spine, and that of the fifth,
an extremely long one (instead of small as in S.
picta) in adults.
In both species the petasma and the thelycum
also exhibit distinctive features. In S. disdorsalis
the distal projection of the distolateral lobule of
the petasma terminates in an acute tip rather
than being compressed laterally and produced in a
• S. picta
A S. disdorsalis
* S. in gent is
FIGURE 52.— Geographic distribution of Sicyonia picta, S. dis-
dorsalis, andS. ingentis.
61
FISHERY BULLETIN: VOL. 83, NO. 1
dorsally directed salient as it is in S. picta. Fur-
thermore, the distal projection of the ventrolateral
lobule in S. disdorsalis is laminar, bifurcate later-
ally, and bears a proximal plate bordered by a
transverse rib; in S. picta, it is roughly sickle
shaped in outline, tapering laterally to a sharp
proximoventrally directed apex. Finally, the
thelycal plate of sternite XIV in S. disdorsalis is
raised in a low but well-defined pair of lateral
protuberances instead of being flat or slightly
raised laterally as it is in S. picta.
In the field, S. picta may be distinguished from
its sympatric congeners by the striking yellow
ocellus with a red center located on the bran-
chiostegite.
Burkenroad (1938) discussed in detail the fea-
tures that distinguish S. picta from the western
Atlantic S. stimpsoni Bouvier 1905. Actually, fea-
tures cited by him for S. stimpsoni also apply to S.
burkenroadi, another western Atlantic species
which was not recognized until described by Cobb
in 1971. S icy onia picta differs from S. stimpsoni,
but resembles S. burkenroadi, in bearing strongly
curved spines on the anteroventral angles of the
second through fourth abdominal pleura. It, in
turn, can be separated from .S. burkenroadi, but
resembles S. stimpsoni, in lacking a posterior
tooth on the tergal carina of the fourth abdominal
somite.
Remarks. — Arana Espina and Mendez G. (1978)
presented an illustration (Fig. 11) in which the
posterior tergal and posteromedian sulci of the
second and third abdominal somites appear co-
alescent. The disposition of the posteromedian sul-
cus seems to be in error because, as stated above,
the two sulci in this shrimp do not merge; instead
the posteromedian one extends anterodorsally,
ventral to the posterior tergal sulcus.
In addition to citing many new localities, this
paper contains the first records of the species from
the ocean side of Baja California Sur, Mexico, as
far north as Bahia Magdalena.
Material.— 602 specimens from 61 lots.
Mexico — Baja California Sur: 19, AHF, 5.5 km
W of mouth of Bahia Magdalena, 64 m, 8 March
1949, Velero IV. U, USNM, off Isla Santa Mar-
garita, 86 m, 8 April 1889, Albatross stn
3039. 16 29, SIO, off Punta Marquez, 64 m, 9
November 1964. 29, SIO, Bahia de la Paz, 82-119
m, 12 January 1968, Thomas Washington . 26 69 ,
SIO, Bahia de la Paz, 119-128 m, 24 July 1965, R.
Rosenblatt. 1<5, AHF, entrance to Bahia Agua
62
Verde, 42-48 m, 17 March 1949, Velero IV. 66 119,
SIO, NW of Isla Monserrate, 170-192 m, 11 July
1965, Horizon. 29, AHF, NW of Isla Danzante
Primero, 44-73 m, 18 March 1949, Velero IV. 16 ,
YPM, Bahia de Santa Ines, 101 m, 17 March 1926,
Pawnee. 49, SIO, off Santa Rosalia, 35-26 m, 25
March 1960, R. Parker Baja California Norte
(all in Gulf of California): 19, YPM, Bahia de los
Angeles, 31-42 m, 13 May 1926, Pawnee. 3d 19,
AHF, Puerto Refugio, Isla Angel de la Guarda,
143-165 m, 28 January 1940. 39 , AHF, N of Isla
Angel de la Guarda, 104 m, 28 January 1940. 66
119, SIO, SE of San Felipe, 75-86 m, 19 January
1968, Washington. 16, YPM, Bahia San Luis
Gonzaga, 17 May 1916, Pawnee. 16 19, USNM,
off Punta San Fermin, 55 m, 27 March 1889, Alba-
tross stn 3035. 19 , SIO, SE of San Felipe, 120 m,
19 January 1968, Washington. Sonora: 26
29, USNM, off Cabo Tepoca, 65 m, 24 March 1889,
Albatross stn 3018. 266 299, USNM, SW of Cabo
de Lobos, 139 m, 24 March 1889, Albatross stn
3016. 16 , USNM, NW of Isla Tiburon, 265 m, 24
March 1889, Albatross stn 3015. 4(5 19, AHF, 3
km W of Tastiota, 60 m, 21 December 1978, A.
Kerotitch. Sinaloa: 3d 29 , USNM, off Punta
Santo Domingo, 135 m, 10 April 1889, Albatross
stn 3043. 19 , USNM, off Peninsula de Quevedo,
67 m, 30 March 1978, Toral Garcia. Nayarit:
26 49, SIO, NE of Isla Maria Madre, Islas Tres
Marias, 82-88 m, 30 March 1973, Agassiz.
Guatemala— 19, SIO, Champerico, 91-104 m, 13
April 1973, Agassiz.
Nicaragua— 29, SIO, off N of Nicaragua, 53-59
m, 17 April 1973, C. Hubbs and S. Luke.
Costa Rica— Id 19 , USNM, Golfo del Papagallo,
2 April 1978, D. Hedgecock. Id, SIO, Punta
Guiones, 104 m, 19 April 1973, C. Hubbs and S.
Luke. 1505 1509 , SIO, Golfo de Nicoya, 86 m, 22
April 1973, A^ass/e. 6d 19, SIO, off Cabo Blanco,
60 m, 18 April 1973, Agassiz. 19, UCR, off Cabo
Blanco, 249 m, 28 April 1973, Enriqueta. 16 149,
SIO, off Cabo Blanco, 137-144 m, 19 April 1973, C.
Hubbs and S. Luke. 19 , USNM, off Cabo Blanco,
247 m, 27 April 1973, Enriqueta.
Panama— Id 19, AHF, Islas Secas, 46-48 m, 27
March 1939. 2d 69 , AHF, off Isla Medidor, 55-64
m, 28 March 1939, Velero III. 26 89, UR 25 km
S of Isla Cebaco, 256 m, 8 August 1972,
Canopus. 16, syntype, USNM, off Punta
Mariato, 333 m, 23 February 1891, Albatross stn
3355. Id 19 , USNM, E of Isla Iguana, 79-77 m, 2
May 1967, Pillsbury stn 502. 39, USNM, NE of
Isla Iguana, 79-77 m, 4 May 1967, Pillsbury stn
515. 4d 29, MCZ, and 2d 29, USNM, syntypes.
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
off Golfo de Panama, 232 m, 8 March 1891, Alba-
tross stn 3387. IS 29 , USNM, S of Isla San Jose,
84 m, 6 May 1967, Pillsbury stn 529. bS 69,
USNM, S of Isla San Jose, 99 m, 7 May 1967,
Pillsbury stn 553. 19 , USNM, SE of Isla San Jose,
68 m, 7 May 1967, Pillsbury stn 555. 26 39,
USNM, SE of Isla San Jose, 60 m, 5 March 1888,
Albatross stn 2797. 26 , USNM, S of Isla del Rey,
44-47 m, 7 May 1967, Pillsbury stn 551. 16 19,
USNM, S of Isla del Rey, 59 m, 8 May 1967,
Pillsbury stn 556. 16 59 , USNM, SW of Golfo de
San Miguel, 64-60 m, 7 May 1967, Pillsbury stn
550.
Colombia— Call: 2c?, USNM, off Bahia de
Buenaventura, 80 m, 16 September 1966, Anton
Bruun, 18B, stn 783.
Ecuador — Manabi : many 6 and 9 , USNM, off
Cabo Pasado, 93 m, 12 September 1966, Anton
Bruun, 18B, stn 778. 16 39, USNM, off Bahia de
Manta, 120-150 m, 12 September 1966, Anton
Bruun, 18B stn 776. 36 39, USNM, off Cabo San
Lorenzo, 185 m, 12 September 1966, Anton Bruun,
18B, stn 775. 16 19 , AHF, off Isla La Plata, 82-101
m, 10 February 1934. El Oro: 26 , USNM, SW
of Isla Santa Clara, depth unrecorded, 10 Sep-
tember 1966, Anton Bruun, 18B, stn 769-D. 27d
679, USNM, SW of Puerto Bolivar, 80 m, 10 Sep-
tember 1966, Anton Bruun, 18B, stn 769.
Peru— Tumbes: lid 89, USNM, off Casitas,
90 m, 8 September 1966, Anton Bruun, 18B, stn
764. Piura: 46 49, USNM, Bahia de Paita,
70-69 m, 8 September 1966, Anton Bruun, 18B, stn
762-A. 26 49 , USNM, Bahia de Paita, 118-133 m,
2 June 1966, Anton Bruun, 16, stn 625-A. 16,
USNM, SW of Isla Foca, 120 m, 7 September 1966,
Anton Bruun, 18B, stn 761. 46 109, USNM, off
Punta Negra, 100 m, 4 June 1966, Anton Bruun,
16, stn 631- A. Lambayeque: Id 19 , IMARPE,
Islas Lobos de Afuera, 360-400 m, 1977, R. Mar-
quina.
Sicyonia disdorsalis (Burkenroad 1934)
Figures 52-56
Eusicyonia disdorsalis Burkenroad 1934a: 96, fig.
25, 36 [syntypes: Id 19, YPM 4391, 5d 69 (not 4d
79 as originally cited), YPM 5075, and Id 19,
YPM 4391, Pearl Islands (Archipielago de las
Perlas), 8°29'40"N, 78°52'30"W, Golfo de
Panama, 19-24 fm (35-44 m), 31 March 1926,
Pawnee; 56 59 (not 6d 49), YPM 5079, and 19,
YPM 5078, Golfo de Panama, 1868, F H. Brad-
ley Id 39, YPM 5076, and Id, YPM 5077, west
coast of Central America, 1872, Capt. Dow].
Burkenroad 1938:87. Anderson and Lindner
1945:318.
Sicyonia disdorsalis. Chirichigno Fonseca 1970:7,
fig. 4. Bayer et al. 1970:A97. Del Solar et al.
1970:18. Rosales Juarez 1976:41, pi. 1, fig. 3.
Rodriguez de la Cruz 1977:11. Arana Espina
and Mendez G. 1978:29, fig. 14-17. Brusca
1980:256. Paul and Hendrickx 1980:
110. Sosa Hernandez et al. 1980:14.
Mendez G. 1981:48, pi. 10, fig. 87-90. Per-
ez Farfante 1982:370.
Vernacular names: rock shrimp (United States);
camaron conchiduro (Mexico, Panama); cama-
ron duro (Ecuador, Peru); langostino cascara
dura, camaron cascara dura (Peru). FAO
names: keeled rock shrimp (English), camaron
carenado (Spanish), boucot carene (French).
Diagnosis. — Antennal spine well developed and
buttressed. Second abdominal somite with dor-
somedian carina lacking incision. First pereopod
with basis and ischium unarmed. Postrostral
carina bearing one tooth posterior to level of he-
patic spine and low throughout its entire length,
not raised in crest behind posterior tooth. Abdo-
men with tooth on dorsomedian carina of first so-
mite considerably larger than posterior tooth on
carapace. Petasma with distal projection of dor-
solateral lobule curved mesially, tapering to apex,
and lacking filament. Thelycum with plate of
sternite XIV raised in pair of lateral bulges; pos-
terior component of median plate flat or slightly
raised laterally. Branchiostegite lacking large
spot or ocellus.
Description. — Body relatively slender (Fig. 53).
Carapace bearing patches of short setae on dor-
sum, antero ventral to hepatic spine, and ventral to
hepatic sulcus; patches of setae also present on
dorsal extremity of abdominal sulci and in depres-
sion of sixth abdominal somite. Abdomen with
numerous tubercles on first three somites.
Rostrum relatively short, rarely overreaching
eye, its length increasing linearly with carapace
length (Fig. 54) to about 18 mm cl, then increasing
little, not surpassing 6.2 mm ^proportional length
decreasing with increasing size from as much as
0.36 to as little as 0.21 cl); slender but occasionally
moderately deep; in males subhorizontal with tip
strongly decurved, in females upturned as much
as 20° with tip slightly decurved; armed with
three, occasionally two, dorsal teeth and two or
three apical teeth (2+2, 2%, 3+2, 92%, 3+3, 6%);
63
FISHERY BULLETIN: VOL. 83, NO. 1
Figure 53 . —Sicyoma disdorsalis (Burkenroad), ? 25 mm cl, Golfo de Fonseca, El Salvador. Lateral view. Scale = 10 mm.
ventral apical tooth smaller than dorsal and
placed almost at same level or, more often, pos-
terior to it. First rostral tooth located well in ad-
vance of orbital margin, between 0.18 and 0.33
(mean 0.25) rl; second tooth from 0.45 to 0.70
(mean 0.58) rl; and third from 0.75 to 0.96 (mean
0.81) rl. Adrostral carina extending to near tip,
relatively far from ventral margin, often slightly
arched either along middle or less often anteriorly,
and occasionally directed anterodorsally.
Carapace with postrostral carina well marked
but low throughout its entire length, bearing two
teeth: 1) epigastric tooth small, subequal to or
slightly larger than first rostral tooth and situated
well in advance of hepatic spine, between 0.06 and
0.12 (mean 0.10) cl from orbital margin; and 2)
posterior tooth, as large as or larger, sometimes as
much as three times higher, than epigastric,
acutely pointed, strongly inclined anteriorly, and
placed considerably in advance of posterior mar-
gin of carapace, between 0.55 and 0.65 (mean 0.60)
cl from orbital margin (both teeth farther anterior
in large individuals than in young). Tuft of setae
present at anterior base of each tooth. Antennal
spine moderately long, sharp, buttressed; hepatic
spine long, conspicuously larger than antennal,
projecting from raised area, and situated between
0.19 and 0.24 (mean 0.22) cl from orbital margin.
64
12 18
carapace length (mm)
24
30
FIGURE 54.— Sicyonia disdorsalis. Relationship between ros-
trum length and carapace length (regression equation for speci-
mens with about 18 mm cl or less, y = -0.03933 + 0.30998x;
regression equation for those larger, > = 2.33498 + 0.14502x).
Postocular sulcus deep anteriorly, continuing
posteriorly as very shallow arched groove; hepatic
sulcus subhorizontal; hepatic carina indistinct;
branchiocardiac carina weak.
Antennular peduncle with stylocerite produced
in long, sharp spine, its length 0.75-0.85 distance
between lateral base of first antennular article and
,1
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
mesial base of distolateral spine; latter long,
reaching as far as distal 0.25 of second antennular
article; antennular flagella short, mesial one,
more slender and shorter than lateral, 0.20-0.30 as
long as carapace; lateral flagellum 0.25-0.35 as
long.
Scaphocerite surpassing antennular peduncle
by no more than 0.1 its own length; lateral rib
ending distally in long, acute spine conspicuously
overreaching margin of lamella. Antennal flagel-
lum about twice as long as carapace.
Third maxilliped stouter than pereopods. Basis
and ischium of first pereopod unarmed.
Abdomen with dorsomedian carina extending
from first through sixth somites, carina on first
produced in strong, anteriorly inclined tooth, ta-
pering suddenly near end to minute, sharp apex
(usually broken and thus appearing blunt); tooth
considerably larger than posterior one on car-
apace; carina on fifth somite abruptly truncate or
produced in sharp tooth posteriorly, and that on
sixth terminating in strong, acute posterior tooth.
Antero ventral margin of ple\iron on first abdom-
inal somite concave in adults, sometimes nearly
straight in juveniles, its extremity ending in
strong spine, that of second through fourth (in
adults) often projecting slightly or forming ven-
trally pointed spine; posteroventral extremity of
third through sixth somites sharply angular, that
of third often, but in last three always bearing
caudally directed spine, that of fifth and sixth
largest and smallest, respectively; additional
spine occasionally present immediately dorsal to
posteroventral one on fourth somite.
First abdominal somite marked with short, deep
anteromedian pleural sulcus and long, united
posterior tergal-posteromedian pleural sulci;
short, longitudinal ridge extending between an-
teromedian pleural and posterior sulcus. Second
and third somites with anterior tergal sulcus join-
ing united posterior tergal-posteromedian pleural
sulci dorsally, and with anteromedian pleural sul-
cus represented by shallow depression setting off
elevation at dorsal extremity. Fourth and fifth so-
mites bearing curved, united posterior tergal-
posteromedian pleural sulci; sometimes fourth
also with faint anterior tergal sulcus. Sixth somite
often marked by weak, sometimes indistinct,
arched, posteromedian sulcus and bearing con-
spicuous cicatrix frequently divided in two.
Telson with median sulcus well defined only
along anterior 0.65 of its length and armed with
pair of minute, fixed, subterminal spines; latter
clearly developed in juveniles but vestigial or lack-
ing in adults. Rami of uropod subequal in length,
falling slightly short of or barely overreaching
apex of telson.
Posterior spine on first abdominal sternite with
wide base and usually concave but sometimes
straight lateral margins.
Petasma (Fig. 55A, B) with cornified distal pro-
jection of dorsolateral lobule raised in prox-
FIGURE 55. Sicyonia disdorsalis , 6 17 mm cl, off Balboa, Panama. A, Petasma, dorsal view; B, ventral view of same; C, right
appendix masculina, dorsolateral view. Scales = 1 mm.
65
FISHERY BULLETIN: VOL. 83, NO. 1
imodorsal rounded prominence and ending in
acute tip curved mesially. Distal projection of ven-
trolateral lobule, falling short of projection of dor-
solateral lobule, laminar, bifurcate laterally, and
thickened proximally forming plate bordered dis-
tally by transverse rib; latter supporting long
proximal salient of bifurcation; terminal part of
projection truncate and curved dorsally.
Petasmal endopods joined in males as small as 3
mm cl, about 13 mm tl, but may be unjoined in
individuals with as much as 8.4 mm cl, about 21
mm tl.
Appendix masculina as illustrated in Figure
55C.
Thelycum (Fig. 56) with plate of sternite XIV
bearing pair of low protuberances bordered later-
ally (in adults) by narrow flanges, and separated
by moderately deep median depression. Median
plate of sternite XIII flask-shaped in outline, ta-
pering into long, slender spine reaching between
base and about midlength of basis of extended
second pereopod; plate set off from posterior com-
ponent by shallow incisions, flat or concave pos-
terolaterally, and with broad median depres-
sion (broader than areas and incisions flanking
it); posterior component of median plate flat or
slightly raised laterally, with posteromedian mar-
gin straight or convex. Paired short spines project-
ing anteroventrally from posterior margin of ster-
nite XI, spines broad basally, sharp and sometimes
produced in fine needle apically. Posterior thoracic
ridge narrow, with well-marked anteromedian
margin.
The smallest impregnated females encountered
have a carapace of 5.3 mm, about 25 mm tl.
Color. — Arana Espina and Mendez G. (1978) de-
scribed specimens from the waters of Peru as fol-
lows: Dorsum greenish gray, lighter-gray to pink
laterally Antennae red. Pereopods and pleopods
pink; merus of third maxilliped and pereopods
with red and yellow bands (toward distal end ac-
cording to their figure 15). Subdistal striking or-
namentation on lateral ramus of uropod consisting
of oval deep blue blotch bordered in yellow. In
contrast, Sosa Hernandes et al. (1980) found that
the specimens from southeast of Salina Cruz,
Golfo de Tehuantepec, Mexico, were cream with
orange hues.
My observations, based on a large number of live
specimens taken off Panama Viejo, Panama, indi-
cate a color pattern much, but not exactly, like that
noted by Arana Espina and Mendez G. Dorsum
of carapace gray with broad transverse dark
66
Figure 56. — Sicyonia disdorsalis, 9 16 mm cl, off Punta
Calabazo, Panama. Thelycum. Scale = 2 mm.
purplish band extending across epigastric tooth
and produced anteriorly in roughly pentagonal
spot reaching base of first rostral tooth. Bran-
chiostegite varying from dark purplish pink (in
most specimens) to milky white, sometimes with
grayish white longitudinal stripe along junction of
branchiostegite and dorsum. Abdomen gray with
middorsal carina banded: transverse dark gray
ones alternating with buff bands; large tooth pro-
jecting from carina on first somite purplish pink.
Anterior margin of pleuron of first three somites
bordered by white vertical stripe and posteroven-
tral areas of third and fourth somites also white.
Tergum of fifth somite bearing purplish pink
V-shaped (vertex anterior) marking posteriorly.
Telson and uropod gray with densely set yellow
chromatophores. Lateral ramus of uropod bearing
large garnet marking subdistally preceded by yel-
low patch, and contiguous to buff dot lying against
its mesial extremity. Antenna dark garnet. Third
maxilliped and pereopods pink, former with two
contiguous transverse bands, orange red one on
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
distal third of merus, followed by bright yellow
band crossing merus and proximal part of carpus;
fourth and fifth pereopods marked with orange red
band flanked by yellow ones extending across
merus and proximal part of carpus. Pleopods
mostly pink, lateroventral part of basis white.
Maximum size. — Males 21 mm cl, 88.8 mm tl;
females 28 mm cl, 98.7 mm tl (Arana Espina and
Mendez G. 1978). Largest specimens examined by
me: males 20 mm cl, females 25.7 mm cl.
Geographic and bathymetric ranges. — Bahia
Santa Maria (24°42'48"N, 112°13'54"W), to the tip
of Baja California Sur, Mexico, and from southern
Sonora, Gulf of California, southward to Pisco
(13°55'S), Peru(Fig. 52).
This species has been found between 5 and
139-93 m, but rarely in water deeper than 65 m;
contrary to most of its congeners from the Ameri-
can Pacific, it does not seem to range beyond the
continental shelf. It occurs on bottoms of mud,
detritus, fine sand, and rock and coral, seemingly
with no preference.
Abundant in the southeastern part of the Gulf of
California (Paul and Hendrickx 1980), it has not
been reported off northern Sonora or along the
east coast of Baja California; the present records
from these latter areas are the first for the species
north of Bahia San Lucas, a locality cited by Bur-
kenroad (1938). The southern limit, Pisco, Peru,
given here is also the first report of the presence of
this shrimp in waters south of San Lorenzo
(12°0.5'S), Peru, the southernmost locality cited
by Arana Espina and Mendez G. (1978). The record
from Pisco is based on specimens collected by M.
Mendez G. and J. Zeballos, at 5.5-13 m, on 5
November 1983 (Matilde Mendez G. footnote 3).
Discussion. — Burkenroad (1938) was the first to
point out some of the differences that separate this
species from its closest relative S. ingentis.
Sicyonia disdorsalis can be distinguished from the
latter by having 1) a sparsely setose carapace, 2)
a less elevated postrostral carina, 3) a weak, al-
most indistinct branchiocardiac carina, 4) a pos-
teriorly truncate carina on the fifth abdominal
somite that is sometimes produced in a spine, 5) an
anteromedian pleural sulcus on the first abdomi-
nal somite which ends abruptly far from the ven-
tral margin, and does not continue ventrally as a
shallow depression, 6) a strong spine on the an-
teroventral extremity of the pleuron of the first
abdominal somite, 7) angular posteroventral
pleural margins on the first two abdominal so-
mites, 8) minute telsonic spines in juveniles and
vestigial or indistinct ones in adults, and 9) short
uropodal rami that fall short of or barely surpass
the apex of the telson.
Various features of the genitalia also allow the
separation of iS. disdorsalis from S. ingentis. The
distal projection of the dorsolateral lobule of the
petasma is curved distomesially instead of extend-
ing distolaterally, and is not produced in a short,
apical filament; and the distal projection of the
ventrolateral lobule does not extend so far distally
as the projection of the dorsolateral lobule, is
bifurcate laterally, and bears a conspicuous trans-
verse rib. In the thelycum, the breadth of the fiat
or concave posterolateral areas of the median
plate, as well as the depth of the delimiting inci-
sions are much less than the depressed area be-
tween them. Furthermore, the posterior compo-
nent of the median plate is sometimes slightly
raised posterolaterally but not forming well-
defined lateral bosses traversed by a suture as in
S. ingentis.
The differences between S. disdorsalis and the
geminate western Atlantic S. dorsalis Kingsley
1878, were discussed in detail by Burkenroad
(1934a).
Commercial importance. — Throughout its range,
S. disdorsalis is present in the commercial catches
of other penaeoid shrimps. It was recorded by
Rosales Juarez (1976) in those off the coast of
Sinaloa, in the Gulf of California, and more re-
cently, on the basis of its abundance in the shrimp
bycatch from the waters off Sinaloa and Nayarit,
Paul and Hendrickx (1980) suggested that this
shrimp has a possible commercial value in that
area. Arana Espina and Mendez G. (1978) recorded
that in 1977 it made up to 5.8% of the total catches
made in northern Peru, a notable increase from
that of previous years in which it constituted
<0.5%. This species is considered by them to have
a significant economic potential.
Material. — 1054 specimens from 85 lots.
Mexico— Baja California Sur: 16 29, SIO,
Bahia Santa Maria, 0-37 m, 8 December 1962, H.
C. Perkins. 16, SIO, NW of Punta Marquez, 37
m, 4 December 1962, H. C. Perkins and R.
Wisner 16 , SIO, NW of Punta Marquez, 18 m, 4
December 1962, H. C. Perkins. 16 29, YPM,
Bahia San Lucas, 5.5 m, 7 May 1936, Zaca stn
135D-20. 26, YPM, Bahia San Lucas, 5-17 m, 7
May 1936, Zaca stn 135D-18-D19. Sonora: 7c?
29, USNM, Bahia de Lobos (boca sur), 30 m, 18
67
FISHERY BULLETIN; VOL. 83, NO. 1
July 1979, F. Paredes M. Sinaloa: 216 169,
SIO, Isla Altamura, 21-31 m, 26 May 1965, £/ Golfo
II stn 50-6. 29, USNM, off San Ignacio, 25 May
1962, R. Bush M. 19 , USNM, N of Mazatlan, 3.5
km off Marmol, 12 January 1964, A. Villania and
E. Chavez. 3d 89, SIO, off Boca Teacapan, 55 m,
25 August 1961, F. H. Berry Nayarit: 89,
SIO, W of Laguna de Agua Brava, 20 m, 24 August
1961, H. DeWitt. 26 79, SIO, SW of Laguna de
Agua Brava, 15 m, 24 August 1961, H. DeWitt and
H. C. Perkins. Id 159, SIO, NE of Isla Maria
Madre, 51 m, 31 March 1973, Agassiz. 29, SIO,
NW of mouth of Rio Grande de Soledad, 38-39 m,
24 August 1961, H. C. Perkins and H. De-
Witt. 30d 309 , SIO, Bahia de Banderas, 28-33 m,
2 June 1965, El Golfo II stn BT-150. 12d 149 , SIO,
Bahia de Banderas, 46-55 m, 21 August 1961, F. H.
Berry Id 19, SIO, Bahia de Banderas, 5-9 m, 19
August 1961, F H. Berry Jalisco: 29 , USNM,
Puerto Vallarta, 13 April 1937. lid 149, SIO,
Bahia Chamela, 15-18 m, 2 April 1973, Agas-
siz. 66 159, SIO, Bahia Chamela, 27-18 m, 2
April 1973, Agassiz. 16 39, AHF, Bahia Tenaca-
tita, 4-15 m, 8 May 1939. Michoacan: 19,
CAS, 14.5 km SE of Punta San Telmo (off Ma-
ruata), 17 July 1932, Zaca. 16 19, SIO, Punta
Lizardo, 22-24 m, 4 April 1973, Agassiz. 21d
25j, SIO, Punta Lizardo, 37-38 m, 4 April 1973,
Agassiz. Guerrero: 39, CAS, 6.5 km SE of
entrance of Bahia de Acapulco, 27 m, 5 April
1932, Zaca. Oaxaca: Id 19, USNM, 24 km
off Puerto Angel, 84-57 m, 13 July 1963, I.
Mayes A. 8d 49, SIO, Golfo de Tehuantepec, 55
m, 6 June 1965, El Golfo II, stn BT-162. 5d 49,
SIO, SW of Santiago Astata, 54 m, 6 June 1965, El
Golfo II, stn BT-162. Id 39, USNM, 16 km W of
Ayutla lighthouse, 54 m, 15 June 1963, I. Mayes
A. 7d 30t, SIO, off Salina Cruz, 44 m, 7 June
1965, El Golfo II. 59 , USNM, Salina Cruz, 64 m,
23 August 1963, I. Mayes A. 4d 29, SIO, off
Salina Cruz, 31-35 m, 8 July 1963, D. Dock-
ins. 19, SIO, off Salina Cruz, 49-73 m, 8 July
1963, D. Dockins. 44d 509, SIO, Golfo de
Tehuantepec, 22 m, 10 April 1973, Agassiz. 56
59, INP, off Tangola, 68 m, 10 July 1963, 1. Mayes
A. 5d , USNM, off Tangola, 139-93 m, 13 July
1963, 1. Mayes A.
Guatemala— 1j, AHF, San Jose, 4-9 m, 23
March 1939.
El Salvador— 3d 89, SIO, Golfo de Fonseca, 18
m, 17 April 1973, C. Hubbs and S. Luke. 6d 49,
SIO, Golfo de Fonseca, 18 m, 17 April 1973, C.
Hubbs and S. Luke. 5d 149, SIO, Golfo de Fon-
seca, 24-29 m, 17 April 1973, Agassiz.
68
Nicaragua — Id 59, USNM, off northern Nica-
ragua, 53-59 m, 17 April 1973, C. Hubbs and S.
Luke.
Costa Rica— 39, USNM, 3 km off Rio Savegre,
Puntarenas, 24 m, 2 December 1981, M. Hat-
ziolos. lOd 149 , SIO, Cabo Blanco, 60 m, 18 April
1973, Agassiz. 56 159, SIO, Cabo Blanco, 60 m,
18 April 1973, Agassiz. 16 29, AHF, Golfo de
Nicoya, about 1 km of east end of Islas Negritos
Afuera, 64 m, 29 June 1973, Velero stn
19132. 30d 309 , USNM, Golfo de Nicoya, 31 m, 22
April 1973, C. Hubbs and S. Luke. 40d 409, SIO,
Golfo de Nicoya, 31 m, 22 April 1973, Agassiz.
Panama— 19, USNM, off Bocas del Toro, 91-97
m, 26 January 1971, Pillsbury stn 1313. 5d 39,
SIO, Isla Cavada, Islas Secas, 40 m, 23 September
1970, W Newman, T Dana, S. Luke. 4d 49,
USNM, S of Rio Hato, 17 m, 1/2 May 1967,
Pillsbury stn 488. 19, USNM, Bahia de Parita,
22-18 m, 2 May 1967, Pillsbury stn 490." 19,
USNM, E of Chitre, 20 m, 2 May 1967, Pillsbury
stn 491. 2d 49, USNM, E of Chitre, 18-16 m, 2
May 1967, Pillsbury stn 492. 6d 69, USNM, N of
Isla Iguana, 37-33 m, 2 May 1967, Pillsbury stn
493. Id , USNM, southern end of Bahia Limon, 3
m, 23 July 1966, Pillsbury stn 449. 5d 59,
USNM, off Punta Calabazo, 20 m, 1 May 1967,
Pillsbury stn 486.. 2d , USNM, off Rio Hato, 15 m,
1 May 1967, Pillsbury stn 485. Id, USNM, En-
senada de Chame, Shimada stn 48. 2d 29,
USNM, S of Isla Bona, 31-26 m, 1 May 1967,
Pillsbury stn 484. 18d 149, USNM, E of Punta
Chame, 22 m, 1 May 1967, Pillsbury stn 483. 2d
19, USNM, off Balboa, surface, 9/10 May 1967,
Pillsbury stn 564. 20d 209, USNM, off Panama
Viejo, 4 m, 23 February 1973, I. Perez Far-
fante. 30d , USNM, off Juan Diaz, 12-22 m, 15
February 1973, Patricia. Id 79, USNM, Juan
Diaz, 5 m, 4 February 1969, L. G. Abele. Id 19,
USNM, W of Punta Brujas, 18 m, 6 May 1967,
Pillsbury stn 536. Id 19, syntypes, YPM, Ar-
chipielago de las Perlas, 35-44 m, 31 March 1926,
Pawnee. 56 69, syntypes, YPM, Archipielago de
las Perlas, 35-44 m, 31 March 1926, Pawnee. 56
59, syntypes, YPM, Golfo de Panama, 1868, F H.
Bradley. 19, syntype, YPM, Golfo de Panama,
1868, F H. Bradley Id 39, syntypes, YPM, W
coast of Central America, 1872, Capt. Dow. Id 39,
syntypes, YPM, W coast of Central America, 1872,
Capt. Dow.
Colombia— 19, USNM, Bahia Humboldt, 20
April 1967, Shimada stn 76B, haul 1. 29, USNM,
Bahia Humboldt, 20 April 1967, Shimada stn
76B haul 2. 69, USNM, off Timbiqui, Cauca,
PfeREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
38-35 m, 16 September 1966, Anton Bruun 18B
stn 785.
Ecuador— 19, USNM, Golfo de Guayaquil, 32
m, 11 September 1966, Anton Bruun 18B stn 772.
Peru— 13d 229, USNM, off Tumbes, 13 m, 10
September 1966, Anton Bruun 18B stn 768. 169,
USNM, off Caleta Cruz, Tumbes, November 1979,
Promaresa. 16d, USNM, off Caleta Cruz,
Tumbes, November 1979, Promaresa. 16d,
USNM, off Caleta Cruz, Tumbes, November 1979,
Promaresa. 169, USNM, off Caleta Cruz,
Tumbes, November 1979, Promaresa. 69,
USNM, off Negritos, 16 m, 2 June 1966, Anton
Bruun 16 stn 624-B. 26 19, USNM, Paita, 1969,
J. Sanchez and E. Valdivia. 29, USNM, NW of
Paita, 40 m, 1977.
Sicyonia ingentis (Burkenroad 1938)
Figures 52, 57-60
Eusicyonia ingentis Burkenroad 1938:88, fig. 31-34
[holotype: 6, AMNH 12388; type-locality: off
east coast of Cedros Island (Isla Cedros),
28°05'N, 115°09'W, Baja California, Mexico, 38
fm (69 m), 27 March 1936, Zaca stn 127D-
1]. Anderson and Lindner 1945:318. Feinberg
1971:6. Frey 1971:16.
Sicyonia ingentis. Parker 1964:162. Carlisle
1969:239. Longhurst 1970:272. Word and
Charwat 1976:19, 3 fig. Holthuis 1980:
61. Wicksten 1980:360. Perez Farfante and
Boothe 1981:424. Perez Farfante 1982:371.
"?Sicyonia sp.", Mathews and Gonzalez, 1975:51.
Sicyonia ringens. Mathews, 1981:329.
Vernacular names: ridgeback prawn, rock shrimp,
Japanese shrimp (United States); camaron de
piedra, cacahuete (Mexico). FAO names:
Pacific rock shrimp (English); camaron de
piedra del Pacifico (Spanish); boucot du Pa-
cifique (French).
Diagnosis. — Antennal spine well developed and
buttressed. Second abdominal somite with dor-
somedian carina lacking incision. First pereopod
with basis and ischium unarmed. Postrostral
carina bearing one tooth posterior to level of he-
patic spine and low throughout entire length, not
raised in crest behind posterior tooth. Abdomen
with tooth on dorsomedian carina of first somite
smaller or only slightly larger than posterior tooth
on carapace. Petasma with distal projections of
dorsolateral lobules divergent and bearing short
terminal filament. Thelycum with plate of ster-
nite XIV raised in pair of lateral bulges; posterior
component of median plate bearing pair of lateral
bosses cut by transverse suture. Branchiostegite
lacking large mark.
Description. — Body slender (Fig. 57) and lacking
Figure 57.— Sicyonia ingentis (Burkenroad 1938),?
36 mm cl, southeast of Punta Abreojos, Baja Califor-
nia Sur, Mexico. Lateral view. Scale = 10 mm.
[
FISHERY BULLETIN: VOL. 83, NO. 1
tubercles or occasionally with few on first abdomi-
nal somite. Carapace bearing patches of short
setae on dorsum, on pterygostomian and anterior
part of branchial regions, bordering branchiocar-
diac carina, and cluster immediately anteroven-
tral to hepatic spine; patches also present on
abdomen flanking dorsomedian carina and on
anteroventral part of pleuron of first three and
sixth somites. Abdomen lacking tubercles or with
few on first somite.
Rostrum slender, usually somewhat decurved
but sometimes subhorizontal, occasionally with
anterior extremity upturned; moderately long,
overreaching distal margin of eye (extending as
far as basal 0.2 of second antennular article), its
length 0.30-0.43 cl, increasing linearly with
carapace length (Fig. 58); armed with three dorsal
teeth and two (rarely three) apical teeth, ventral
one considerably smaller than dorsal and usually
placed posterior to it but occasionally at same level
or even more anteriorly; first rostral tooth sub-
equal to, or slightly smaller than epigastric and
located opposite and anterior to level of orbital
margin, second tooth situated between 0.32 and
0.44 (mean 0.37) rl from orbital margin; and third
tooth betwen 0.58 and 0.80 (mean 0.66) rl. Strong
adrostral carina, parallel to and rather near ven-
tral margin, extending along entire length of ros-
trum.
Carapace with postrostral carina low but robust
throughout its entire length in adults, weak in
juveniles, and bearing two teeth: 1) epigastric
tooth small, subequal to or barely larger than first
rostral tooth, situated anterior to but relatively
near level of hepatic spine, between 0.11 and 0.17
(mean 0.16) cl from orbital margin; and 2) pos-
terior tooth usually slightly, sometimes conspicu-
ously, larger than epigastric and placed well in
advance of posterior margin of carapace, between
0.57 and 0.65 (mean 0.63) cl from orbital margin.
Tuft of setae present immediately anterior to base
of each tooth. Antennal spine moderately long,
projecting from sharp, elongate buttress; hepatic
spine long, acutely pointed, arising from raised
area, and placed between 0.20 and 0.25 (mean
0.22) cl from orbital margin. Postocular sulcus
deep anteriorly, continuing posteriorly as long,
well-marked arched groove; hepatic sulcus sub-
horizontal; hepatic carina indistinct; branchio-
cardiac carina strong, longitudinally disposed
but curving dorsally near posterior margin of
carapace where also often sending short branch
ventrally.
First article of antennular peduncle and gna-
10
20 30 40
carapace length (mm)
50
Figure 58. — Sicyonia ingentis. Relationship between rostrum
length and carapace length (regression equation, >- = 0.75763 +
0.33933X).
thai appendages, except third maxilliped, illus-
trated in Figure 4.
Antennular peduncle with stylocerite produced
in long, sharp spine, its length 0.85-0.95 distance
between lateral base of first antennular article and
mesial base of distolateral spine; latter reaching
as far as midlength of second antennular article;
antennular flagella relatively long, mesial one,
about 0.4 as long as carapace, longer and more
slender than lateral; latter about 0.30 as long as
carapace.
Scaphocerite overreaching antennular peduncle
by as much as 0.2 of its own length; lateral rib
produced distally in long, acute spine considerably
surpassing margin of lamella. Antennal flagellum
about 2 times as long as carapace.
Third maxilliped about as slender as pereopods.
Basis and ischium of first pereopod unarmed.
Abdomen with dorsomedian carina extending
from first through sixth somites, carina on first
very low and produced in small, stubby, anterior
tooth, smaller or only slightly larger than pos-
terior tooth on carapace; carina on first five
somites sloping posteriorly, on sixth produced in
large acute posterior tooth.
Anteroventral margin of pleuron of first abdom-
inal somite slightly convex, sometimes straight in
juveniles; posteroventral margin, similar to that of
second and usually third somites, gently curved.
Anteroventral extremity of pleuron of first four
somites lacking spine, although that of second and
70
PfeREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
third occasionally projecting slightly or forming
small spine. Posteroventral extremity of pleuron
of first and second somites rounded, that of third
variably angular (sometimes bearing spine), and
that of fourth through sixth produced in caudally
directed spine.
First somite marked with short anteromedian
pleural sulcus continuing as shallow depression to
near ventral margin of pleuron, and long, united,
posterior tergal-posteromedian pleural sulci. Sec-
ond through fourth bearing anterior tergal sulcus
(that of fourth weak or sometimes lacking), and
united posterior tergat-posteromedian pleural
sulci; second and third also bearing shallow
depression representing anteromedian pleural
sulcus. Fifth somite with almost indistinct an-
terior tergal and strongly arched, united posterior
tergal-posteromedian pleural sulci. Sixth somite
with arched posteromedian pleural sulcus barely,
if at all, distinct, and bearing well-marked, long
cicatrix.
Telson with median sulcus deep basally, fading
posteriorly, and armed with small but well-
defined, fixed subterminal spines. Rami of uropod
subequal in length, exceeding apex of telson by as
much as 0.25 of their length.
Posterior spine on first abdominal sternite
broadly subtriangular with blunt apex and
straight or usually convex, instead of concave, lat-
eral margins.
Petasma (Fig. 59A,B) with cornified distal pro-
jection of dorsolateral lobule directed distolater-
ally, acutely pointed, ending in short filament, and
raised in proximodorsal, subhemispheric promi-
nence. Distal projection of ventrolateral lobule
reaching as far as projection of dorsolateral lobule,
mostly fieshy, blunt, and produced in small lateral
tooth just proximal to midlength.
Petasmal endopods joined in males 10.5 mm cl,
about 41 mm tl, but in individuals with carapace of
as much as 19 mm, about 70 mm tl, they may not be
joined.
Appendix masculina as illustrated in Figure
59C.
Thelycum (Fig. 60) with plate of sternite XIV
bearing paired strong protuberances bordered lat-
erally by narrow flanges and separated by deep
median depression sharply delimiting their pos-
teromesial margins. Median plate of sternite XIII
flask-shaped in outline, tapering gradually into
long, slender spine reaching between base and
midlength of basis of extended second pereopods;
plate set off from posterior component by deep
incisions and usually raised posterolaterally in
paired rounded prominences flanking narrow de-
pression (narrower than prominences); posterior
component of median plate bearing paired strong,
short bosses separated by deep median depression,
each boss cut by transverse suture. Paired short
spines projecting anteroventrally from posterior
Figure 59. — Sicyonia ingentis, i 16 mm cl, southeast of Punta Tasco, Isla Santa Margarita, Baja California Sur, Mexico. A,
Petasma, dorsal view; B, ventral view of same; C, right appendix masculina, dorsolateral view. Scale = 1 mm.
71
FISHERY BULLETIN: VOL. 83, NO. 1
Figure 60. — Sicyonia ingentis, -. 23 mm cl, southeast of Punta
Tasco, Isla Santa Margarita, Baja California Sur, Mexico.
Thelycum. Scale = 1 mm.
margin of sternite XI, spines broad basally and
sharp or sometimes needlelike apically.
The smallest impregnated females encountered
had a carapace of 14 mm, about 57 mm tl.
Maximum size. — Males 157 mm tl; females 180
mm tl, measured from "telson to base of antenna"
(Herkelrath 1977). In my sample: males 31 mm cl,
about 112 mm tl; females 40.2 mm cl, about 133
mm tl.
Geographic and bathymetric ranges. — Monterey
Bay, 36^50 'N, 121°50'W (Perez Farfante and
Boothe 1981), California, southward to Isla Maria
Madre, 22°00'N, 106°16'W, Nayarit, Mexico; in the
Gulf of California (Fig. 52) along the central part
of the eastern coast; and in the southern part along
both coasts. This species has been found between 5
and 293-307 m and is most abundant from 55 to 82
m, at which depth it is commercially fished off
Ventura, Calif. (Frey 1971); also most of the many
specimens examined by me were taken within this
range. According to Carlisle (1969) it is common at
depths between 61 and 183 m. Sicyonia ingentis
occurs on substrates of sand, shell, and green mud,
but seems to prefer sandy bottoms on which com-
mercial concentrations are located.
This species is the only member of Sicyonia that
has been recorded along the west coast of the
United States and north of Punta Canoas, Baja
California Sur — about 1,000 km south of Mon-
terey Bay, the northern limit of its range. The
record from Isla Maria Madre, Nayarit, is the first
from waters south of the Gulf of California.
Discussion. — Sicyonia ingentis, the largest east-
ern Pacific species in the genus, has its closest
affinities with the much smaller, sympatric S.
disdorsalis . It differs from the latter in possess-
ing 1) a carapace bearing, not lacking, patches of
long setae, 2) a robust postrostral carina rather
than a slender one, 3) a strong branchiocardiac
carina instead of an almost indistinct one, 4) a
carina on the fifth abdominal somite which slopes
gently to near the posterior cleft rather than being
truncate or produced in a spine, 5) an anterome-
dian pleural sulcus on the first abdominal somite
which continues as a shallow depression almost to
the ventral margin of the pleuron instead of end-
ing abruptly and well above it, 6) an unarmed
antero ventral extremity on the pleuron of the first
abdominal somite rather than one armed with a
strong spine, 7) curved, instead of angular, pos-
teroventral pleural margins on the first two ab-
dominal somites, 8) well-developed telsonic spines
instead of minute or indistinct ones, and 9) long
uropodal rami that considerably surpass the apex
of the telson instead of falling short of or barely
overreaching it.
Sicyonia ingentis also differs from S. disdorsalis
in characters of the genitalia. The distal projection
of the dorsolateral lobule of the petasma is di-
rected distolaterally instead of curving distome-
sially and is produced in a short apical filament
which is lacking in S. disdorsalis. The distal pro-
jection of the ventrolateral lobule reaches, instead
of falls short of, the terminal margin of the dor-
solateral lobule; furthermore, it is neither bifur-
cate laterally nor does it bear a transverse rib. In
the thelycum, the median depression on the pos-
terior part of the median plate of sternite XIII is
narrower than the usually rounded protuberances
flanking it, whereas in S. disdorsalis the depres-
sion is much broader than the flat or concave areas
which occupy the position of the two protuber-
72
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
I
ances. Finally, the paired lateral bosses, repre-
senting the posterior component of the median
plate and each cut by a transverse suture, are
found only in S. ingentis.
The "pencil of hairs" that Burkenroad (1938)
stated to be located on the dorsal surface of the
distal part of the ocular peduncle, near its disto-
lateral margin, actually is placed on the distome-
sial margin. He distinguished S. ingentis from S.
disdorsalis by, among other characters, the rela-
tive length of that tuft of setae, stating that in
large adults of the former species it overreaches
the eye whereas in S. disdorsalis it spans no more
than half the cornea. This character does not seem
to be a reliable one for, except in occasional speci-
mens of S. ingentis, in neither species does the tuft
surpass the eye. Burkenroad also considered the
disposition of the adrostral rib as a diagnostic fea-
ture that would serve to separate the two species.
Although in S. ingentis the rib lies parallel to the
ventral margin of the rostrum, in S. disdorsalis its
course varies: sometimes it is slightly arched near
the anterior end, as Burkenroad described it, but
often it is curved along the middle and occasion-
ally is slightly turned anterodorsally. The distance
of the rib from the ventral margin in the two
shrimps, however, exhibits a slight difference — in
S. ingentis it extends close to the margin whereas
in S. disdorsalis it lies more dorsally.
The characters exhibited by S. ingentis, S. dis-
dorsalis, and S. picta suggest that they must have
diverged quite early from a common ancestor in
the group of species that share two teeth on the
postrostral carina.
Notes on biology. — Herkelrath (1977) investigated
the temperature tolerance and age- growth and
length-weight relationships in this shrimp. He
found that within a salinity range of 33-35%o it
exhibits a wide range of tolerance to temperature
(4°-30°C). At a stressed salinity (261) this toler-
ance was considerably reduced (7°-25°), and mor-
tality increased proportionately with the duration
of exposure, regardless of temperature. His
studies indicated that shrimp with a total length
of 50-90 mm increased 10 mm per month and also
that there is no difference in length-weight ratio
between sexes. He also stated that among shrimp
"averaging 70 mm or greater in total length, the
average length of females was greater than that of
males."
Anderson (1983) studied growth rates, molting,
and certain aspects of reproduction in a population
of S. ingentis occurring off Santa Barbara, CA.
She found that spawning takes place far offshore
in deep water, about 145 m, and lasts from May
through October with the peak during the late
summer. She also observed that molt frequency is
highest in the winter and spring, that females do
not molt during the summer (the reproductive
period), and that males exhibit a similar pattern.
Size-frequency analyses based on monthly off-
shore and nearshore sampling indicated that ju-
veniles increased at a monthly rate of about 1-2
mo.
Commercial importance. — There is a fishery for
this shrimp between Santa Barbara and Ventura,
Calif According to the California Department of
Fish and Game, landings in 1982 amounted to
127,000,956 lb with a value of $156,000,385.
Mathews (1981) stated that "Sicyonia ringens" is
occasionally fished in Magdalena Bay, which is
located on the ocean side of Baja California Sur. I
have little doubt that his remark applies to S.
ingentis and that "ringens" is an erroneous spell-
ing. Moreover, it seems to me almost certain that
the study of "Sicyonia sp." (distribution, abun-
dance, rate of growth, ratio total weight/total
length) in Magdalena Bay by Mathew and Gon-
zalez (1975), was based on a population of this
species, apparently the only abundant rock
shrimp in the area. However, because Magdalena
Bay is within the range of S. penicillata , another
species reaching sizes reported by the authors, it is
not possible to be certain of the identity of the
shrimp studied by them. It is indeed unfortunate
that the valuable information presented cannot be
definitely associated with a specific shrimp, par-
ticularly in view of the fact that so little is known
of the biology of any of the eastern Pacific rock
shrimps. Although S. ingentis is present in the
Gulf of California, it is not commercially exploited
there.
Material. — 946 specimens from 52 lots.
United States— California: 1?, CAS, 2 km W
of Moss Landing, Monterey Bay, 50 m, 23 Sep-
tember 1978, D. D. Chivers. IS 3$ , AHF, 5 km off
Point Mugu, 40-59 m, 25 April 1976, Velero IV stn
24833. Id , AHF, 8.4 km W of Venice, 70-73 m, 22
July 1958, J. L. Baxter. 1$, SIO, SW of Santa
Monica Bay, 22 March 1962, F H. Berry and H. C.
Perkins. 39 , SIO, San Pedro Bay 27 m, 20 March
1964, U.S. Fish and Wildlife Service staff. 16 46 ,
SIO, N of Dana Point, 53-48 m, 29 March 1974,
Agassiz. 316 20V, JlO, off San Onofre, 54 m, 29
March 197 4, Agassiz. 26 29 , SIO, off San Onofre,
73
FISHERY BULLETIN: VOL. 83, NO. 1
91 m, 29 March 1974, Agassiz. 116 159, SIO, off
Encinitas, 51 m, 29 March 1974, Agassiz.
Mexico— Baja California Norte: 76 59, SIO,
off Bahia de San Quintin, 57 m, 1 April 1962, Fish
and Wildlife Service staff. 15c? 119, SIO, off
Bahia de San Quintin, 73 m, 4 December 1960, C.
Boyd and D. Dockins. 126 109 , SIO, off Bahia de
San Quintin, 74-77 m, H. C. Perkins. 66 69 , SIO,
off Bahia de San Quintin, 143-148 m, 1 April 1962,
H. C. Perkins. 26 59, SIO, SE of San Felipe, 120
m, 19 January 1968, Thomas Washington. 19,
SIO, W of Punta Prieta, 23 March 1960, H. C.
Perkins. 66 79, SIO, Bahia Sebastian Vizcaino,
88 m, 19 August 1960, W. D. Clarke. 19, YPM, E
of Isla Cedros, 110 m, 22 May 1936, Zaca stn
126D-10. 46 19, SIO, between San Benito and
Isla Cedros, 247-265 m, 27 May 1971, C. Hubbs and
S. Luke. 4(5, YPM, E of Isla Cedros, 80 m, 27
March 1936, Zaca stn 125D-1. 246 219 , USNM, E
of Isla Cedros, 80 m, 5 May 1888, Albatross stn
2838. 126 199, SIO, WSW of Red Rock, Bahia
Sebastian Vizcaino, 113-119 m, 25 November 1961,
E H. Berry Id , YPM, E of Isla Cedros, 73 m, 22
May 1936, Zaca stn 126D-4. 46 69, YPM, E of
Isla Cedros, 69 m, 27 March 1936, Zaca stn
126D-2. 6 holotype, AMNH, off east coast of
Isla Cedros, 69 m, 27 March 1936, Zaca stn
127D-1. 36 19 and 26 29 paratypes, AMNH and
YPM, respectively, collected with holotype. 36
li, YPM, E of Isla Cedros, 70-110 m, 27 March
1936, Zaca stn 125D-1. Baja California Sur:
36 19, SIO, Bahia Sebastian Vizcaino, 55 m, 11
August 1952, K. S. Norris. 26 29, SIO, Bahia
de San Cristobal, 83-87 m, 2 December 1961, F
H. Berry 196 179, SIO, Bahia Asuncion, 68-64
m, 17 November 1964, Black Douglas. 206 209,
SIO, SW of Punta San Hipolito, 6 March 1954,
"J.M. and W.H." 13d 209, SIO, SE of Punta Abre-
ojos, 55-59 m, 17 November 1964, Black Doug-
las. 46 179, SIO, SE of Punta Abreojos, 73-79
m, 17 November 1964, Black Douglas. 216 219,
SIO, SE of Punta Abreojos, 91 m, 2 December
1960, C. Boyd and D. Dockins. 20d 209, SIO,
WSW of Punta Pequeha, 68-73 m, 16 November
1964, Black Douglas. 26 39, SIO, 15 km WSW
of Boca de las Animas, 55-57 m, 16 November
1964, Black Douglas. 146 69, SIO, SW of Santo
Domingo del Pacifico, 100 m, 20 April 1969. 19d
lb , SIO, 16 km NW of Isla Magdalena, 99-102
m, 16 November 1964, Black Douglas. 236 229,
SIO, off Bahia Magdalena, 88 m, 3 February
1964, C. Hubbs. 30d 30.-, SIO, SW of Isla San-
ta Margarita, 75-81 m, 13 November 1964, Black
Douglas. 446 269, SIT, SE of Punta Tasco, Isla
74
Santa Margarita, 102-106 m, 27 June 1965, Hori-
zon. 256 259, SIO, W of Inocentes, 91-93 m, 10
November 1964, Black Douglas. 29, SIO, WNW
of Punta Lobos, 183-201 m, 9 November 1964,
Black Douglas. 16, SIO, Bahia de la Paz, 82-
119 m, 12 January 1968, Thomas Washington.
Sonora: Id 19, SIO, off Hermosillo coast, 289-
304 m, 25 March 1960, Curray and R. H. Parker.
19, AHF, S of Isla Tiburon, 4-29 m, 25 January
1940. 15d 119, SIO, off Santa Rosalia, 64-48 m,
25 March 1960, R. H. Parker. 25d 259, SIO, off
Isla San Pedro Martir, 293-307 m, 21 January
1968, Thomas Washington. 19, AHF, Bahia de
Guaymas, 5 m, 23 March 1949. Sinaloa: 2d 19,
USNM, Puerto de la Punta Altata, 9 May 1962,
R. E. Bush. 19, USNM, Los Cocos, 42 m, 18
May 1962, R. E. Bush. Nayarit: 24d 219, SIO,
NE of Isla Maria Madre, Islas Tres Marias, 82-88
m, 30 March 1973, Agassiz.
ACKNOWLEDGMENTS
Many persons have assisted me throughout the
course of this study. Because of the large area
covered I was dependent upon many sources for
specimens. I am deeply indebted to the following
who have lent collections to me, many of which
included materials representing new locality
records and range extensions: Dustin D. Chivers,
California Academy of Sciences; Enrique M.
Del Solar, Instituto del Mar del Peru; Harold S.
Feinberg, American Museum of Natural History;
Jacques Forest, Museum National d'Histoire
Naturelle, Paris; H. E. Gruner, Zoologisches
Museum, Humboldt- Universitat, Berlin; Janet
Haig, Allan Hancock Foundation, University of
Southern California; Willard D. Hartman, Pea-
body Museum of Natural History, Yale University;
Leslie W. Knapp, Smithsonian Oceanographic
Sorting Center, Smithsonian Institution; Herbert
V. Levi and Catharine G. Sibble, Museum of Com-
parative Zoology, Harvard University; Spencer R.
Luke, Scripps Institution of Oceanography; Juan
B. del Rosario, Universidad de Panama; and Mary
K. Wicksten, Texas A & M University, formerly of
Allan Hancock Foundation.
I have the privilege of drawing on the consider-
able knowledge of decapod crustaceans system-
atics of Horton H. Hobbs, Jr., of the Smithsonian
Institution, who has given me numerous sugges-
tions during the investigation and has criticized
the manuscript. Fenner A. Chace, Jr., of the
Smithsonian Institution, and Bruce B. Collette
and Austin B. Williams, both of the Systematics
P6REZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
Laboratory, National Marine Fisheries Service,
also have read the manuscript and made helpful
comments. I acknowledge their assistance with
deep appreciation. I am deeply grateful to Matilde
Mendez G., Instituto del Mar del Peru, and to Con-
cepcion Rodriguez de la Cruz, Instituto de Pesca,
Mexico, for the loan of specimens and for invalu-
able information concerning materials deposited
in their respective institutions. Thanks are also
extended to Meredith L. Jones, Smithsonian In-
stitution, whose interest and efforts facilitated my
field work in Panama; and for making available
critical bibliographic references to Lipke B.
Holthuis, Rijksmuseum van Natuurlijke Historie,
Leiden; Alexander Dragovich, Southeast
Fisheries Center, National Marine Fisheries Ser-
vice; and to Michel E. Hendrickx, Instituto de
Ciencias del Mar y Limnologia, Estacion Maza-
tlan, Mexico.
I wish to thank Billy B. Boothe, Jr., who sorted
and identified the Sicynnia that had been collected
among large quantities of penaeoids from the re-
gion under investigation and assisted me with the
morphometric work. Joseph L. Russo, formerly of
the NMFS Systematics Laboratory, helped with
statistical analyses and computer work, and Ruth
Gibbons also assisted in the analyses and prepared
the graphs and distribution maps. Maria M.
Dieguez applied her artistic talent to the prepara-
tion of all of the illustrations except Figures 3, 4,
and 7 which were ably rendered by Keiko H.
Moore. Finally, I also acknowledge with gratitude
the assistance of Arleen S. McClain and Virginia
R. Thomas, who patiently typed several drafts of
the manuscript.
LITERATURE CITED
ALLEN, D. M.
1973. Rock shrimp (Sicyonia brevirostris) production -
South Atlantic coast of the United States and Gulf of
Mexico. Summary Report. Natl. Mar Fish. Serv,
NOAA, Southeast Fish. Cent., Miami Lab., 15 p.
ANDERSON, S. L.
1983. Molt and reproduction of the ridgeback prawn,
Sicyonia ingentis (Penaeidae). Ph.D. Thesis, Univ.
California, Davis, 115 p.
ANDERSON, W. W.
1956. January to April distribution of the common shrimp
on the South Atlantic Continental Shelf. U.S. Fish
Wildl. Serv, Spec. Sci. Rep. Fish. 171, 14 p.
1962. Recognizing important shrimps of the South. U.S.
Fish Wildl. Serv, Fish. Leafl. 536, 5 p. (Supersedes Fish.
Leaf!. 366.)
ANDERSON, W. W., AND M. J. LINDNER.
1945. A provisional key to the shrimps of the family
Penaeidae with especial reference to American forms.
Trans. Am. Fish. Soc. 73:284-319.
ANDERSON, W. W., M. J. LINDNER, AND J. E. KING.
1949. The shrimp fishery of the southern United States.
Commer. Fish. Rev 11(2):1-17.
ANONYMOUS.
1980. Crustaceos colectados con red de arrastre en el Golfo
de California. Invest. Oceanogr. B-80-04, Seer. Mar.,
Mex., 25 p.
ARANA ESPINA, R, AND M. MENDEZ G.
1978. El genero Sicyonia H. Milne Edwards, 1830 en el
Pacifico Sur Oriental, con observaciones biologicas sobre
Sicyonia alliaffinis Burkenroad 1934 (Crustacea: De-
capoda: Penaeidae). Rev Com. Perm. Pac. Sur. 9:19-40.
ARREGLfiN SANCHEZ, F
1981. Diagnosis de la pesqueria de camaron de roca
{Sicyonia brevirostris Stimpson, 1871) de Contoy, Q. Roo,
Mexico. Cienc. Pesq., Inst. Nac. Pesca, Dep. Pesca, Mex.
1(2):21-4L
BALSS, H.
1914. Ostasiatische Decapoden II. Die Natantia und Rep-
tantia. Beitrage zur Naturgeschichte Ostasiens.
Herausgegeben von Dr. F. Doflein. Abh. Bayer Akad.
Wiss. Math-Phys. Kl., Suppl. 2, Pt. 10, p. 1-101.
1925. Macrura der Deutschen Tiefsee-Expedition. 2.
Natantia, Teil A. Wiss. Ergeb. "Valdivia" Exped. 20, p.
217-315.
BARNARD, K. H.
1950. Descriptive catalogue of South African decapod
Crustacea. Ann. S. Afr Mus. 38:1-837.
BATE, C. S.
1888. Report on the Crustacea Macrura collected by
H.M.S. Challenger during the years 1873-76. Rep. Sci.
Results Voyage H.M.S. Challenger. Zool. 24, 942 p.
BAYER, F M., G. L. VOSS, AND C. R. ROBINS.
1970. Bioenvironmental and radiological safety feasibility
studies Atlantic-Pacific interoceanic canal. Report on the
marine fauna and benthic shelf-slope communities of the
Isthmian region. Rosenstiel School Mar. Atmos. Sci., Univ
Miami, 311 p.
BOECK, A.
1864. Beskrivelse og fremlagde Tegninger af 4 norske De-
capoder, underaOgte af Overlaege Danielssen og
ham. Forh. Vidensk. Selsk., Christ. (1863):189-190.
BOONE, L.
1930. Crustacea: Anomura, Macrura, Schizopoda, Isopoda,
Amphipoda, Mysidacea, Cirripedia, and Copepoda. Scien-
tific results of the cruises of the yachts "Eagle" and "Ara",
1921-1928, William K. Vanderbilt, commanding. Bull.
Vanderbilt Mar. Mus. Vol. 3, 221 p.
BOUVIER, E. L.
1905. Sur les macroures nageurs (abstraction faite des
carides), recueillis par les expeditions americaines du
Hassler et du Blake. C. R. Acad. Sci., Paris 140:746-749.
1918. Sur une petite collection de crustaces de Cuba offerte
au Museum par M. de Boury Bull. Mus. Hist. Nat. Paris
24:6-15.
BRUNNICH, M. T
1768. Ichthyologia Massiliensis, sistens piscium descrip-
tiones eorumque apud incolas nomina. Accedunt spolia
maris Adriatici, Hafniae at Lipsiae, apud Rothii viduam
et Proft, 110 p.
BRUSCA, R. C.
1973. A handbook to the common intertidal invertebrates
of the Gulf of California. 1st ed. Univ Ariz. Press, Tuc-
son, 427 p.
75
FISHERY BULLETIN: VOL. 83, NO. 1
1980. Common intertidal invertebrates of the Gulf of
California. Univ. Ariz. Press, Tucson, 513 p.
BRUSHER, H. A., AND L. H. OGREN.
1976. Distribution, abundance, and size of penaeid shrimps
in the St. Andrew Bay system, Florida. Fish. Bull., U.S.
74:158-166.
BRUSHER, H. A., W. C. RENFRO, AND R. A. NEAL.
1972. Notes on distribution, size, and ovarian development
of some penaeid shrimps in the northwestern Gulf of
Mexico, 1961-1962. Contrib. Mar Sci. 16:75-87.
BRYAN, C. E., AND T. J. CODY.
1975. Abundance of rock shrimp, Sicyonia brevirostris
(Stimpson), in Texas. In A study of commercial shrimp,
rock shrimp, and potentially commercial finfish 1973-
1975, Part II, p. 1-11. Texas Parks Wildl. Dep., Austin,
Texas.
BURKENROAD, M. D.
1934a. Littoral Penaeidea chiefly from the Bingham
Oceanographic Collection with a revision of Penaeopsis
and descriptions of two new genera and eleven new Ameri-
can species. Bull. Bingham Oceanogr. Collect., Yale
Univ 4(7):1-109.
1934b. The Penaeidea of Louisiana with a discussion of
their world relationships. Bull. Am. Mus. Nat. Hist.
68:61-143.
1938. The Templeton Crocker Expedition. XIII. Penaeidae
from the region of Lower California and Clarion Island,
with descriptions of four new species. Zoologica (N.Y.)
23:55-91.
1939. Further observations on Penaeidae of the northern
Gulf of Mexico. Bull. Bingham Oceanogr. Collect., Yale
Univ 6(6):l-62.
1946. Status of the name Sicyonia H.M.E., with a note on
S. typica (Boeck) and descriptions of two new species.
Ark. Zool. 37A(9):1-10.
Cain, T. D.
1972. Additional epifauna of a reef off North Carolina. J.
Elisha Mitchell Sci. Soc. 88:79-82.
Camp, d. K., n. h. whiting, and r. E. Martin.
1977. Nearshore marine ecology at Hutchinson Island,
Florida: 1971-1974. V. Arthropods. Fla. Mar. Res. Publ.
25, 63 p.
Carlisle, J. G., Jr.
1969. Invertebrates taken in six year trawl study in Santa
Monica Bay Veliger 11:237-242.
Castille, F L., Jr., and A. L. Lawrence.
1981. The effect of salinity on the osmotic, sodium and
chloride concentrations in the hemolymph of the rock
shrimps, Sicyonia brevirostris and Sicyonia dor-
salis. Comp. Biochem. Physiol. 70A:519-523.
Castro, p
1966 The shrimps (Crustacea Decapoda Natantia) of the
Sonoran coast of the Gulf of California. Univ Ariz. Biol.
Stud. Gulf Calif 4(2):l-33.
CERAME-VIVAS, M. J., AND I. E. GRAY.
1966. The distributional pattern of benthic invertebrates
of the continental shelf off North Carolina. Ecology
47:260-270.
CHACE. f a., Jr.
1972. The shrimps of the Smithsonian-Bredin Caribbean
expeditions with a summeu-y of the West Indian shallow-
water species (Crustacea: Decapoda: Natantia). Smith-
son, Contrib. Zool. 98. 179 p.
CHAPA SALDANA, H.
1%4. Lista preliminar de los crustaceos existentes en el
Laboratorio Central del I.N.I. B. P. Inst. Nac. Invest.
76
Biol.-Pesq. Ser. Trab. Divulg. 9(87), 40 p.
CHIRICHIGNO FONSECA, N.
1970. Lista de crustaceos del Peru (Decapoda y
Stomatopoda) con dates de su distribucion geografi-
ca. Inst. Mar. Peru (Callao), Inf. 35, 95 p.
COBB, S. P
1971. A new species of Sicyonia (Decapoda, Penaeidae)
from the western Atlantic with notes on S. stimpsoni
Bouvier Crustaceana 20:104-112.
COBB, s. P, c. R. futch, and d. k. Camp.
1973. Memoirs of the Hourglass Cruises: the rock shrimp,
Sicyonia brevirostris Stimpson, 1871 (Decapoda,
Penaeidae). Fla. Dep. Nat. Res. Mar. Res. Lab. 3 (Part 1),
38 p.
coen, l. d., and k. l. heck, Jr.
1983. Notes on the biology of some seagrass-dwelling crus-
taceans (Stomatopoda and Decapoda) from Caribbean
Panama. Proc. Biol. Soc. Wash. 96:202-224.
DAY, J. W, JR., W. G. SMITH, P R. WAGNER, AND W. C. STOWE.
1973. Community structure and carbon budget of a salt
marsh and shallow bay estuarine system in Louisi-
ana. Cent. Wetland Resour, La. State Univ. Publ. LSU-
SG-72-04, 79 p.
DE HAAN, W.
1833-1850. Crustacea. In P. F. von Siebold, Fauna
Japonica sive descriptio animalium, quae in itinere per
Japoniam, jussu et auspiciis superiorum, qui summum in
India Batava Imperium tenent, suscepto, annis 1823-1830
collegit, notis, observationibus et adumbrationibus
illustravit. Lugduni-Batavorum [Leiden], 243 p.
DE MAN, J. G.
1907. On a collection of Crustacea, Decapoda and
Stomatopoda, chiefly from the Island Sea of Japan; with
descriptions of new species. Trans. Linn. Soc. Lond.
Zool., Ser. 2, 9:387-454.
1911. The Decapoda of the Siboga Expedition. Part I, Fam-
ily Penaeidae. Siboga-Exped. Monogr. 39a, 131
p. (Suppl. to Part 1, 1913.)
DE Natale, G.
1850. Descrizione zoologica d' una nuova specie di Plojaria
e di alcuni crostacei del porto di Messina con poche con-
siderazioni generali sulla natura delle appendici
aculeiformi delle pinati e degli animali. Giuseppe
Fiumara, Messina, 31 p. app.
DE SAUSSURE, H.
1857. Diagnoses de quelques crustaces nouveaux des An-
tilles et du Mexique. Rev Mag. Zool., Ser. 2, 9:304-308.
DEL SOLAR C.,E. M.
1972. Addenda al Catalogo de crustaceos del Peru. Inst.
Mar. Peru (Callao), Inf 38, 21 p.
DEL SOLAR C, E. M., F BLANCAS S., AND R. MAYTA L.
1970. Catalogo de crustaceos del Peru. D. Miranda, Lima,
Peru, 53 p.
Dunn, D. f
1982. Announcement. J. Crustacean Biol. 2:153.
ELDRED, B.
1959. A ref)ort on the shrimps (Penaeidae) collected from
the Tbrtugas controlled area. Fla. Board Conserv., Mar
Lab., Spec. Sci. Rep. 2, 6 p.
ELDRED, B., J. WILLIAMS, G, T MARTIN, AND E. A. JOYCE, JR.
1965. Seasonal distribution of penaeid larvae and postlar-
vae of the Tampa Bay area, Florida. Fla. Board Conserv.
Mar. Lab., Tech. Ser. 44, 47 p.
FAUSTO FILHO, J.
1966a. Primeira contribuicao ao inventario dos crustaceos
decapodos marinhos do nordeste brasileiro. Arq. Estac.
PfeREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
Biol. Mar. Univ. Fed. Ceara 6:31-37.
1966b. Sbbre os peneideos do nordeste brasileiro. Arq.
Estac. Biol. Mar. Univ. Fed. Ceara 6:47-50.
1968. General considerations on the peneids of north and
northeast of Brazil. Arq. Estac. Biol. Mar. Univ. Fed.
Ceara 8:69-73.
Faxon, W.
1893. VI. Preliminary descriptions of new species of Crus-
tacea. Reports on the dredging operations off the west
coast of Central America to the Galapagos, to the west
coast of Mexico, and in the Gulf of California, in charge of
Alexander Agassiz, carried on by the U.S. Fish Commis-
sion steamer "Albatross," during 1891, Lieut. Commander
Z. L. Tanner, U.S.N., commanding. Bull. Mus. Comp.
Zool, Harv Coll. 24:149-220.
1895. XV. The stalk-eyed Crustacea. Reports on an ex-
ploration off the west coast of Mexico, Central and South
America, and off the Galapagos Islands, in charge of
Alexander Agassiz, by the U.S. Fish Commission steamer
"Albatross," during 1891, Lieut. Commander Z. L. Tanner,
U.S.N. , commanding. Mem. Mus. Comp. Zool., Harv.
Coll. 18:1-292.
1896. XXXVII. Supplementary notes on the Crustacea.
Reports on the results of dredging, under the supervision
of Alexander Agassiz, in the Gulf of Mexico and the Carib-
bean Sea, and on the east coast of the United States, 1877
to 1880, by the U.S. Coast Survey steamer "Blake,"
Lieut. -Commander C. D. Sigsbee, U.S.N., and Com-
mander J. R. Bartlett, U.S.N. , commanding. Bull. Mus.
Comp. Zool., Harv Coll. 30:153-166.
FEINBERG, H. S.
1971. A catalogue of type specimens in the Department of
Living Invertebrates. The American Museum of Natural
History. New York, New York, U.S.A. Phylum Arthropoda;
Class Crustacea. Part one: Order Decapoda. Am. Mus.
Nat. Hist., N.Y, 75 p.
FRANKS, J. S., J. Y. CHRISTMAS, W. L. SILER, R. COMBS, R.
WALLER, AND C. BURNS.
1972. A study of nektonic and benthic faunas of the shal-
low Gulf of Mexico off the state of Mississippi as related to
some physical, chemical and geological factors. Gulf
Res. Rep. 4:1-148.
FREY, H. W.
1971. California's living marine resources and their utili-
zation. Calif. Dep. Fish Game, Resour Agency, 148 p.
Garcia Pinto, l.
1971. Identificacion de las postlarvas del camaron (genero
Penaeus) en el occidente de Venezuela y observaciones
sobre su crecimiento en el laboratorio. Proyecto Invest.
DesarroUo Pesq. MAC-PNUD-FAO Inf. Tec. 39, 23 p.
Greening, H. S., and r. j. Livingston.
1982. Diel variation in the structure of seagrass-associated
epibenthic macroinvertebrate communities. Mar. Ecol.
Prog. Ser. 7:147-156.
GUNTER, G. and D. MCCAUGHAN.
1959. Catalepsy in two common marine animals. Science
130:1194-1195.
HAAN, W. de. See De Haan, W.
HALL, D. N. F
1956. The Malayan Penaeidae (Crustacea, Decapoda).
Part I. Introductory notes on the species of the general
Solenocera, Penaeus, and Metapenaeus. Bull. Raffles
Mus. 27:68-90.
HAY, W P, AND C. A. SHORE.
1918. The decapod crustaceans of Beaufort, N.C., and the
surrounding region. Bull. U.S. Bur. Fish. 35:369-475.
HEDGPETH, J. W
1953. An introduction to the zoogeography of the north-
western Gulf of Mexico with reference to the inver-
tebrate fauna. Publ. Inst. Mar. Sci., Univ. Tex. 3:111-
224.
HELLER, C.
1863. Die Crustaceen des siidlichen Europa. Crustacea
Podophthalmia. Mit einer iibersicht iiber die horizontale
Verbreitung sammtlicher europaischer Arten, Vien-
na. Wien, W. Brawmiiller, 336 p.
HEMMING, F. (editor).
1958. Official list of generic names in zoology. First in-
stallment: Names 1-1274. Int. Trust. Zool. Nomencl.,
Lend., 200 p.
HERKELRATH, J. M.
1977. Some aspects of the growth and temperature toler-
ance of the ridgeback prawn, Sicyonia ingentis Burken-
road in southern California waters. M.S. Thesis, Whit-
tier College, Whittier, CA, 67 p.
HILDEBRAND, H. H.
1954. A study of the fauna of the brown shrimp {Pe-
naeus aztecus Ives) grounds in the western Gulf
of Mexico. Publ. Inst. Mar. Sci., Univ. Tex. 3:233-
366.
1955. A study of the fauna of the pink shrimp (Penaeus
duorarum Burkenroad) grounds in the Gulf of Caim-
peche. Publ. Inst. Mar. Sci., Univ Tex. 4:169-232.
HOLTHUIS, L. B.
1952. Proposed use of the Plenary Powers to validate the
generic name "Sicyonia" H. Milne Edwards, 1830 (Class
Crustacea, Order Decapoda). Bull. Zool. Nomencl.
6:339-342.
1980. FAO species catalogue. Vol. 1. Shrimps and prawns
of the world. An annotated catalogue of species of interest
to fisheries. FAO Fish. Synop. 125, 261 p.
HOOKS, T A., K. L. HECK, JR., AND R. J. LIVINGSTON.
1976. An inshore marine invertebrate community: struc-
ture and habitat associations in the northeastern Gulf of
Mexico. Bull. Mar. Sci. 26:99-109.
HUFF, J. A., AND S. P COBB.
1979. Memoirs of the Hourglass Cruises: penaeoid and
sergestoid shrimps (Crustacea: Decapoda). Fla. Dep.
Nat. Resour. Mar. Res. Lab. 5(part 4), 102 p.
HUTTON, R. E, F. SOGANDARES-BERNAL, B. ELDRED, R. M.
INGLE, AND K. D. WOODBURN.
1959. Investigations on the parasites and diseases of salt-
water shrimps (Penaeidae) of sports and conamercial im-
portance to Florida. Fla. Board Conserv. Tech. Sen 26,
36 p.
INTERNATIONAL COMMISSION ON ZOOLOGICAL NOMENCLA-
TURE.
1956. Opinion 382. Validation under the Plenary Powers of
the generic name Sicyonia Milne Edwards (H.), 1830
(Class Crustacea, Order Decapoda) and action consequen-
tial thereon. In Opinions and declarations rendered by
the International Commission on Zoological Nomencla-
ture, Vol. 12, p. 43-58.
JOYCE, E. A., JR.
1965. The commercial shrimps of the northeast coast of
Florida. Fla. Board Conserv. Mar. Res. Lab. Prof Pap.
Ser. 6, 224 p.
1968. Project Hourglass explores the continental
shelf. Sea Front. 14:352-359.
JOYCE, E. A., Jr., AND B. ELDRED.
1966. The Florida shrimping industry Fla. Board Con-
serv. Mar Res. Lab. Educ. Ser. 15, 47 p.
77
FISHERY BULLETIN; VOL. 83, NO. 1
KENNEDY, F. S., J. J. CRANE, R. A. SCHLIEDER, AND D. G.
BARBER.
1977. Studies of the rock shrimp, Sicyonia brevirostris , a
new fishery resource on Florida's Atlantic shelf. Fla.
Mar Res. Publ. 27, 69 p.
KINGSLEY, J. S.
1878. List of the North American Crustacea belonging to
the Suborder Caridea. Bull. Essex Inst. 10:53-71.
1880. On a collection of Crustacea from Virginia, North
Carolina, and Florida, with a revision of the genera of
Crangonidae and Palaemonidae. Proc. Acad. Nat. Sci.,
Phila. 31:383-427.
KUBO, I.
1949. Studies on penaeids of Japanese and its adjacent
waters. J. Tokyo Coll. Fish. 36(l):l-467.
KUTKUHN, J. H.
1962. Conversion of "whole" and "headless" weights in
commercial Gulf of Mexico shrimps. U.S. Fish Wildl.
Serv, Spec. Sci. Rep. Fish. 409, 7 p.
LOCKINGTON, W. N.
1879. Notes on Pacific coast Crustacea. Bull. Essex Inst.
10:159-165.
LONGHURST, A. R.
1970. Crustacean resources. In J. A. Gulland (editor),
The fish resources of the ocean, p. 252-305. FAO Fish.
Biol. Tech. Pap. 97.
LUNZ, G. R.
1945. Carolina shrimps of the genus £i/sJC3'o«ia. Char-
leston Mus. Leafl. 20, 12 p.
1957. Notes on rock shrimp Sicyonia brevirostris
(Stimpson) from exploratory trawling off the South
Carolina coast. Contrib. Bears Bluff Lab. 25, 10 p.
Lyons, w. G., S. P Cobb, d. k. Camp, J. A. Mountain, T
Savage, L. Lyons, and E. a. Joyce, jr.
1971. Preliminary inventory of marine invertebrates col-
lected near the electrical generating plant, Crystal River,
Florida, in 1969. Fla. Dep. Nat. Resour Mar Res. Lab.
Prof Pap. Sen 14, 45 p.
MaN,J. G., DE. See De Man, J. G.
Mathews, C. R
1981. A review of the North American penaeid fisheries
with particular reference to Mexico. Kuwait Bull. Mar.
Sci. 2:325-409.
Mathews, C. P, and J. A. Gonzalez.
1975. Potencial pesquero y estudios ecologicos de Bahia
Magdalena I. Las existencias de camaron con referenda
especial al camaron de roca o camaron japones. Cienc.
Pesq., Inst. Nac. Pesca, Mex. 2(l):51-57.
MCCONNELL, R. H.
1960. Part II. The interpretation ofthe catch records. The
trawl survey carried out by the RA^ "Cape St. Mary" off
British Guiana 1957-59. Br Guiana Fish. Bull. 2:25-53.
MENDEZ G., M.
1981. Claves de identificacion y distribucion de los langos-
tinosycamarones (Crustacea: Decapoda)del mary riosde
la costa del Peru. Bol. Inst. Mar Peru 5:1-170.
MENZEL, R. W.
1956. Annotated check-list ofthe marine fauna and flora of
the St. George's Sound -Apalachee Bay region, Florida
Gulf coast. Oceanogr. Inst., Fla. State Univ., Contrib. 61,
78 p.
MIERS, E. J.
1881. On a collection of Crustacea made by Baron
Hermann-Maltzam at Goree Island, Senegambia. Ann.
Mag. Nat. Hist., Ser 5, 8:204-220, 259-281, 364-377.
MILNE Edwards, a., and E. L. bouvier.
1909. XLIV. Les Peneides et Stenopides. Reports on the
results of dredging, under the supervision of Alexander
Agassiz, in the Gulf of Mexico (1877-78), in the Caribbean
Sea (1878-79), and along the Atlantic coast ofthe United
States (1880), by the U.S. Coast Survey steamer "Blake,"
Lieut. -Com. C. D. Sigsbee, U.S.N., and Commander J. R.
Bartlett, U.S.N., commanding. Mem. Mus. Comp. Zool.,
Harv. Coll. 27:177-274.
MILNE Edwards, H.
1830. Description des genres Glaucothoe, Sicyonie,
Sergeste et Acete, de I'ordre des Crustaces Decapodes.
Ann. Sci. Nat., Sen 1, 19:333-352.
1837. Histoire naturelle des crustaces, comprenant
I'anatomie, la physiologie et la classification de ces
animaux. [Atlas] Roret, Paris, 2, 532 p.
MONOD, T, AND P CALS.
1970. Sur une espece nouvelle de crevette cavernicole:
Typhlatya galapagensis (Decapoda Natantia: Aty-
idae). Mission zool. belg iles Galapagos Ecuador 2:57-
103.
NatALE, G. De. See De Natale, G.
Office of Geography, department of the Interior.
1956. NIS Gazetteer Mexico. U.S. Printing Office, Wash-
ington, D.C., 750 p.
PARKER, R. H.
1964. Zoogeography and ecology of some macro-
invertebrates, particularly mollusks, in the Gulf of
California and the continental slope off Mexico. Vid-
ensk. Med. Dan. Naturh. Foren. 126:1-178.
PAUL, R. K. G., AND M. E. HENDRICKX.
1980. Crustaceans in the shrimp by-catch from off the
coasts of Sinaloa and Nayarit, Mexico. Bull. South. Calif
Acad. Sci. 79:109-111.
PEARSE, A. S., AND L. G. WlLLL^MS.
1951. The biota of the reefs off the Carolinas. J. Elisha
Mitchell Sci. Soc. 67:133-161.
PEREZ FARFANTE, I.
1978. Families Hippolytidae, Palaemonidae (Caridea), and
Penaeidae, Sicyoniidae and Solenoceridae (Penaeoidea).
In Fischer, W. (editor), FAO species identification sheets for
fishery purposes, western central Atlantic (fishing area
31), Vol. VI (unpaginated). FAO, Rome.
1980. A new species of rock shrimp of the genus Sicyonia
(Penaeoidea), with a key to the western Atlantic spe-
cies. Proc. Biol. Soc. Wash. 93:771-780.
1982. Camarones. In N. Chirichigno, W. Fischer, and C.
E. Nauen (compositors), INFOPESCA. Catalogo de es-
pecies marinas de interes economico actual o potencial
para America Latina. Parte 2. - Pacifico centro y sur-
oriental, p. 363-381. Roma, FAO/PNUD, SIC/82/2.
P6REZ FARFANTE, I., AND B. B. BOOTHE, JR.
1981. Sicyonia martini, a new rock shrimp (Decapoda:
Penaeoidea) from the American Pacific. J. Crustacean
Biol. 1:424-432.
PESTA, O.
1915. Die Penaeidea des Wiener naturhistorischen Hof-
museums. Arch. Naturgesch. 81, Abt. A, Hft. 1:99-122.
RATHBUN.M. J.
1901. The Brachyura and Macrura of Porto Rico. [Pre-
print from U.S. Fish Comm. Bull, for 1900 [1902] 20(2):
1-127, 129-137 (preprint index)].
1920. Stalk-eyed crustaceans ofthe Dutch West Indies. In
J. Boeke, Rapport betreffende een voorloopig onderzoek
naar den toestand van de Visscherij en de Industrie van
78
PEREZ FARFANTE: ROCK SHRIMP GENUS SICYONIA
Zeeproducten in de Kolonie Curapao, ingevolge het Minis-
terieel Besluit van 22 November 1904, Vol. 2, p. 317-
348. F. J. Belinfante, 'S-Gravenhage.
RODRIGUEZ, G.
1980. Los crustaceos decapodos de Venezuela. Inst. Venez.
Invest. Cient., Caracas, 494 p.
RODRIGUEZ DE LA CRUZ, M. C.
1977. Decapodos marines del Golfo de California. Tesis
Maestro en Ciencias Marinas, Escuela de Ciencias
MaritimasyAlimentariasdell.T.Y.E.S.M. Inst. Tec. Es-
tud. Super. Monterrey, Guaymas, Mex., 243 p.
1981. Aspectos pesqueros del camaron de alta mar en el
Pacifico mexicano. Cienc. Pesq., Inst. Nac. Pesca, Mex.
1(2):1-19.
ROSALES JUAREZ, E J.
1976. Contribucion al concimiento de la fauna de acom-
panamiento del camaron de alta mar, frente a la costa de
Sinaloa, Mexico. Mem. Reun. Recursos Pesca Costera
Mex., Veracruz, Ver, 23-25 Nov. 1976, p. 25-88.
ROUSE, W. L.
1969. Littoral Crustacea from southwest Florida. Q. J.
Fla. Acad. Sci. 32:127-152.
SAUSSURE, H., De. See De Saussure, H.
SCHMITT, W. L.
1924. Crustacea (Macrura and Anomura). Expedition of
the California Academy of Sciences to the Gulf of Califor-
nia in 1921. XXIV Proc. Calif. Acad. Sci., Ser. 4, 13:381-
388.
1935. Crustacea Macrura and Anomura of Porto Rico and
the Virgin Islands. In Scientific Survey of Porto Rico and
the Virgin Islands, p. 125-227, 255-262. N.Y. Acad. Sci. 15,
Part 2.
SOTO, L. A.
1980a. Decapod crustacean shelf-fauna of the Campeche
Bank: fishery aspects and ecology. Proc. Gulf Caribb.
Fish. Inst. 32d Annu. Sess., p. 66-81.
1980b. Decapod Crustacea shelf-fauna of the northeastern
Gulf of Mexico. Ann. Cent. Cienc. Mar Limnol., Univ.
Nac. Auton. Mex. 7(2):79-110.
SOSA HERNANDEZ, R, J. L. HERNANDEZ AGUILERA, AND J.L.
VILLALOBOS HIRIART.
1980. Estudio prospective de los crustaceos (Decapoda y
Stomatopoda) del Golfo de Tehuantepec, Mexico. Invest.
Oceanogr. B-80-10, Seer Mar, Mex., 50 p.
STEBBING, T. R. R.
1914. South African Crustacea (Part VII. of S. A. Crus-
tacea, for the marine investigations in South Afri-
ca). Ann. S. Afr Mus. 15:1-55.
STEINBECK, J., AND E. RICKETTS.
1941. Sea of Cortez. The Viking Press, N.Y, 598 p.
STIMPSON, W.
1871. Notes on North American Crustacea, in the museum
of the Smithsonian Institution. No. III. Ann. Lyceum Nat.
Hist. N.Y, 10:92-136. [Also reprinted with Notes. . . I and
II as a separate publication with continuous pagination;
the pagination of part III being: 119-163.]
V6LEZ, J., J. ZEBALLOS, AND M. MENDEZ G.
In press. Changes in the distribution pattern and abun-
dance of some fishes and crustaceans in the central coast of
Peru during the 1982-83 El Niiio. Tropical Ocean-
Atmosphere Newsletter.
WASS, M. L.
1955. The decapod crustaceans of Alligator Harbor and
adjacent inshore areas of northwestern Florida. Q. J.
Fla. Acad. Sci. 18:129-176.
WELLS, H. W.
1961. The fauna of oyster beds, with special reference to the
salinity factor Ecol. Monogr. 31:239-266.
WENNER, E. L., AND D. F BOESCH.
1979. Distribution patterns of epibenthic decapod Crus-
tacea along the shelf-slope coenocline. Middle Atlantic
Bight, U.S.A. Bull. Biol. Soc. Wash. 3:106-133.
WENNER, E. L., AND T. H. READ.
1981. Distribution and assemblages of decapod crusta-
ceans from the continental shelf of the South Atlantic
Bight: 1977-1979 MARMAP Investigations. Mar Resour
Res. Inst., S.C. Wildl. Mar Resour. Dep., Charleston, Tech.
Rep. 49, 41 p.
1982. Seasonal composition and abundance of decapod
crustacean assemblages from the South Atlantic Bight,
USA. Bull. Mar. Sci. 32:181-206.
WICKSTEN, M. E.
1980. Mainland and insular assemblages of benthic
decapod crustaceans of southern California. In D. M.
Power (editor). The California islands: Proceedings of a
multidisciplinary symposium, p. 357-367. Santa Bar-
bara Mus. Nat. Hist., Santa Barbara, Calif
WILLIAMS, A. B.
1965. Marine decapod crustaceans of the Carolinas. U.S.
Fish Wildl. Serv, Fish. Bull. 65:1-298.
1984. Shrimps, lobsters, and crabs of the Atlantic coast of
the eastern United States, Maine to Florida. Smithson.
Inst., 550 p.
WORD, J. Q., AND D. K. CHARWAT.
1976. Invertebrates of southern California coastal waters.
II. Natantia. S. Calif. Coastal Water Res. Proj., 238 p.
YOUNG, J. H.
1959. Morphology of the white shrimp Penaeus setiferus
(Linnaeus 1758). U.S. Fish Wildl. Serv., Fish. Bull.
59:1-168.
ZARIQUIEY ALVAREZ, R.
1968. Crustaceos decapodos ibericos. Cons. Superior In-
vest. Cient., Patronato Juan de la Cierva, Invest. Pesq. 32,
510 p.
ZYZNAR, E. S.
1970. The eyes of white shrimp, Penaeus setiferus (Lin-
naeus) with a note on the rock shrimp, Sicyonia breviros-
tris Stimpson. Contrib. Mar. Sci. 15:87-102.
1
79
VARIABILITY IN DIMENSIONS OF SALMONID OTOLITH NUCLEI:
IMPLICATIONS FOR STOCK IDENTIFICATION AND
MICROSTRUCTURE INTERPRETATION
John D. Neilson.i Glen H. Geen ^ and Brian Chan^
ABSTRACT
Sagittal otoliths in rainbow trout, Salmo gairdneri, and chinook salmon, Oncorhynchus tshawytscha,
arise by fusion of otolith precursors (primordia) before hatching. Size of the otolith nucleus exhibited
considerable variability even in the progeny of a single female. Otolith nucleus length was directly
related to the number and position of the primordia and water temperature at which the eggs were
incubated. This variability limits the utility of nucleus dimensions as criteria for separating sympatric
populations of juvenile steelhead and rainbow trout. Variability in otolith nucleus dimensions also
accounted for a significant error in otolith size-fish size relationships in recently hatched alevins.
The early development of otoliths is poorly un-
derstood considering their potential use in stock
identification (Postuma 1974; Rybock et al. 1975)
and in the provision of data on fish age and growth
to the daily level of precision (Pannella 1971;
Wilson and Larkin 1982). Variability of otolith
nucleus size and shape is of particular concern in
stock identification studies since nucleus dimen-
sions may be racial characteristics. Rybock et al.
(1975) have suggested a positive correlation of the
rainbow trout, Salmo gairdneri, otolith nucleus
size and the mean egg size of the female which, in
turn, is positively correlated to the size of the
female. Their data on Deschutes River steelhead
trout (the sea-run form of S. gairdneri) females,
which were larger, on average, than females of the
sympatric population of freshwater resident rain-
bow trout, led to the suggestion that otolith nu-
cleus dimensions would differ significantly and
provide a basis for racial identification of juveniles.
This hypothesis was of particular significance
since no other meristic or morphometric trait is
known which permits identification of juvenile
sea-run and freshwater resident S. gairdneri.
Nucleus dimensions might affect the widths of
concentrically formed daily growth increments
deposited around the otolith nucleus. Bipartite
daily growth increments consist of alternating
^Department of Biological Sciences, Simon Fraser University,
Bumaby, B.C. V5A 1S6; present address: Marine Fish Division,
Canada Department of Fisheries and Oceans, Biological Station,
St. Andrews, N.B., Canada EOG 2X0.
^Department of Biological Sciences, Simon Fraser University,
Bumaby, B.C., Canada V5A 1S6.
^British Columbia Fish and Wildlife Branch, Ministry of Envi-
ronment, Kamloops, B.C., Canada V2C 5Z5.
protein and calcium rich zones (Brothers 1981),
and their widths are proportional to fish growth
during the period of increment formation (Wilson
and Larkin 1982). If increment width and number
vary as a function of nucleus size and shape, then a
source of the 15% error described by Wilson and
Larkin in the estimation of fish growth from
otolith growth could be identified.
In this paper, we describe development of sagit-
tal otoliths of S. gairdneri (sea-run and fresh-
water resident) and chinook salmon, Oncorhyn-
chus tshawytscha, and examine the effect of water
temperature on otolith nucleus dimensions. These
data permit a reexamination of the hypothesis of
Rybock et al. (1975). Finally, the implications
of variability in otolith nucleus size on otolith
microstructure and its interpretation are con-
sidered.
METHODS
To study otolith nucleus development in S.
gairdneri, we obtained eggs from steelhead trout
in the Deadman River, British Columbia (B.C.), in
1981 and from the Nicola and Deadman Rivers in
1982 (Thompson River tributaries). Rainbow trout
eggs were taken from the Deadman River in 1981,
and from stocks in Mission Creek and Pennask
Lake in south-central B.C. in 1982. Prior to fertili-
zation, samples of eggs (n = 20) were taken for dry
weight determination (17 of 18 fish collected in
1982). In all cases, eggs were fertilized with pooled
sperm from 2 to 3 males of similar size and origin
as the female. In total, eggs from 10 steelhead and
11 rainbow trout were used in this study.
Manuscript accepted April 1984.
FISHERY BULLETIN: VOL. 83, NO. 1, 1985.
81
FISHERY BULLETIN: VOL. 83, NO. 1
The fertilized eggs of each female were incu-
bated in separate compartments in Heath Trays at
Abbotsford and Loon Lake trout hatcheries. In
1981, fertilized eggs from two female steelhead and
one female rainbow trout were subdivided into
three lots and held at 6.5° 9.5° and 15.0°C until
yolk-sac absorption. In 1982, all fish were held at
11°C. An approximate 12:12 LD photoperiod was
maintained through incubation and rearing.
Samples of steelhead and rainbow trout eggs or
alevins were taken at biweekly intervals in 1981.
Alevins only were sampled in 1982.
Oncorhynchus tshawytscha eggs were taken
from the 1981 Capilano River stock and were incu-
bated at 6°C under an approximate 12:12 LD
photoperiod. Hatchery practice did not allow sepa-
rate rearing of groups of eggs from individual
females.
Otolith development in S. gairdneri embryos
was studied by dissecting the embryo from the egg,
clearing it with carbol xylol, and then squashing
the embryo between two microscope slides. This
treatment, which made noncalcified tissue trans-
parent and amorphous compared with otoliths and
other hard parts, permitted otolith examination
with a transmitted light microscope at 400 x.
While we also examined embryos with X-ray and
xeroradiographic techniques, satisfactory results
were obtained more simply with the carbol xylol
treatment.
Examination of the nuclei of otoliths from ale-
vins required that otoliths be ground and polished
following the method of Neilson and Geen (1981).
The extent of the otolith nucleus in both embryos
and alevins was delimited by the first growth in-
crement encircling all central otolith precursors or
primordia (Fig. 1). The first growth increment en-
circling the central primordia generally appeared
dark when viewed with a transmitted light micro-
scope. The only primordium outside the nucleus
was in the anterior-ventral quadrant and was as-
sociated with the formation of the rostrum, the
pointed anterior extremity of the otolith showti in
Figure 1.
To avoid bias, otolith nucleus length was mea-
sured from coded preparations with an ocular
Nucleus length
Primordium
Rostral primordium
*' I
lOOiJm
Figure l.— SagitUl otolith from a Capilano River chinook salmon, Oncorhynchus tshawytscha, alevin showing the otolith
nucleus, primordia, and rostral primordium.
82
NEILSON ET AL.: DIMENSIONS OF SALMONID OTOLITH NUCLEI
micrometer along the longest axis through the
nuclear zone. The area of the otolith nucleus was
measured from photographic enlargements with a
polar planimeter. Increment widths were mea-
sured with a vernier caliper from photographic
enlargements (final magnification 9700 x). The
frequency of increment formation was determined
from slopes of regressions of increment counts
from otoliths offish of known age.
Nucleus measurements and primordia counts
are only reported for otoliths removed from the
fishes' left side as nucleus lengths were signifi-
cantly greater in left-side than right-side sagittae,
albeit at a low level of significance {P < 0.10,
Wilcoxon Paired Sample Test).
During the course of this study, otoliths from
257 rainbow trout, 187 steelhead trout, and 50
O. tshawytscha were examined.
RESULTS
To examine the hypothesis that egg size (a func-
tion of female fork length) influences otolith
nucleus length in progeny, we examined the rela-
tionship of female fork length to egg dry weight
and nucleus length in S. gairdneri. The dry weight
of steelhead and rainbow trout eggs was positively
correlated with the size of the female from which
the eggs originated (r^ = 0.54, P < 0.001, Fig. 2).
The slope of the geometric mean regression shown
0.042 -1
0.040-
0.038-
0.036
D)
0.034-
s:
^ 0.032
>.
d
Q) 0.030
o>
LlJ
c
g 0.028
0.026-
0.024
0.022-
0,020
y=0.2204x10-^(x)+0.0198
200
300
400
500
600
700
800
900
Fork Length (mm)
Figure 2. — Geometric mean regression of mean unfertilized egg dry weight on fork length of
female Salmo gairdneri from which eggs were obtained. Each point is the mean of 20 eggs from each
female. Fish in the 300-400 mm size interval were rainbow trout from Pennask Lake, those 500-600
mm were rainbow trout from Mission Creek, and those >700 mm were Deadman or Nicola River
steelhead.
83
FISHERY BULLETIN: VOL. 83, NO. 1
in Figure 2 differed significantly from zero (t-test,
P < 0.001). However, there was no significant rela-
tionship between otolith nucleus length and fe-
male fork length {t-test, P > 0.05, Fig. 3), or egg
dry weight {t-test, P > 0.10). We also investigated
the utility of otolith nucleus lengths as a racial
characteristic by calculating D^, a part of a dis-
criminant function analysis. In this instance, D^
is a measure of the power of discrimination of
nucleus length in separating juvenile sea-run and
freshwater S. gairdneri. D^ was 0.063 and was
not significant {P > 0.1).
A major source of the variability in the otolith
nucleus length-female parent length relationship
(Fig. 3) was apparently related to the ontogeny of
otolith nuclei in the salmonid embryos. Otolith
nuclei result from the fusion of primordia. Pri-
mordia, the first calcified structures to arise in S.
gairdneri during embryonic development, ap-
peared at 115-214 Centigrade degree-days. Indi-
vidual primordia increase in size by concentric
accretions, ultimately fusing with neighboring
0.24 n
0.22 ^
^ 0.20 -
Z
UJ
o
o
0.18-
O
X
I—
o
z
UJ
_J
Ul
o
§
0.16-
0.14-
0.12
0.10-
0.08-
0.06
•
•
• •
•
•
•
•
• •
•
•
•
•
•
•
•
• •
•
•
•
•
• •
• •
• •
• •
•
•
• •
•>•
•
• •
•>
•
• •
•
•
•
• •
•
• •
• ••
•
• •
•
• •
• !•
•
• •
• •
•
•>•
•
•
• '•
•
• •
• •
•
•
•>•
•
• •
•>
•
•
•
•
•
• •
• •
•
• •
• •
•
•
•
I I r -1 1 1 1
300 400 500 600 700 800 900
FEMALE PARENT FORK LENGTH (mm)
Figure 3. — Scatter plot of Salmo gairdneri female parent size
on otolith nucleus length of progeny. The origin of the adults is
given in the caption of Figure 2.
84
primordia to form the nucleus of the otolith at
226-241 degree-days (Fig. 4). Hatching occurred at
about 320 degree-days. The pattern of nucleus de-
velopment was similar in both rainbow and
steelhead trout. Although we did not follow otolith
development in O. tshawytscha, examination of
their nuclei suggested that they also arose from
fusion of multiple primordia. Deposition of growth
increments commenced immediately after fusion.
The number of primordia fusing to form the
otolith nucleus in the salmonid species we
examined was variable, even within the progeny
of a single female. In rainbow trout, there was an
average of 8. 2 ± 2.7 primordia (±1 standard devia-
tion indicated). In steelhead trout and O.
tshawytscha numbers of primordia averaged 10.7
± 2.4 and 10.1 ± 2.7, respectively. There were no
significant differences in mean primordia counts
among the three stocks of rainbow trout or the two
stocks of steelhead trout examined (analysts of
variance, P > 0.05). Figure 5 shows the relation-
ship between the number of primordia deposited
and otolith nucleus length.
The variable location of primordia within the
nucleus also affects nuclear dimensions and
further increases variability. In some instances
(<5%), primordia were formed at the periphery of
the nucleus, resulting in a local distortion of
otherwise regular growth increments (Fig. 6).
Otolith nucleus length (mm) ±1 SE in S.
gairdneri from the Deadman River was also af-
fected by incubation temperature as shown below:
Water temperature
6.5°C
9.5°C
15.0°C
Mean nucleus length (mm)
Rainbow
trout 0.142 ± 0.009 0.174 ± 0.009 0.172 ± 0.008
Steelhead
trout 0.154 ± 0.004 0.197 ± 0.008 0.191 ± 0.005
One-way analysis of variance and the Student-
Newman-Keuls test indicated that the mean
otolith nucleus length in rainbow or steelhead
trout reared at 6.5°C was significantly less (P <
0.01) than at 9.5° or 15.0°C, although no significant
differences in otolith nucleus length (P > 0.05)
existed in fish reared at the two higher tempera-
tures. The number of primordia formed in both
Deadman River steelhead and rainbow trout was
independent of the water temperature at which
the eggs and alevins were incubated (analysis of
variance, P > 0.05).
NEILSON ET AL.: DIMENSIONS OF SALMONID OTOLITH NUCLEI
/
Figure 4. — Deadman River steelhead trout sagittal primordia before fusion (right, 214 degree-days) and after fusion (left, 331
degree-days). Bar = 10 /xm.
We determined the effect of nucleus size varia-
tion on otolith size by examining correlations be-
tween nucleus area and otolith area at several
stages of development of steelhead trout and O.
tshawytscha of similar size. We chose to report
nucleus area in this case, as it reflects nucleus
dimension more precisely than one-dimensional
measurements such as nucleus length. While
nucleus area and length are significantly corre-
lated (P < 0.001), nucleus length accounted for
only 47 and 52% of the variability in nucleus area
in steelhead trout and O. tshawytscha, respec-
tively. The best correlations between nucleus area
and subsequent otolith area were noted in rela-
tively small otoliths of recently hatched alevins.
The greatest degree of variability in otolith
area occurred up to 15 d after nucleus formation
(Table 1).
Table l. — Coefficients of variability in otolith area at several
stages of development, and coefficients of determination for re-
gressions of otolith area at several stages of development. N =
15 for both steelhead trout and Oncorhynchus tshawytscha. The
steelhead trout were 29-30 mm FL, and O. tshawytscha 30-31
mm. Trout were reared at 9.5°C and O. tshawytscha at 6°C.
Steelhead trout
0. tshawytsctia
Coefficient of
Coefficient of
Coefficient determination Coefficient determination
(
Df variation
(r^) when
of variation
(r^) when
stage of otolith
in otolith
regressed on
in otolith
regressed on
development
area (%)
nucleus area
area (%)
nucleus area
Otolith area at
nucleus formation
33
n/a
23
n/a
Otolith area 15 d
after nucleus formation
15
0.41"
14
0.62"
Otolith area 35 d
after nucleus formation
6
0.21 NS
10
0.21 NS
Otolith area 50 d
after nucleus formation
7
0.16 NS
11
0.15 NS
" = P sO.01.
NS = not significant (P > 0.05).
85
FISHERY BULLETIN: VOL. 83, NO. 1
.275
.250 -
.225 -
.200 -
.175 -
.150 -
.125
.100
y=0.006(x) + 0.104
r2 = 0.34
•(2)
J L
£ .225
I- .200
O
-z.
UJ .175
CO
3 .150
LU
d .1251-
3
Z
.100
.225
.200
.175
.150
.125
.100
y=0.006{x)+0.105
r^ = 0.32
y=0.006(x)+ 0.114
r^ = 0.26
•12)
• (2)
• (2)
4 8 12 16
NUMBER OF PRIMORDIA PER SAGITTAL OTOLITH
Figure 5. — Geometric mean regressions of number of primordia per sagittal otolith on otolith nucleus length for steelhead
trout (top), rainbow trout (middle), and Capilano River Oncorhynchus tshawytscha (bottom). Trout were incubated at 9.5°C
and salmon at 6°C.
86
NEILSON ET AL.: DIMENSIONS OF SALMONID OTOLITH NUCLEI
Figure 6. — Development of a steelhead trout otolith nucleus
resulting from a peripheral primordium (top) and the typical
pattern of nucleus development (bottom). Note compression of
otolith growth increments in the postrostral quadrant. Otoliths
were from progeny of the same female parent.
We did not find any correlation between mean
increment width through the various stages of
development and nucleus area in either species
«-test, P > 0.05). In addition, examination of re-
gressions of increment counts on nucleus area
indicated that the frequency of increment forma-
tion did not vary as a function of nucleus dimen-
sion (P > 0.10 for both S. gairdneri and O. tsha-
wytscha).
DISCUSSION
Sagittal otoliths in S. gairdneri embryos arise
by fusion of primordia, the first calcified struc-
tures to appear during development (McKern et al.
1974). Radtke and Dean (1982) reported similar
results for mummichogs, Fundulus heteroclitus,
and also noted that the otolith nucleus was first
apparent as an amorphous gel-like mass in the
area of the labyrinth in the developing larvae.
Calcified primordia appeared later although
Radtke and Dean did not describe any variability
in their number or position.
The number and position of the primordia were
variable, even within the progeny of a single
female. This variation affected the extent of the
otolith nucleus. In addition, we observed that
water temperature influenced nucleus size. The
observed variation in nucleus size limits the util-
ity of this feature as a criterion for stock identifica-
tion. However, differences in nucleus size did not
affect the number of growth increments sub-
sequently formed and had no significant influence
on their width.
In our studies eggs were fertilized with the
pooled sperm of several males. It is possible that
the observed variability in otolith nucleus size was
related to the differences between the male par-
ents. There was little difference in the size of the
males used, either within the group or relative to
the females. We cannot rule out genetic differ-
ences between males as a factor affecting variabil-
ity in nucleus size. However, any genetic effects
influencing our results would be no greater than
would be expected in natural populations. The
numbers of males from which sperm was pooled
was usually three, a number frequently involved
in fertilization of eggs of a single female in nature
(Schroeder 1982; Gross in press).
In developing a hypothesis to explain the basis
for use of otolith nucleus length as a means of
distinguishing races, Rybock et al. (1975)
suggested that nucleus length was related to egg
size, although no data were presented. While we
found that greater nucleus lengths were as-
sociated with larger eggs on average, and larger
eggs originated from larger female parents, the
slope of the regression of nucleus length on egg
weight was not significant (Fig. 3). Furthermore,
the variability of otolith nucleus dimensions in
rainbow and steelhead trout from south-central
B.C. made their measurement much less useful for
stock identification that has been suggested for S.
gairdneri from the Deschutes River, Oreg. (Rybock
87
FISHERY BULLETIN: VOL. 83, NO. 1
et al. 1975). However, otolith nucleus dimensions
did serve to separate summer and winter races of
steelhead trout (McKern et al. 1974). Workers
proposing to use otolith nucleus dimensions as
stock identification criteria should consider rear-
ing fish under controlled conditions to establish
the extent of nucleus size variability in the stocks
in question.
Otolith nucleus length is also influenced by
water temperature during embryonic develop-
ment. Our data showed an increase of about 25%
in length in fish reared at 9.5° or 15°C relative to
that observed in fish incubated at 6.5°C. The sen-
sitivity of otolith nucleus length to water tempera-
ture may allow separation of selected fish stocks
whose eggs are incubated at different water tem-
peratures. For example, O. tshawytscha juveniles
originating from Campbell River stock reared in
the Canada Department of Fisheries and Oceans
Quinsam Hatchery on Campbell River had sig-
nificantly greater otolith nucleus lengths (P <
0.01) than wild Campbell River O. tshawytscha
incubated in cooler waters (M. Bradford pers.
commun.^). Increased water temperature may in-
fluence nucleus length through a greater rate of
accretion of the calcium/protein matrix around
primordia, reflecting a faster rate of embryonic
development.
The definition of otolith nucleus suggested here
can be consistently applied. With relatively simple
preparation techniques, otolith nucleus dimen-
sions can be measured from micrographs or by
using a light microscope equipped with an ocular
micrometer Previous workers have delimited the
otolith nucleus in relation to metamorphic or
nuclear checks. Such terms are ill-defined and
should be avoided since they imply that otolith
checks result from important developmental
events. While it seems likely that such events may
result in growth interruptions or checks, causal
links have not yet been demonstrated.
The imprecise definition of the periphery of the
otolith nucleus may reduce the comparability of
measured dimensions derived in various studies.
While we have defined the nucleus as lying within
the first increment surrounding the primordia,
several checks occur during early otolith develop-
ment. Use of one of these checks to define the
periphery of the nucleus would result in inconsis-
tency between various investigations. For exam-
ple, nucleus lengths of steelhead trout used in this
*M. Bradford, Department of Biological Sciences, Simon
Fraser University, Burnaby, B.C., Canada V5A 1S6, pers. com-
mun. November 1983.
88
study were generally <0.2 mm (Fig. 3). The mean
diameter of the otolith nucleus of summer and
winter steelhead reported by McKern et al. (1974)
were 0.348 and 0.436 mm, respectively. Differ-
ences between studies of this magnitude may be
racial in nature or may reflect differences in defi-
nition of the extent of the nucleus.
Data on variation in primordia number and lo-
cation have not been reported previously although
the existence of primordia was described by
Radtke and Dean (1982) in mummichogs. McKern
et al. (1974) did not describe primordia in their
work involving the otolith nucleus in steelhead
trout. Their results were based on the use of X-ray
techniques. We were not able to detect primordia
using this method.
It is likely that the otoliths of many fish species
are formed by fusion of multiple primordia. From
our observations, this is apparently the case in all
five species of Pacific salmon and the Pacific her-
ring, Clupea harengus pallasi. Radtke and Dean
(1982) noted multiple primordia in masou salmon,
O. masou; Arctic char, Salvelinus alpinus; brook
trout, S. fontinalis; and the sculpin, Cottus
nozawa.
While both steelhead trout and O. tshawytscha
otolith nucleus areas were variable, otolith areas
in older fish (longer than 15 d after primordia
fusion) were less so as indicated by the decreasing
coefficient of variation of otolith area with increas-
ing age (Table 1). The decreased variation proba-
bly reflects the development of otoliths from an
indeterminant array of primordia to the otoliths of
adult fish, the latter considered a species-specific
characteristic (Fitch 1968; Morrow 1979). How-
ever, variation in otolith development in the
juvenile salmonids studied here do not present
difficulties for the interpretation of microstruc-
ture as neither the number nor width of growth
increments is significantly affected by nucleus
size variation.
ACKNOWLEDGMENTS
The cooperation of the staff at British Columbia
Department of the Environment fish hatcheries at
Abbotsford, Loon Lake, and Summerland is grate-
fully acknowledged. In particular, we wish to
thank John Cartwright, Dennis Graf, Chris Hous-
ton, Bob Land, Don Peterson, and Hugh Sparrow
for their exceptional support. Eldon Stone of the
Canada Department of Fisheries and Oceans
Capilano Hatchery provided the chinook salmon
used in this study. Mike Bradford suggested calcu-
NEILSON ET AL.: DIMENSIONS OF SALMONID OTOLITH NUCLEI
lation of the D^ statistic. Barbara Puselja and
Tracey Crawford assisted with otolith preparation
and examination. Ron Long, Department of
Biological Sciences, Simon Fraser University, pre-
pared the photographs. This work was supported
by a Graduate Research Engineering and
Technology Award to G. H. Geen from the British
Columbia Secretariat of Science, Research and
Development, and a Canada Department of
Fisheries and Oceans Subvention Grant.
LITERATURE CITED
Brothers, E. B.
1981. What can otolith microstructure tell us about daily
and subdaily events in the early life history of
fish? Rapp. P.-v. Reun. Cons. int. Explor Mer 178:393-
394.
Fitch, J. E.
1968. Fish otoliths in cetacean stomachs and their impor-
tance in interpreting feeding habits. J. Fish. Res. Board
Can. 25:2561-2574.
Gross, m. r.
In Press. Sunfish, salmon and the evolution of alternative
reproductive strategies and tactics in fishes. In R. J.
Wooton and G. Potts (editors). Fish reproduction:
strategies and tactics. Acad. Press, N.Y.
MCKERN, J. L., H. F HORTON, AND K. V. KOSKI.
1974. Development of steelhead trout (Salmo gairdneri)
otoliths and their use for age analysis and for separating
summer from winter races and wild from hatchery
stocks. J. Fish. Res. Board Can. 31:1420-1426.
MORROW, J. E.
1979. Preliminary keys to otoliths of some adult fishes of
the Gulf of Alaska, Bering Sea, and Beaufort Sea. U.S.
Dep. Commer., NOAA Tech. Rep. NMFS CIRC 420, 32 p.
NEILSON, J. D., AND G. H. GEEN.
1981. Method of preparing otoliths for microstructure
examination. Prog. Fish-Cult. 43:90-91.
PANNELLA, G.
1971. Fish otoliths: daily growth layers and periodical pat-
terns. Science (Wash., D.C.) 173:1124-1127
POSTUMA, K. H.
1974. The nucleus of the herring otoliths as a racial
character. J. Cons. Int. Explor. Mer 35:121-129.
RADTKE, R. L., AND J. M. DEAN.
1982. Increment formation in the otoliths of embryos, lar-
vae, and juveniles of the mummichog, Fundulus hetero-
clitus. Fish. Bull., U.S. 80:201-215.
RYBOCK, J. T, H. F. HORTON, AND J. L. FESSLER.
1975. Use of otoliths to separate juvenile steelhead trout
from juvenile rainbow trout. Fish. Bull., U.S. 73:654-
659.
SCHROEDER, S. L.
1982. The influence of intrasexual competition on the dis-
tribution of chum salmon in an experimental stream. In
E. L. Brannon and E. O. Salo (editors), Salmon and trout
migratory symposiiun, p. 275-285. School Fish. Univ.
Wash.
Wilson, k. h., and p a. larkin.
1982. Relationship between thickness of daily grovrth in-
crements in sagittae and change in body weight of sockeye
salmon (Oncorhynchus nerka) fry. Can. J. Fish. Aquat.
Sci. 39:1335-1339.
k
89
EFFECTS OF FEEDING REGIMES AND DIEL TEMPERATURE CYCLES ON
OTOLITH INCREMENT FORMATION IN
JUVENILE CHINOOK SALMON, ONCORHYNCHUS TSHAWYTSCHA
John D. Neilson' and Glen H. Geen'^
ABSTRACT
The effects of constant and diel cyclic water temperature regimes, feeding frequency, fish activity, and
ration level on growth increment formation in juvenile chinook salmon, Oncorhynchus tshawytscha,
are described. Of the variables examined, any event which recurred more than once every 24 hours
increased the rate of increment production above 1 increment per 24 hours. The results were consistent
with the hypothesis that environmental variables modify the rate of increment formation by altering
the periodicity of fish activity. Both water temperature and ration level interacting with water
temperature affected otolith increment width, a measure offish growth, although ration level did not.
To realize the potential of otolith microstructure
in detailed age and growth studies of fishes,
knowledge of factors influencing otolith growth is
required. The principle features of otoliths likely
to be used in such studies are the growth incre-
ments which are deposited in a concentric fashion
around the otolith nucleus. The frequency of depo-
sition (often 1 increment/24 h) and the width of the
increments are both affected by environmental
conditions (Neilson and Geen 1982).
The growth increments result from accretion of
CaCO^ and to a lesser extent, protein (Simkiss
1974). The daily nature of their deposition ob-
served by many workers (Pannella 1971; Brothers
et al. 1976; Wilson and Larkin 1982; and others)
appears related to a daily rhythm in the relative
rates of calcium carbonate and protein deposition
(Mugiya et al. 1981). The cyclic deposition of cal-
cium and protein over a 24-h period results in the
formation of the bipartite features now referred to
as daily growth increments.
The effects of environmental variables on
otolith increment formation have been the subject
of some controversy. Taubert and Coble (1977) con-
cluded that a 12:12 LD photoperiod was responsi-
ble for entraining diel rhythms in the growth of
juvenile Lepomis and Tilapia sp. otoliths. How-
ever, juvenile starry flounder, Platichthys stel-
^ Department of Biological Sciences, Simon Fraser University,
Bumaby, B.C., Canada V5A 1S6; present address: Marine Fish
Division, Canada Department of Fisheries and Oceans, Biologi-
cal Station, St. Andrews, N.B., Canada EOG 2X0.
^Department of Biological Sciences, Simon Fraser University,
Bumaby B.C., Canada V5A 1S6.
Manuscript accepted February 1984.
FISHERY BULLETIN: VOL. 83. NO. 1, 1985.
latus, and chinook salmon, Oncorhynchus
tshawytscha , continued to produce daily growth
increments when exposed to constant light (Cam-
pana and Neilson 1982; Neilson and Geen 1982).
The latter authors presented evidence that feed-
ing frequency affected both increment number
and width in O. tshawytscha . They also suggested
that feeding frequency (or any other environmen-
tal variable) was probably not the ultimate factor
determining the frequency of otolith increment
production. Environmental modulation of endo-
crine rhythms (Menaker and Binkley 1981) may
ultimately control otolith increment periodicity.
Diel cycles in water temperature have received
little consideration as an environmental variable
potentially affecting increment formation.
Brothers (1978) suggested that diel temperature
variations were responsible for otolith increment
formation in temperate stream-dwelling fish al-
though no data were presented. This gap in our
understanding of factors influencing otolith in-
crement production is significant since diel
changes in water temperature are a common fea-
ture of aquatic environments. In this study we
examined the effects of diel water-temperature
regimes on formation of otolith growth increments
in O. tshawytscha alevins and fry. We also present
data on the effects of interactions of water-
temperature regimes, feeding frequency, and ra-
tion level on otolith increment formation in O.
tshawytscha fry. Finally, we tested the suggestion
made earlier (Neilson and Geen 1982) that feeding
periodicity (or any other periodic event affecting
fish activity) modifies the rate of otolith increment
production through changes in fish activity.
91
FISHERY BULLETIN: VOL. 83, NO. 1
METHODS
Alevins
Fish used in the experiments described below
originated from the 1981 brood of the Canada De-
partment of Fisheries and Oceans Capilano
Hatchery. Eggs were transferred to incubation
facilities at Simon Fraser University at the "eyed"
stage of development, corresponding to 347 Cel-
sius degree-days. Prior to transfer, the eggs were
held under a 12:12 LD photoperiod and at a con-
stant 8°C water temperature. The eggs were held
for 5 d in our laboratory at 8.5°C before exposure to
diel water-temperature regimes.
Two lots of 100 fish were exposed as eggs and
later, as alevins, over a 69-d period to a water-
temperature regime whose diel amplitude aver-
aged 2" and 4°C (range 1.8°-2.4° and 3.0°-4.5°C)
above a daily average minimum temperature of
8.5°C. These temperatures were similar to those
observed in May-June 1981 in the Deadman River,
B.C., a stream supporting an O. tshawytscha
population. All eggs hatched by day 29. Eggs or
alevins in = 10) were sampled at days 19, 40, 55,
and 69. On day 39, 20 alevins were transferred
from a temperature regime with a 4°C amplitude
and 24-h period to a regime with the same temper-
ature amplitude but a 12-h period. A fourth group
was held at a constant 8.5°C. The constant water
temperature corresponded to that of the cool
period of the diel water-temperature regimes.
Sagittal otoliths were removed from preserved
fish and prepared following the methods of Neilson
and Geen (1981). Otolith sections were examined
using a light microscope or scanning electron mi-
croscope (SEM) as described in Neilson and Geen
(1982).
Fry
Fry used in these experiments were about 90-d-
old posthatch and originated from Capilano River
hatchery stock. Prior to transfer to 25 1 aquaria at
Simon Fraser University, fish were held under
natural light at a constant 8°C and fed once every
24 h. After transfer to our laboratory, fry were held
for 2 wk in flow-through aquaria supplied with
aerated and dechlorinated water at 6°C before ex-
periments commenced. During this period the 50
fish in each aquarivun were fed to satiation with
Oregon Moist Pellets once per 24 h and exposed to
a 12:12 LD photoperiod.
Experimental feeding and temperature regimes
to which fry were exposed are summarized in
Table 1. Amplitude of daily temperature fluctua-
tions was 4°C (range 3.6°-4.4°C) above the average
minimum of 6°C. The diel temperature cycle in
relation to photoperiod and feeding events is
shown in Figure 1. The activity of one group offish
was artificially increased to examine the effects of
activity on otolith increment formation. These fish
were forced to evade a slowly moving aquarium
net for 10-min beginning at 1900 h daily. The in-
duced activity level appeared similar to that as-
sociated with feeding. Ration provided to experi-
mental lots of fish was maintained as a constant
proportion (4% or 8% ) of average fish dry weight by
105-
9.5-
O
0)
2
«
a.
E
®
0)
IS
$
w 8 5"
7.5-
6.5-
5.5
0100 0500 f 1000 1500 f 2000 0100 0600 f
1 1 00 1 600
t 2100
2400
Time (24-h clock)
Figure \. — Did water-temperature cycle in relation to photoperiod and feeding events (f)
for Oncorhynchus tshawytscha fry. Light and dark periods are indicated by the open and
solid bars respectively.
92
NEILSON and GEEN: CHINOOK SALMON OTOLITH INCREMENT FORMATION
Table L — List of abbreviations denoting
experimental regimes to which On-
corhynchus tshawytscha fry were exposed
in 1982. Percent ration (% of body
weight offered every 24 h ) is given and the
water temperature at time of feeding dur-
ing the diel cycle, if applicable, is indi-
cated in parentheses. Refer to Figure 1 for
details of feeding, temperature, and
photoperiod regimes.
Time of feeding
Treatment
(h)
8% (warm)
0700
8% (cool)
1900
8% (constant)'
0700
4% (warm)
0700
4% (cool)
1900
4% (constant)'
0700
2 X 4%2
0700 and 1900
2 X 2% 2
0700 and 1900
4% + activity^
0700
Starvation
n/a
' Fish in these treatments were held at constant
temperature.
^Fish in these treatments were fed 2 times per
24 h.
^Fish in this treatment were held at a constant
temperature and exposed to a 10-min bout of
forced activity at 1900 h every day.
adjusting total food offered as fish grew or were
sampled. Every third day, excess food was removed
from the aquaria within 30 min of offering,
weighed, and consumption estimated.
On day 26, we exposed fry for 30 min to a hyper-
tonic solution of 1 g/1 sodium chloride and 40 mg/1
oxytetracycline hydrochloride. The tetracycline
was incorporated into the otolith and provided a
time marker which exhibited fluorescence when
viewed with ultraviolet illumination. All fry were
successfully marked by this method.
Originally, we had intended to sample 15 fish at
days 10, 20, and 40. However, an accidental inter-
ruption of the dechlorinated water supply on day
19 resulted in the mortality of some fish in treat-
ments 4% (cool), 4% (constant), 2 x 4%, and 4% +
activity. Complete mortality of starved fish oc-
curred at that time. To ensure an adequate (N ^
10) sample on experiment completion, no samples
were taken at day 20 for the above four treat-
ments. Even so, only five fish remained by day 40
in the 4% (cool) treatment.
Fork lengths were determined immediately
after the fish were sacrificed. Fish were then dried
to a constant weight (60°C for 48 h) in individual
labeled containers, and weighed. Sagittal otoliths
were then removed, weighed with an electrobal-
ance, and prepared for examination with the SEM
or a light microscope.
Increment counts were conducted as described
by Neilson and Geen (1982). No attempt was made
to distinguish between the daily and subdaily in-
crements as did Brothers (1978) and Campana
(1983). Such distinctions are often based on subjec-
tive appraisals of increment continuity and ap-
pearance when viewed with a light microscope. We
did not observe any such differences in growth
increments of O. tshawytscha. Moreover, as the
purpose of this study was to determine the
periodicity of increment formation as a basis for
detailed study of fish growth, the classification
of increments as daily or subdaily was not neces-
sary.
RESULTS
Eggs and Alevins
The formation of growth increments com-
menced before hatching under all experimental
regimes. One increment/24 h was formed on aver-
age under all temperature regimes (Table 2). No
significant departure from unity was noted (anal-
ysis of variance, P > 0.05). However, the appear-
ance of the daily growth increments differed be-
tween treatments. Otoliths offish subject to a cycle
of temperature were characterized by more regu-
lar and easily observed growth increments than
those held under constant temperatures (Fig. 2).
Examination with a SEM at 1,000 x revealed
that the bipartite nature of otolith growth incre-
ments differed between the temperature regimes.
After etching with a weak acid (Neilson and Geen
1982), the relatively deeply etched portion of the
bipartite growth increment (corresponding to the
opaque portion of the bipartite structures when
viewed with a transmitted light microscope) com-
prised a larger average fraction of the growth in-
crements (P < 0.01) in otoliths offish subjected to a
diel cycle in temperature than those offish held at
constant water temperatures. The lightly etched
portion of daily growth increments did not differ
significantly between fish held in diel temperature
regimes with 2°C and 4°C amplitude (analysis of
Table 2. — Summary of Oncorhynchus tshawytscha otolith in-
crement counts for alevins held under various temperature re-
gimes.
Experiment
1
Increment count'
day
Constant temperature
2°C amplitude
4°C amplitude
19
17.8±2.6
18.5± 1.2
17.4± 1.0
40
—
38.0 ±2.4
39.5±2.1
55
51.82:2.8
54.1 ± 1.9
53.3 ±3.0
69
68.4 ±5.6
68.4±4.1
70.2 ±4.6
'± 1 standard deviation indicated, n = 1 0.
93
V*
\
i -»k'.
E
:t
o
in
FISHERY BULLETIN; VOL. 83, NO. 1
variance and the Student-Newman-Keuls test, P
> 0.05).
Oncorhynchus tshawytscha transferred from a
4°C diel temperature regime (24-h period) to a
regime with a 12-h period and similar amplitude
produced an average of 1.56 increments/24 h. The
slope of the regression of mean increment count on
experiment day differed significantly from unity
(P < 0.01). An example of an otolith from a fish
exposed to the 12-h period, cyclic temperature re-
gime is shown in Figure 3 and illustrates the nar-
rower increments associated with the 12-h cycle.
y
u
o
CM
SO
<u
a, iti
■a 0)
3 w
■ - (U
-a. ^
6 -2
« g
't s
c
bo c
t. c
3 C8
2 ^
11
||
tg
^ o.
.2 £
T3 ca
c c
TO ;0
a
■C CO
■s *
is >-
0) O
e 6
1 «
^^
CC -4-*
2 I
Fry
Otolith growth increments were formed at the
rate of one every 24 h in fish fed once per day. No
significant departures were noted (^-tests, n ^ 20,
P > 0.05). Fish which received 2 feedings/24 h or 1
feeding and a 10-min bout of activity deposited
significantly >1 increment/24 h (i-tests, P < 0.01).
Arithmetic mean regressions of increment counts
on experiment day for the latter treatments are
given below:
Treatment
Regression equation
r^
8% B.W. ration fed
y= 1.45U)+1.58
0.91
2 times/24 h
4% B.W. ration fed
J = 1.76 (x)- 1.40
0.98
2 times/24 h
4% B.W. ration and
y = 1.50(x)-0.80
0.93
forced activity
Slopes of regressions in groups of fish producing
>1 increment/d did not differ significantly from
each other (analysis of covariance, P > 0.10).
The distributions of increment widths in fed
groups of fish are presented in Figure 4. A sum-
mary of the comparisons of increment width data
among treatments is provided in Figure 5. One-
way analysis of variance and the Student-
Newman-Keuls test indicated that mean incre-
ment widths in otoliths offish receiving a ration of
8% B.W./24 h in one feeding differed significantly
between groups (P < 0.05). Mean increment
widths in otoliths of fish receiving a ration of 4%
B.W./24 h in one feeding did not differ signifi-
cantly in fish receiving the ration either during
the cool or warm portion of the diel temperature
cycle (Student-Newman-Keuls test, P > 0.05).
However, fish receiving 4% B.W./24 h under con-
stant water temperature produced growth incre-
ments whose mean width was significantly less
than those of fish held in the diel water-
94
NEILSON and GEEN: CHINOOK SALMON OTOUTH INCREMENT FORMATION
Figure 3. — Change in otolith microstructure in a Oncorhynchus tshawytscha alevin
transferred from a 24-h period temperature cycle (4°C amplitude) to a 12-h period tempera-
ture cycle (4°C amplitude).
50 ^tm
temperature regimes (P < 0.05, Student-
Newman-Keuls test).
The top two horizontal strata of Figure 4 consti-
tute a 3 X 2 factorial design and were examined
with a two-way analysis of variance. The effects of
time of feeding with respect to the diel tempera-
ture cycle, ration level, and their interaction were
examined in relation to mean otolith increment
width. The effect of time of offering with respect to
the diel temperature cycle on mean increment
width was significant (P < 0.001), whereas ration
level was not (P > 0.05). The interaction of time of
offering in relation to the diel temperature cycle
and ration level on otolith increment width was
also significant (P < 0.001).
Fish in treatments receiving 2 feedings/24 h or
fed once per 24 h and exposed to a 10-min bout of
activity produced growth increments whose aver-
age widths were significantly less than those of
fish in treatments fed the same ration once per 24
h. Treatments in which fish received either rations
of 8% or 4% with 1 or 2 feedings/24 h comprise a
2x2 factorial design, and were analyzed with a
two-way analysis of variance. Increased feeding
frequency significantly reduced mean increment
width (P < 0.001), although ration level did not (P
> 0.1). The interaction of feeding frequency and
ration level was not significant (P > 0.1).
Widths of otolith increments formed when fish
were fed 4% B.W./24 h and subjected to a 10-min
bout of activity were not significantly different
from widths of increments in fish which received
two feedings equivalent to the 4% B.W./24 h ration
level ( ^-test, P > 0.05). However, fish fed a ration of
8% B.W./24 h with two feedings produced incre-
ments whose average width was significantly
greater than the latter two treatments (analysis of
variance and the Student-Newman-Keuls test, P
< 0.01). Mean increment widths in fish fed 4%
B.W./24 h and exposed to a constant water-
temperature regime were compared with incre-
ment widths in fish receiving the same ration plus
95
FISHERY BULLETIN: VOL. 83, NO. 1
(0
o
c
(1)
k_
o
o
O
>
DC
50n
8% (warm
mean width = 3. 77
no. of increments=386
(099)
8% (cool)
8%(constant)
mean wiclth= 2.78
no. of increments =384
(0.96)
mean width = 2.29
no. of increments = 36 3
(0.94)
J
50-,
25-
4% (warm)
mean width = 3.06
no. of increments = 37 4
(0.98)
rw
0
50n
4%(cool)
I2=i
mean width = 3.21
no of increments = 1 80
(0.99)
4% (constant)
mean width = 2.23
no. of increments = 393
(1.02)
i=.
25-
0-
2 X 4%
mean width = 1 66
no of increments=588
(1.45)
J^
5
10
2x2%
mean width = 1 .45
no of increments = 733
(1-76)
i.
— r-
5
10
4% + activity
mean width = 1 .34
no of increments =556
(1 50)
10
Increment Width i/jjm)
Figure 4. — Distribution of otolith increment widths under the experimental regimes. Treatments are identified by numbers in the
top-left comers of histograms and correspond to treatments listed in Table 1. The average rate of increment formation every 24 h is
shown in brackets.
8%(warm) ». 8%(cool)
8%(constant)-
4%(warm
Figure 5. — Summary of Student-Newman-Keuls or <-test (a =
0.05) comparisons of mean increment widths in Oncorhynchus
tshawytscha fry held under the various experimental regimes.
Arrow heads pointing left or right signify "less than" and
"greater than" respectively.
96
a 10-min period of enforced activity. The mean
increment width associated with the latter treat-
ment was significantly less (^-test, P < 0.01).
Production of the narrower growth increments
associated with 2 feedings/24 h or 1 feeding and
induced activity did not occur immediately upon
commencement of the experimental regimes. A
period of transition in otolith microstructure was
evident. Figure 6 shows the decrease in increment
widths with time in fish previously provided a
ration of 8% B.W./24 h in one feeding and then
offered the same total ration in 2 feedings/d. For
comparison, data on increment widths in fish fed
8% B.W./24 h are provided (Fig. 6). The slope of the
regression of increment width on date in the latter
NEILSON and GEEN: CfflNOOK SALMON OTOLITH INCREMENT FORMATION
3.5n
E 3-
•g
5 2.5-
c
(0
0)
2-
c
0
E
b
c
ii.5-
o
O
1-
0.5-
^-
'^o ■ "o
■ o
0
I
10
~^
— I —
30
— I —
40
Experiment Day
50
Figure 6. — Mean otolith increment widths (0) for Oncorhyn-
chus tshawytscha fry from the 2 x 4% experimental feeding
regime over days 1-40. Prior to day 1, fish were fed once every 24
h. Also shown are mean increment widths ( ■ ) offish from the 8%
(constant) feeding regime, where fish received one feeding only
every 24 h.
treatment did not significantly differ from zero (P
> 0.10), whereas the former did (f-test, P < 0.01).
Starved fry continued to produce one otolith in-
crement every 24 h. However, the growth incre-
ments were faint when observed with a transmit-
ted light microscope. That portion of otolith
growth formed under starvation conditions was
more transparent than the portion of otolith
growth produced when fish were fed. Growth in-
crement diel periodicity was also more pronounced
during the portion of otolith growth corresponding
to that period when fish were fed (Fig. 7).
To confirm that increment widths were propor-
tional to fish growth, we plotted instantaneous
growth in dry weight against average increment
width for all treatments except the starved group
(Fig. 8). The coefficient of determination (r^) as-
sociated with those treatments in which fish
formed 1 growth increment/24 h was 0.735 and the
slope of the regression was significantly different
from zero (P < 0.01). Note that points associated
with treatments in which fish formed more than 1
increment/24 h lie considerably above the regres-
sion. The regression of these data differs signifi-
Fed 1x/24h
%
SOyum
Figure 7. — Example of otolith microstructure from a starved Oncorhynchus tshawytscha salmon fry when viewed with transmitted
light microscopy. The relatively transparent region near the otolith periphery corresponds to the starvation period.
97
FISHERY BULLETIN: VOL. 83, NO. 1
UJ
o
or
o
(/)
Z)
o
to
3.0 ^
2.5-1
2.0-
1.5-
1.0 -
0.5
0.0
8% (warm)
,4% (cool)
4%X2 >^ 4% (warm)
D 4% (constant)
8% (cool)
2% X 2
4% + activity
o
8% (constant)
— 1 1 1 1
AC o Q ^ '^
MEAN INCREMENT WIDTH (urn)
3.5
4
Figure 8. — Regressions of mean otolith increment width versus instantaneous growth rate (dry weight) for the various
experimental regimes. Solid line represents groups where fish produced one increment every 24 h on average; dashed line
represents treatments where fish produced significantly more than one increment every 24 h.
cantly in both slope and y-intercept (analysis of
covariance and Mest, P < 0.01) from that of fish
fed once per day.
Slopes of arithmetic mean linear regressions of
fish dry weight on experiment day indicated that
the average rate of growth offish fed 8% B.W./24 h
at the beginning of the warm portion of the diel
temperature cycle was significantly greater than
that offish fed at the beginning of the cool period of
the diel temperature regime or at the constant
water temperature (6°C) (analysis of covariance
and the Student-Newman-Keuls test, P < 0.01).
Similar analyses among treatments in which fish
were fed 4% B.W./24 h [4% (warm), 4% (cool), 4%
(constant)] or among fish that received two feed-
ings or one feeding coupled with an additional
bout of activity (2 x 4%, 2 x 2%, 4^^ + activity)
indicated no significant differences in growth rate
(P> 0.05).
To determine whether otolith growth-fish
growth relationships were similar among treat-
ments, we calculated otolith weight-fish dry
weight regressions for data from all experimental
regimes. Analysis of covariance indicated that the
98
slopes of the predictive regressions among groups
of fish fed 8% B.W./24 h and exposed to different
temperature regimes did not significantly differ
from each other (P > 0.1). Nor were there signifi-
cant differences among treatments in which fish
were fed twice/24 h or fed once/24 h and exposed to
an enforced 10-min bout of activity. The slope of the
regression representing the otolith weight-fish
weight relationship for those fish receiving a ra-
tion of 4% B.W./24 h on the cool portion of the diel
cycle was significantly greater than the slopes of
regressions representing fish fed 4% B.W./24 h
(warm or constant) (analysis of covariance and the
Student-Newman-Keuls test, P < 0.05). However,
as mentioned earlier, the treatment where fish
received a ration of 4*^ B.W./24 h on the cool por-
tion of the diel temperature cycle was affected by
an interruption in water supply. Only five fish
survived to day 40 and may not have been repre-
sentative offish held under those conditions.
DISCUSSION
Under most environmental conditions consid-
NEILSON and GEEN: CHINOOK SALMON OTOUTH INCREMENT FORMATION
ered during this study and reported by Neilson
and G«en (1982), one otolith growth increment
was formed each day. This supports the hypothesis
that an endogenous rhythm influences growth in-
crement formation. Earlier, Neilson and Geen
(1982) reported that multiple feedings within a
24-h period resulted in the formation of >1
increment/24 h. We suggested that this resulted
from the interaction of an endogenous diel rhythm
of increment production and some regularly re-
curring environmental event. Data presented
here are consistent with that view, as increased
feeding frequency, exposure to a warm/cool tem-
perature cycle twice in 24 h and an enforced in-
crease in fish activity were all associated with an
increased rate of increment formation. The effects
of at least some of these environmental events on
otolith microstructure may be mediated through
activity-induced modification of fish metabolism,
which often follows a circadian rhythm (Matty
1978). If otolith growth increment production fol-
lows a circadian rhythm that is sometimes over-
lain by environmental events, it seems reasonable
to assume that fish may produce one or more
growth increments but not less than one every 24
h. In our studies, O. tshawytscha alevins and fry
produced one or more growth increments every 24
h, a result consistent with most earlier studies.
Even when fish were exposed to light and tempera-
ture stimuli with periods >24 h, Campana and
Neilson (1982) reported that only one increment
was formed every 24 h.
Diel water-temperature fluctuations were not
required for otolith increment production in O.
tshawytscha. However, cyclic changes in tempera-
ture with a 24-h periodicity apparently result in
differences in the appearance of otolith growth
increments (Fig. 2). The deeply etched portion of
the increments is significantly wider in otoliths of
fish taken from a diel water-temperature regime
than those from fish held in water of constant
temperature. Mugiya et al. (1981) concluded that
the deeply etched portions of goldfish, Carassius
auratus, otoliths have a relatively high concentra-
tion of protein relative to calcium carbonate.
Degens et al. (1969) suggested that the deposition
of the organic matrix is not readily modified by
environmental events. If these results are appli-
cable to salmonids, the greater contrast in otoliths
of fish reared under a diel temperature regime
may result from changes in the rate of calcium
carbonate deposition. However, the presumed
change in composition and structure of daily
growth increments produced under various en-
vironmental conditions does not affect the incre-
ment width-fish growth relationship illustrated in
Figure 8.
Interactions between ration level and time of
feeding with respect to the 24-h temperature cycle
affected mean increment width. Ration level as a
single factor influencing increment width was not
significant. However, the interaction between
temperature and ration on increment width was
not significant suggesting higher calcium car-
bonate deposition on the otolith when temper-
atures were elevated at time of feeding. In a
two-way comparison with ration level and feed-
ing frequency (water temperature was constant),
increment width was affected by feeding fre-
quency but not by ration level. This agrees with
the results of Neilson and Geen (1982) who showed
that the rate of increment production is affected by
feeding frequency.
Mean increment width reflected fish growth
under a variety of water-temperature and ration
regimes (Fig. 8). However, different equations de-
scribed increment width-growth relationships
under conditions that produced 1 increment/d or
>1 increment/d (Fig. 8). The extent to which in-
crement width data can be used to predict instan-
taneous growth rates in natural populations re-
mains to be examined.
Increment widths can provide an indicator of
environmental changes and consequent alteration
of growth rates. However, such changes, at least
under laboratory conditions, did not occur rapidly
(Fig. 6). These data suggest that at least 3 wk
would be required before the change in increment
width would be statistically detectable.
Our data indicate that otolith weight-fish
weight regressions are similar under a range of
experimental conditions suggesting that otolith
growth in salmon fry is closely coupled to fish
growth. Marshall and Parker (1982) also reported
that differences in ration and water temperature
did not significantly affect slopes of otolith size-
fish size regressions among fed sockeye salmon, O.
nerka, fry. Exceptions to the isometric growth re-
lation between fish size and otolith size have only
been observed in recently hatched salmonid ale-
vins (Neilson unpubl. data) and in starved O.
tshawytscha fry. Fry deprived of food for 19 d con-
tinued to form daily growth increments. Assum-
ing fish dry weight did not increase over this
period, then the slope of the otolith weight-fish
weight regression would probably be greater than
for fed fish. Marshall and Parker (1982) also re-
ported continued otolith growth in O. nerka fry
99
FISHERY BULLETIN: VOL. 83, NO. 1
over a 2-wk starvation period. Evidently con-
tinued otolith growth in starved fish resulted from
the metabolism of stored energy reserves.
Estimates of food consumption indicated that
fish held under diel cyclic temperatures and fed 89c
B.W./24 h consumed significantly more food per
gram of fish when the food was offered during the
warm period (^-test, P < 0.01). No differences in
food consumption were noted in fish receiving a 4%
B.W./24 h ration on either the warm or cool portion
of the diel water-temperature regime (^-test, P >
0.05). It is likely that fish were not satiated at this
ration under either water- temperature regime.
Under the high ration, fish were satiated even
when the food was offered during the cool period of
the water-temperature cycle. Additional con-
sumption occurred only if food was offered during
the warm portion of the diel temperature cycle.
The additional food consumption was associated
with increased growth rates. It is not clear
whether the increased growth was simply a re-
sponse to differences in food consumption or also
reflected enhanced efficiency of food utilization in
fish exposed to cyclic temperatures similar to that
described by Brett (1979) and Biette and Geen
(1980). Differences in growth rate of fish fed 4%
B.W./24 h strongly suggest more efficient food
utilization in fish exposed to a cyclic temperature
regime. Food consumption did not differ although
growth rates (and increment widths) are signifi-
cantly greater
Given that water temperature and food con-
sumption are considered the most important fea-
tures of fishes' environment affecting their growth
(Paloheimo and Dickie 1966), it is not surprising
that water-temperature regimes and ration levels
influence otolith growth increment production.
Our findings and those of English (1981) suggest
that interpretation of prey abundance and feeding
success from otolith microstructure data may be
masked by relatively small changes in water
temperature. Workers attempting to quantify fish
growth with respect to ration size through exami-
nation of otolith microstructure should be aware
of the effects of water temperature documented
here and design studies accordingly.
ACKNOWLEDGMENTS
We thank Eldon Stone of the Canada Depart-
ment of Fisheries and Oceans Capilano Hatchery
for providing the fish used in this study Tracey
Crawford and Jeff Johansen assisted with otolith
preparation. Ron Long, Department of Biological
100
Sciences, Simon Eraser University, prepared the
photographs. The critical review of an earlier draft
of this manuscript by S. Campana and M. Healey
is particularly appreciated. This work was sup-
ported by grants from Canada Department of
Fisheries and Oceans and the Natural Sciences
and Engineering Research Council to Glen H.
Geen.
LITERATURE CITED
Biette, R. M., and G. H. Geen.
1980. Growth of underyearling sockeye salmon (On-
corhynchus nerka) under constant and cyclic tempera-
tures in relation to live zooplankton ration size. Can. J.
Fish. Aquat. Sci. 37:203-210.
Brett, j. r.
1979. Environmental factors and growth. In W. S. Hoar,
D. J. Randall, and J. R. Brett (editors), Fish physiology,
Vol. 8, p. 599-675. Acad. Press, N.Y.
BROTHERS, E. B.
1978. Exogenous factors and the formation of daily and
subdaily g^rowth increments in fish otoliths. Am. Zool.
18:631.
BROTHERS, E. B., C. R Mathews, and R. Lasker.
1976. Daily growth increments in otoliths from larval and
adult fishes. Fish. Bull., U.S. 74:1-8.
Campana, S. E.
1983. Factors affecting the production of daily growth in-
crements in the otoliths of fishes. Ph.D. Thesis, Univ.
British Columbia, Vancouver, B.C., 146 p.
Campana, S. E., and J. D. Neilson.
1982. Daily growth increments in otoliths of starry floun-
der (Platichthys stellatus ) and the influence of some en-
vironmental variables in their production. Can. J. Fish.
Aquat. Sci. 39:937-942.
Degens, E. T, w. g. deuser, and R. L. HAEDRICH.
1969. Molecular structure and composition of fish oto-
liths. Mar. Biol. (Berl.) 2:105-113.
English, k. k.
1981. Growth and feeding of juvenile chinook salmon, On-
corhynchus tshaivytscha , in in situ enclosures. M.S.
Thesis, Univ. British Columbia, Vancouver, B.C., 86 p.
Marshall, S. L., and S. S. Parker.
1982. Pattern identification in the microstructure of sock-
eye salmon (Oncorhynchus nerka ) otoliths. Can. J. Fish.
Aquat. Sci. 39:542-547.
Matty, a. J.
1978. Pineal and some pituitary hormone rhythms in
fish. In J. E. Thorpe (editor). Rhythmic activity of fishes,
p. 21-30. Acad. Press, N.Y.
Menaker, m., and S. BINKLEY.
1981. Neural and endocrine control of circadian rhythms in
the vertebrates. In J. Aschoff (editor). Handbook of be-
havioral neurobiology, p. 234-256. Plenum Press, N.Y.
MUGIYA, Y, N. WATABE, J. YAMADA, J. M. DEAN, D. G. DUN-
kelberger, and M. SHIMUZU.
1981. Diurnal rhythm in otolith formation in the goldfish,
Carassius auratus. Comp. Biochem. Physiol. 68A:659-
662.
NEILSON, J. D., AND G. H. GEEN.
1981. Method for preparing otoliths for microstructure
examination. Prog. Fish-Cult. 43:90-91.
NEILSON and GEEN: CHINOOK SALMON OTOLITH INCREMENT FORMATION
1982. Otoliths of chinook salmon (Oncorhynchus
tshawytscha): daily growth increments and factors in-
fluencing their production. Can. J. Fish. Aquat. Sci.
39:1340-1347.
PALOHEIMO, J. E., AND L. M. DICKIE.
1966. Food and growth of fishes. II. Effects of food and
temperature on the relation between metabolism and
body weight. J. Fish. Res. Board Can. 23:869-908.
Pannella, G.
1971. Fish otoliths: daily growth layers and periodical pat-
terns. Science (Wash., D.C.) 173:1124-1127.
SIMKISS, K.
1974. Calcium metabolism of fish in relation to age-
ing. In T. B. Bagenal (editor), Ageing of fish, p.
1-12. Unwin Bros., Ltd., Old Woking Surrey
Taubert, B. d., and D. W Coble.
1977. Daily rings in otoliths of three species of Lepomis
and Tilapia mossambica. J. Fish. Res. Board Can.
34:332-340.
Wilson, k. h., and p a. larkin.
1982. Relationship between thickness of daily growth in-
crements in sagittae and change in body weight of sockeye
salmon (Oncorhynchus nerka) fry. Can. J. Fish. Aquat.
Sci. 39:1335-1339.
101
INFORMATION FOR CONTRIBUTORS TO THE FISHERY BULLETIN
Manuscripts submitted to the Fishery Bulletin will reach print faster if they conform to the following instructions.
These are not absolute requirements, of course, but desiderata.
CONTENT OF MANUSCRIPT
The title page should give only the title of the paper,
the author's name, his affiliation, and mailing address,
including ZIP code.
The abstract should not exceed one double-spaced
page.
In the text, Fishery Bulletin style, for the most part,
follows that of the U.S. Government Printing Office
Style Manual. Fish names follow the style of the Amer-
ican Fisheries Society Special Publication No. 12, A
List of Common and Scientific Names of Fishes from the
United States and Canada, Fourth Edition, 1980.
Text footnotes should be typed separately from the
text.
Figures and tables, with their legends and headings,
should be self-explanatory, not requiring reference to
the text. Their placement should be indicated in the
right-hand margin of the manuscript.
Preferably figures should be reduced by photography
to 5% inches (for single-column figures, allowing for
50% reduction in printing), or to 12 inches (four double-
column figures). The maximum height, for either width,
is 14 inches. Photographs should be printed on high
quality or glossy paper.
Do not send original drawings to the Scientific Editor;
if they, rather than the photographic reductions, are
needed by the printer, the Scientific Publications Office
will request them.
Each table should start on a separate page. Consis-
tency in headings and format is desirable. Vertical
rules should be avoided, as they make the tables more
expensive to print. Footnotes in tables should be num-
bered sequentially in arable numerals. To avoid confu-
sion with powers, they should be placed to the left of
numerals.
Acknowledgments, if included, are placed at the
end of the text.
Literature is cited in the text as: Lynn and Reid
(1968) or (Lynn and Reid 1968). All papers referred to
in the text should be listed alphabetically by the senior
author's surname under the heading "Literature Cited."
Only the author's surname and initials are required in
the literature cited. The accuracy of the literature
cited is the responsibility of the author. Abbreviations
of names of periodicals and serials should conform to
Serial Sources for the BIOSIS Data Base. (Chemical
Abstracts also uses this system, which was developed
by the American Standards Association.)
Common abbreviations and symbols, such as
mm, m, g, ml, mg, °C (for Celsius), %,7«, , and so forth,
should be used. Abbreviate units of measure only when
used with numerals. Periods are only rarely used with
abbreviations.
We prefer that measurements be given in met-
ric units; other equivalent units may be given in
parentheses.
FORM OF THE MANUSCRIPT
The original of the manuscript should be tjqjed,
double-spaced, on white bond paper. Please triple space
above headings. We would rather receive good dupli-
cated copies of manuscripts than carbon copies. The
sequence of the material should be
TITLE PAGE
ABSTRACT
TEXT
LITERATURE CITED
TEXT FOOTNOTES
APPENDIX
TABLES (Each table should be numbered with an
arable numeral and heading provided)
LIST OF FIGURES (Entire figure legends)
FIGURES (Each figure should be numbered with
an arable numeral; legends are desired)
ADDITIONAL INFORMATION
Send the ribbon copy and two duplicated or carbon
copies of the manuscript to:
Dr. William J. Richards, Scientific Editor
Fishery Bulletin
Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service, NOAA
75 Virginia Beach Drive
Miami, FL 33149-1099
Fifty separates will be supplied to an author free of
charge and 50 supplied to his organization. No covers
will be supplied.
• GPO 693-007
OF,
Fishery Bulletin
Vol. 83, No. 2 April 1985
BOEHLERT, GEORGE W. Using objective criteria and multiple regression
models for age determination in fishes 103
HUNTER, J. ROE, and BEVERLY J. MACEWICZ. Rates of atresia in the ovary of
captive and wild northern anchovy, Engraulis mordax 119
LO, NANCY C. H. Egg production of the central stock of northern anchovy,
Engraulis mordax, 1951-82 137
MULLIN, M. M., E. R. BROOKS, R M. H. REID, J. NAPP, and E. E STEWART. Ver-
tical structure of nearshore plankton off southern California: a storm and a larval
fish food web 151
DEMARTINI, EDWARD E., LARRY G. ALLEN, ROBERT K. FOUNTAIN, and
DALE ROBERTS. Diel and depth variations in the sex-specific abundance, size
composition, and food habits of queenfish, Seriphus politus (Sciaenidae) 171
HEWITT, ROGER R Reaction of dolphins to a survey vessel: effects on census
data 187
CROSS, JEFFREY N. Fin erosion among fishes collected near a southern Cali-
fornia municipal wastewater outfall (1971-82) 195
DEC 6 1985
Woods Ho!e, Um\
Notice
NOAA Technical Reports NMFS published during last 6 months of 1984
V
Seattle, Washington
U.S. DEPARTMENT OF COMMERCE
Malcolm Baldrige, Secretary
NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION
John V. Byrne, Administrator
NATIONAL MARINE FISHERIES SERVICE
William G. Gordon, Assistant Administrator
Fishery Bulletin
The Fishery Bulletin carries original research reports and technical notes on investigations in fishery science, engineering, and
economics. The Bulletin of the United States Fish Commission was begun in 1881; it became the Bulletin of the Bureau of Fisheries
in 1904 and the Fishery Bulletin of the Fish and Wildlife Service in 1941. Separates were issued as documents through volume 46; the
last document was No. 1103. Beginning with volume 47 in 1931 and continuing through volume 62 in 1963, each separate appeared as
a numbered bulletin. A new system began in 1963 with volume 63 in which papers are bound together in a single issue of the bulletin
instead of being issued individually. Beginning with volume 70, number 1, January 1972, the Fishery Bulletin became a periodical,
issued quarterly. In this form, it is available by subscription from the Superintendent of Documents, U.S. Government Printing
Office, Washington, DC 20402. It is also available free in limited numbers to libraries, research institutions. State and Federal
agencies, and in exchange for other scientific publications.
SCIENTIFIC EDITOR, Fishery Bulletin
Dr. William J. Richards
Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service, NOAA
Miami, FL 33149-1099
Editorial Committee
Dr. Bruce B. Collette Dr. Donald C. Malins
National Marine Fisheries Service National Marine Fisheries Service
Dr. Edward D. Houde Dr. Jerome J. Pella
Chesapeake Biological Laboratory National Marine Fisheries Service
Dr. Merton C. Ingham Dr. Jay C. Quast
National Marine Fisheries Service National Marine Fisheries Service
Dr. Reuben Lasker Dr. Carl J. Sindermann
National Marine Fisheries Service National Marine Fisheries Service
Mary S. Fukuyama, Managing Editor
The Fishery Bulletin (ISSN 0090-06561 is published quarterly by the Scientific Publications Office, National Marine Fisheries
Service, NOAA, 7600 Sand Point Way NE, BIN C1570O, Seattle, WA 98115. Second class postage is paid at Seattle, Wash., and
additional offices. POSTMASTER send address changes for subscriptions to Superintendent of Documents, U.S. Government
Printing Office, Washington, DC 20402.
Although the contents have not been copyrighted and may be reprinted entirely, reference to source is appreciated.
The Secretary of Commerce has determined that the publication of this periodical is necessary in the transaction of the public
business required by law of this Department. Use of funds for printing of this periodical has been approved by the Director of the
Office of Management and Budget through 1 April 1985.
Fishery Bulletin
CONTENTS
Vol. 83, No. 2 April 1985
BOEHLERT, GEORGE W. Using objective criteria and multiple regression
models for age determination in fishes 103
HUNTER, J. ROE, and BEVERLY J. MACEWICZ. Rates of atresia in the ovary of
captive and wild northern anchovy, Engraulis mordax 119
LO, NANCY C. H. Egg production of the central stock of northern anchovy,
Engraulis mordax, 1951-82 137
MULLIN, M. M., E. R. BROOKS, F M. H. REID, J. NAPP, and E. R STEWART. Ver-
tical structure of nearshore plankton off southern California: a storm and a larval
fish food web 151
DEMARTINI, EDWARD E., LARRY G. ALLEN, ROBERT K. FOUNTAIN, and
DALE ROBERTS. Diel and depth variations in the sex-specific abundance, size
composition, and food habits of queenfish, Seriphus politus (Sciaenidae) 171
HEWITT, ROGER P Reaction of dolphins to a survey vessel: effects on census
data 187
CROSS, JEFFREY N. Fin erosion among fishes collected near a southern Cali-
fornia municipal wastewater outfall (1971-82) 195
Notice
NOAA Technical Reports NMFS published during last 6 months of 1984
L5 T^ ;r>, .': c-j
DEC 6 1985
Woods Hole, Mass.
Seattle, Washington
1985
I
For sale by the Superintendent of Documents, U.S. Government Printing Office, Washing-
ton DC 20402 — Subscription price per year: $21.00 domestic and $26.25 foreign. Cost per
single issue: $7.00 domestic and $8.75 foreign.
The National Marine Fisheries Service (NMFS) does not approve, recommend or
endorse any proprietary product or proprietary material mentioned in this pub-
lication. No reference shall be made to NMFS, or to this publication furnished by
NMFS, in any advertising or sales promotion which would indicate or imply that
NMFS approves, recommends or endorses any proprietary product or proprietary
material mentioned herein, or which has as its purpose an intent to cause directly
or indirectly the advertised product to be used or purchased because of this NMFS
publication.
USING OBJECTIVE CRITERIA AND MULTIPLE REGRESSION MODELS
FOR AGE DETERMINATION IN FISHES
George W. Boehlert^
ABSTRACT
Analysis of the age structure of exploited fish papulations is necessary for models upon which manage-
ment decisions are made, but existing aging methodology for many species is hindered by subjective
criteria used in age determination. A new technique is described in which age is estimated using
multiple regression models based upon the measurable parameters otolith weight, otolith length, and
otolith width in the splitnose rockfish, Sebastes diploproa , and the canary rockfish, S. pinniger. Models
were calibrated using ages determined by interpretation of both whole otoliths and otolith sections
which differ within these species, particularly at greater lengths. The models typically explained from
70 to 92% of the variability in age depending upon species, sex, and method of age analysis. In another
sample used to verify the precision of the models, variability associated with model-estimated ages was
generally less than that induced by variability in ages between different agencies. Based upon the
pattern of otolith growth in length, width, and weight in these and other species, it is suggested that
these methods would be applicable to a wide variety of fishes. Implementation of this type of age
determination methodology could result in savings in time and cost for fisheries management agencies
while decreasing variability among age estimates between different laboratories.
Virtually all methods of age determination in
fishes involve a certain degree of subjectivity. De-
ciding whether a mark on an otolith or scale con-
stitutes 1 year's growth is difficult; precision in fish
aging improves only with experience. Even so, var-
iability between experienced readers may be
great. Sandeman (1969), for example, observed
only 9% agreement between readers for a wide age
range of otoliths of Sebastes marinus and S. men-
tella, and noted greater variability with increas-
ing age of the fish. Kimura et al. (1979) suggested
that bias between readers within a given agency is
likely to be much less than among different agen-
cies. In a situation such as exists on the Pacific
coast, where several management agencies may
routinely determine ages for the same species,
interagency calibrations are necessary but are
rarely achieved. Williams and Bedford (1974)
suggested ". . . that otolith reading remains, for the
present at least, as much an art as a science, and
that proficiency cannot easily be achieved without
examination of very large numbers of otoliths."
Clearly, objective, repeatable age determination
methodology which will minimize variability is
desirable.
Traditional methodology for age determination
^Oregon State University, College of Oceanography, Marine
Science Center, Newport, Oreg.; present address: Southwest
Fisheries Center Honolulu Laboratory, National Marine
Fisheries Service, NOAA, PO. Box 3830, Honolulu, HI 96812.
in fishes generally involves some calcified struc-
ture; in Sebastes, Six and Horton (1977) tested 25
different structures. By far the most commonly
used structures, however, are the otolith and
scales. Scales are often best for short-lived, fast-
growing species because annuli become indistinct
near the margin in long-lived, slower growing
species (Power 1978; Maraldo and MacCrimmon
1979). When this is the case, the otolith becomes
the superior structure for age determination; even
in the otolith, however, annuli may become indis-
tinct on the margin as otoliths thicken and become
opaque with age. For this reason several inves-
tigators have used broken or sectioned otoliths to
determine age from internal banding patterns.
While some studies using otolith sections have
provided clear continuation of growth patterns
obvious on whole otoliths from younger specimens,
others have suggested maximum ages which are
double or triple those estimated from whole
otoliths. Power (1978), for example, suggested ages
of >50 yr in Salvelinus namaycush and Coregonus
clupeaformis and provided confirming evidence
based upon population structure. In the redfish,
Sebastes marinus, Sandeman (1961) suggested
that specimens exceeding 50 yr of age were pres-
ent in the population; ages up to 80 yr have since
been estimated (Sandeman^). Similarly, Beamish
Manuscript accepted April 1984
FISHERY BULLETIN; VOL. 83, NO. 2, 1985.
^E. J. Sandeman, Biological Station, St. John's, Newfound-
land, Canada, pers. commun. July 1978.
103
(1979b) estimated ages approaching 90 yr in cer-
tain Pacific species of Sebastes, including S.
alutus. In the genus Sebastes, these estimates of
extended longevity have recently been confirmed
by Bennett et al. (1982), who used geochronologi-
cal methods to confirm age in S. diploproa. Under-
standing population structure for such long-lived
species will require a large number of age esti-
mates using otolith sections. Routine sectioning
and interpretation of otoliths, however, is a time-
consuming process, and age structure would need
to be determined frequently for management of an
active fishery. In this paper I suggest a possible
alternative method for age determination.
Otolith growth begins with the initial "focus"
and thereafter by incremental concretions of cal-
cium carbonate in the form of aragonite. Otolith
size increases with increasing size and age of the
fish. Differential addition of crystalline material
to the otolith, however, results in a species-specific
shape (Bingel 1981). In flatfish and certain other
species, Williams and Bedford (1974) observed con-
tinued linear growth of the otolith with growth of
the fish only until maximum size was achieved;
beyond this time, the otolith began to thicken.
This has been observed in several other species
(Blacker 1974a). Linear measurements of the
otolith (i.e., length and width) are directly related
to fish length and show little variability, but
otolith thickness and weight are highly variable
in larger fish (Templeman and Squire 1956;
Beamish 1979a, b).
Templeman and Squire (1956) observed that
length and width of otoliths from slow- and fast-
growing populations of haddock did not differ at
the same fish length, whereas otolith weight was
consistently greater in the slower growing (and
therefore older) populations at a given length. The
same trend appears to exist in some members of
the genus Sebates (G. W. Boehlert unpubl. data).
Beamish (1979a) observed an increase in thick-
ness of the hake otolith with increasing otolith
section age and a nearly linear relationship of
otolith thickness and otolith weight. If otolith
thickness, and therefore weight, is a function of
fish age, then if fish length (or otolith length, since
the two are related) is known, one should be able to
estimate fish age. This was suggested by Brander
(1974) with Irish Sea cod. The objective of this
study is to determine the trends of otolith growth
in terms of thickness, length, width, and weight,
and to determine the potential of these criteria for
estimation of age in splitnose rockfish, S. diplop-
roa, and canary rockfish, S. pinniger.
FISHERY BULLETIN: VOL. 83, NO. 2
MATERIALS AND METHODS
Otolith Collection
Otoliths of S. pinniger and S. diploproa were
collected during the 1980 West Coast Survey con-
ducted by the Northwest and Alaska Fisheries
Center on the FV Pat San Marie and the FV Mary
Lou. Gear and sampling strategy were similar to
that described in Gunderson and Sample (1980).
Otoliths were collected from fish captured in all
hauls until desired numbers of specimens in
specified length categories were obtained. Both
otoliths from each specimen were removed,
cleaned, and stored in individual, labeled vials
containing 50% ethanol. Data taken with each
specimen included vessel, haul (with latitude, lon-
gitude, and bottom depth), sex, and fork length
(to the nearest 0.1 cm). After returning to the
laboratory, otoliths were thoroughly cleaned and
the preservative renewed.
Age Determination
General information on otolith morphology and
whole otolith aging methodology in Sebastes is
described in detail by Kimura et al. (1979). Age
determined from whole otoliths followed the aging
methodology of Boehlert (1980) for S. diploproa
and that of Six and Horton (1977) for S. pinniger.
Ages determined in this manner are referred to as
whole otolith ages.
Otolith sections were prepared for selected
specimens using the left otolith after the
methodology of Nichy^ with several modifications.
Specimens were affixed to heavy-duty cardboard
tags with double-faced tape and embedded in
polyester casting resin in preparation for section-
ing. Specimens were mounted in a chuck specifi-
cally designed to accommodate the cardboard tags
and fed onto a pair of thin diamond blades sepa-
rated by acetate spacers on a Buehler** low-speed
Isomet saw. Dorsal-ventral sections through the
focus and perpendicular to the sulcus, about 0.4
mm thick, were removed from the center of the
otolith. Sections were removed from the tag and
attached to labeled microscope slides with his-
tological mounting medium. They were sub-
sequently ground to eliminate surface artifacts,
'F. Nichy, Northeast Fisheries Center Woods Hole Laboratory,
National Marine Fisheries Service, NOAA, Woods Hole, MA
02543.
■* Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
104
BOEHLERT: AGE DETERMINATION IN FISHES
first with 400-grit carborundum paper and then
polished with 3 ^im jeweler's rouge.
To compare internal otolith section annuli with
surface annuli, 25 whole left otoliths from S. pin-
niger and 50 from S. diploproa were selected.
Sample size was chosen to represent the range of
ages estimated from whole otoliths. I determined
the distance from focus to each annulus on the
whole otolith along the dorsal- ventral axis from
focus to dorsal edge of the otolith using an ocular
micrometer on a dissecting microscope. These
measurements were used to identify the first sev-
eral annuli on corresponding sections. By follow-
ing these identified annuli around to the internal
dorsal surface it was determined that each small
ring in the direction of counting (from focus to
dorsal, interior surface) corresponded to a single
year of growth (Fig. 1).
Sections were initially examined under a dis-
secting microscope at 30 x magnification with
either reflected light and a black background or
transmitted light, depending upon the clarity of
the annuli. Discerning and counting the narrow
zones in otoliths from older fish was facilitated by
the use of a compound microscope interfaced with
a video camera and television screen. A more ac-
curate estimate of age was made possible by the
increased magnification and enhanced contrast of
the compound microscope, coupled with the ease of
viewing annuli on an enlarged screen.
Sections were aged by identifying the first
translucent annulus (winter growth zone) and
counting sequential growth zones from the center
to the dorsal edge. Subsequent annuli were fol-
lowed from the dorsal edge to the interior dorsal
quadrant (after Beamish 1979b), and counted to
the internal surface. In this paper, ages deter-
mined by different methods and sources will be
discussed; none of these ages is known with cer-
tainty. For this reason, given ages will be defined
as "standard ages" only for purposes of compari-
son.
Calibration Subsample
To establish models of age based upon otolith
dimension and weight criteria, otoliths from the
entire collection were subsampled. Every fourth
otolith pair of S. diploproa and every third of S.
pinniger were selected to provide roughly equal
sample sizes representative of all sizes and collec-
tion (latitudinal) areas. These subsampled
otoliths were used to develop the multiple regres-
sion models (see section on Data Analysis) and
were treated as described below.
Whole otolith ages were determined by an ex-
perienced otolith reader to whom fish length re-
mained unknown. This practice has been recom-
mended by Williams and Bedford (1974), among
others, to minimize bias in otolith reading.
Otoliths were then dried to a constant weight at
58°C and placed in a dessicator for 8 h. Intact left
otoliths were weighed to the nearest milligram.
Otoliths were measured with dial calipers in the
anteroposterior dimension (length) to the nearest
0.02 mm and in the maximum dorsoventral di-
FlGURE 1. — Dorsal-ventral section of the left otolith of a 305 mm FL female Sebastes diploproa. Whole otolith ages are generally
determined from the focus (F) to the dorsal edge (A), but often extend to the posterior margin (not shown) which may include additional
annuli extending to greater ages (A to B). Section ages are determined from the focus (F) to the internal dorsal surface (C). Note the
additional growth zones on axis F-C which have been deposited after the latest visible zones on axis F-A. The otolith section age of this
specimen is 40 yr.
105
FISHERY BULLETIN; VOL. 83, NO. 2
mension (width) to the nearest 0.05 mm. When the
left otolith was chipped or broken, the right one
was substituted for measurements, since no sys-
tematic differences between left and right otolith
measurements were apparent for either species.
The left otolith was subsequently sectioned and
age determined by the same otolith reader. Otolith
thickness, which is too variable to measure on the
whole otolith, was measured on the section from
internal to external surface just dorsal to the sul-
cus (Fig. 1).
Confirmation Subsample
In order to test the precision of the model, sub-
samples of 50 otoliths by sex and species were
drawn randomly from samples not used in the
calibration subsample. These samples were han-
dled in the following way: A second whole otolith
age was determined by reader A to determine
within-reader variability for S. diploproa and
between-reader variability for S. pinniger (reader
B had left this laboratory). The otoliths were sent
to the Northwest and Alaska Fisheries Center
(Seattle, Wash. ) for an additional whole otolith age
to determine between-agency variability. The
otolith was dried, weighed, measured, and sec-
tioned as described above; a single otolith section
age for each specimen was determined by reader A
for both species. Model-estimated ages were de-
termined by use of the multiple regression models
described below.
Data Analysis
Generally, data were recorded in a standard
format and stored on the Oregon State University
Cyber 70 computer. Data management and analy-
sis were assisted by use of the Statistical Package
for the Social Sciences (SPSS) (Nie et al. 1975).
From the calibration subsample of otoliths, pre-
dictive regression equations were developed to es-
timate age from otolith morphometries. Multiple
regression models were fitted in the following
form:
Age = 6iXi -I- 62^2 + 63X3 -I- b^X^ + c
where age (years) is determined by conventional
methods, bn's = regression coefficients, X 's = in-
dependent variables, and c = constant. Models
were developed for males and females separately
within each species with both otolith section ages
and whole otolith ages as dependent variables.
Independent variables included otolith weight,
otolith length, otolith width, the respective square
and cubic terms of each, and the interaction vari-
ables (otolith weight/otolith length and otolith
length/otolith width). With the exception of
otolith weight, where both weight and the cube of
weight were used as independent variables,
square or cubic terms were not used if the raw
values were entered. This decreased problems of
multicollinearity. Models were fitted in a forward
stepwise manner (Nie et al. 1975) with the inclu-
sion level for independent variables set at
P = 0.10.
The 1980 confirmation subsample was used to
verify the models. Direct comparisons between
ages determined for the same otoliths but dif-
ferent reading methods were accomplished by
paired ^-tests. Since age is not known with cer-
tainty for any otolith, the ages determined by
reader A for S. diploproa and by reader B for S.
pinniger, which were used to calibrate the models
in the calibration subsample, were considered as
"standard age". To conduct multiple comparisons
of variability, deviations from standard age were
defined as follows: "model-induced variation" is
the difference between the standard age and the
model-predicted age; "within-agency variation" is
the difference between ages determined by reader
A for S. diploproa and between readers A and B for
S. pinniger; "between-agency variation" is the dif-
ference between the standard age and the age de-
termined by the National Marine Fisheries Ser-
vice (NMFS). A one-way analysis of variance
(ANOVA) was used to compare these deviations.
Multiple range testing was conducted using the
least significance difference method with
a = 0.05. This analysis was conducted only for
whole otoliths since only a single section age was
determined on the 1980 confirmation subsample.
RESULTS
Sehastes diploproa
Locations of the collections of S. diploproa are
shown in Figure 2; this species was taken from lat.
36°49' to 48°47'N and over a depth range of 62 to
338 m. The distribution was similar to that noted
in 1977 (Boehlert 1980). A total of 975 male and
1,145 female specimens were taken during the
survey. The length frequencies show a mode near
23 cm for males and 24 cm for females with sec-
ondary modes at 26 and 27 cm, respectively. Cor-
responding age frequencies (based upon whole
106
BOEHLERT: AGE DETERMINATION IN FISHES
otoliths) show a clear mode at 7 yr for both males
and females, with whole otolith age ranges from 1
to 46 for males and 0 to 55 for females. Mean
lengths-at-age for males and females are similar
until age 8, after which females grow more rapidly
(Boehlert 1980; Boehlert and Kappenman 1980).
Subsampling every fourth pair of otoliths from
all collections of S. diploproa resulted in 290
female and 246 male specimens. The subsample
was representative of the latitudinal distribution,
age range, and length range of the whole collec-
tion. Capture, otolith, and age data from these
samples are summarized in Table 1. Otolith sec-
tion ages, as expected, were typically greater than
whole otolith ages (Table 1); this was particularly
true at greater lengths. Correlation matrices of
pertinent otolith and age data (Table 2) show that
otolith weight has the strongest linear association
with otolith section age; both otolith weight and
age are exponential functions offish length. Plot-
ting otolith length, fish length, and otolith weight
against otolith section age demonstrates the pat-
tern of otolith growth (Fig. 3). Past an age of about
25 yr, both otolith length and fork length reach
approximate asymptotes, whereas otolith weight
continues to increase. The wide fluctuations in
otolith weight apparent at older ages correlate
closely with changes in fork length (Fig. 3 ); for this
reason, otolith weight alone is a relatively poor
predictor of fish age at greater ages where fork
length is highly variable. Addition of otolith
FIGURE 2. — Locations of 1980 West Coast Survey collections
from which otoliths of Sebastes diploproa were taken.
10 20 30 40 50 60 70
OTOLITH SECTION AGE (YEARS)
Figure 3. — Otolith characteristics of male Sebastes diploproa
from the calibration subsample as related to fish length and
age. A'' = 246. Note the covariation among the three curves,
particularly at older ages.
Table l. — Summary of biological and otolith data from the subsampled groups of Sebastes diploproa
used in developing the age models.
Females (N = 290)
Males (W = 246)
Variable
Minimum Maximum Mean
SD
Minimum Maximum
Mean
SD
Depth of capture (fathoms) 34 185 137 29.36 53 185 136 28.45
Fork length (mm) 130 378 264 56.16 94 364 246 48.19
Otolith length (mm) 7.71 18.02 12.49 2.35 5.47 17.03 11.82 2.14
Otolith width (mm) 5.08 11.25 7.97 1.31 3.59 10.32 7.57 1.14
Otolith thickness (mm) 0.83 2.97 1.41 0.44 0.73 2.84 1.35 0.39
Otolith dry weight (mg) 59 724 244.6 150.4 25 659 208 117.4
Whole otolith age (yr) 1 56 15.2 11.97 1 40 13.5 9.78
Otolith section age (yr) 2 66 17.2 15.68 1 74 16.9 16.41
107
FISHERY BULLETIN: VOL. 83, NO. 2
Table 2. — Correlation matrix for selected otolith morphometric, weight, and age data
for the calibration subsample of Sebastes diploproa.
Whole
Ofclith
Otolith
Otolith
Otolith
Otolith
otolith
section
weight
length
width
thickness
age
age
Females (A/ = 290)
Fork length
0.912
0.969
0.956
0.766
0.862
0.819
Otolith section age
0.947
0.859
0.788
0.938
0.917
Whole otolith age
0.925
0.893
0.837
0.901
Otolith thickness
0.930
0.843
0.778
Otolith width
0.893
0.948
Otolith length
0.940
Males (W =246)
Fork length
0.895
0.971
0.959
0.815
0.835
0.769
Otolith section age
0.938
0.807
0.710
0.905
0.907
Whole otolith age
0.923
0.885
0.778
0.846
Otolith thickness
0.903
0.778
0.725
Otolith width
0.857
0.778
Otolith length
0.922
length and the interaction variables compensate
for these changes in the pattern of otolith weight
in the multiple regression models offish age.
The multiple regression models relating fish age
with otolith data were fitted with both whole
otolith age and otolith section age as dependent
variables. Independent variables included in the
whole otolith age models, their coefficients, and
significance levels are presented in Table 3. All
coefficients were highly significant and the models
explain 88.1% of the variation in age for females
and 92.0% for males, as measured by the coeffi-
cient of determination, R"^. Residuals from the
models by age category show no trend up to age 35
for females and age 30 for males, after which there
is a trend of increasing positive deviation with
increasing age. The ages included in this part of
the model, however, represented only 7.7% of
female and 8.6% of male S. diploproa and are
therefore not of great concern. These deviations
are positive, however, suggesting that the model
predictions may relate to otolith growth patterns
which are more indicative of otolith section ages.
Variables included in the otolith section age
models, their coefficients, standard errors, and
significance levels are presented in Table 4. Again,
all coefficients are highly significant, but the co-
efficients of determination are slightly less, ex-
plaining 86.1% of the variation in age for females
and 85.0% for males. Mean residuals for the dif-
ferent age categories show no significant trend
with age.
The model based upon whole otolith ages suffers
from inaccuracies in the older ages, where otolith
section ages are much greater than whole otolith
ages. This is demonstrated in the trend of increas-
ing residuals with increasing age. The model
based upon otolith section age, however, is charac-
108
Table 3. — Regression coefficients and associated statistics on
the multiple regression models of whole otolith age for Sebastes
diploproa .
Variable
Coefficient
SE
P
Females (N = 290)
Otolith weight
0.1343
0.0091
<0.001
(Otolith weight)^
-0.107 X 10-6
0.14 X 10"'
<0.001
Otolith width
-2.558
0.571
<0.001
Constant (a)
6.4303
3.004
0.033
SD = 4.15
Multiple correlation, R
= 0.939
Males (W = 246)
Otolith weight
0.2179
0.0145
<0.001
(Otolith weight) 3
-0.1945 X 10-6
0.14 X 10-'
<0.001
Otolith width
-3.4542
0.3942
<0.001
Otolith weight/length
-1.0997
0.2402
<0.001
Constant (a)
16.2572
2.2186
<0.001
SD = 2.797
Multiple correlation, R
= 0.959
Table 4. — Regression coefficients and associated statis-
tics on the multiple regression models of otolith section
age for Sebastes diploproa .
Variable
Coefficient
SE
Females (A/ = 290)
Otolith weight
(Otolith width) 2
(Otolith weight)^
(Otolith length)^
Constant (a)
SD = 4.232
Multiple correlation, R
Males (W = 246)
Otolith weight
Otolith width^
(Otolith weight)^
(Otolith length)^
Constant (a)
SD = 4.620
Multiple correlation, R
0.2270
-0.3288
-0.1134 X 10-'
-0.1114
5.0243
= 0.928
0.2496
-5.7233
-0.1315 X 10-'
-0.0882
23.540
0.922
0.0137
0.0377
0.155 X 10-
0.0205
1 .2982
00158
0.6949
0.266 X 10-
0.0256
3.3823
<0.001
<0.001
<0.001
<0.001
<0.001
0.001
0.001
0.001
0.001
<0.001
terized by slightly lower multiple correlation co-
efficients (Table 4). This may be a result of inac-
curacies in estimates of otolith section age of
younger fish, where greater difficulty in age de-
BOEHLERT: AGE DETERMINATION IN FISHES
termination exists with sections. For this reason, I
also constructed a hybrid multiple regression
model based upon a combination of otolith section
and whole otolith ages. The decision on which age
to use was arbitrary in the following way: If the
difference (otolith section age minus whole otolith
age) was "^ 5 yr, whole otolith age was chosen; if the
difference was >5 yr, otolith section age was cho-
sen. The resulting models are described in Table 5.
Independent variables similar to those in the
other two models were chosen, and the multiple
correlation coefficients were greater in each case.
To analyze the precision of the models, subsam-
ples of 50 male and 50 female S. diploproa were
taken from the remaining samples not used in the
calibration subsample. Lengths and ages were
representative of the respective ranges in the
overall collection. Ranges of whole otolith age,
NMFS age (that from the other agency), and
otolith section age in these samples were 2-50,
3-49, and 2-75 for females and 3-34, 4-25, and 3-84
for males, respectively.
Whole otolith age was predicted based upon the
appropriate whole otolith age models. Values of
estimated age, whole otolith age, and NMFS age
as a function of length are plotted in Figure 4. The
deviation of NMFS age from whole otolith age
increases with increasing length for both males
and females. Deviations from the first whole
otolith age are presented in Figure 5. Model-
induced variability is the difference between es-
timated whole otolith age and whole otolith age;
between-agency variability is whole otolith age
minus NMFS age; within-agency variability is the
difference of two successive age determinations by
Table 5. — Regression coefficients and associated statis-
tics on the multiple regression models of age in Sebastes
diploproa . The ages used for the calibration of these mod-
els are based upon either whole otoliths or otolith sec-
tions as described in the text.
Variable
Coefficient
SE
Females (A/ = 290)
Otolith weight 0.2233
(Otolith width) 2 -0.2983
(Otolith weight)^ -0.1244 x 10"
Otohth length -2,495
Constant (a) 17.7993
SD = 4.3967
Multiple correlation, R = 0.962
Males {N = 246)
Otolith weight 0.2504
(Otolith width)2 -0.3598
(Otolith weight) 3 -0.1272 x IQ-
Otolith length -2.4123
Constant (a) 16.6069
SD = 4.7479
Multiple correlation, R = 0.958
0.0135
0.0403
0,1685 X 10-
0.5084
3,7339
0,0157
0,0549
0-2800 . 10-'
0,6071
3,9145
0001
0,001
;0.001
-0.001
0,001
; 0.001
0,001
0,001
;0.001
tO.001
the same reader Mean values of these sources of
variation are presented in Table 6 for females and
Table 7 for males. In both cases, the mean
between-agency variability is greater than either
model-induced or within-agency variability.
One-way ANOVA demonstrates a significant dif-
ference among the three sources (Tables 6, 7). Mul-
tiple range testing (least significant difference,
a = 0.05), moreover, demonstrates that the means
are significantly different for both females and
males; the range tests suggest that within-agency
and model-induced variability are equal and are
both significantly less than the between-agency
variability.
Only a single otolith section age was determined
for specimens from the 1980 confirmation subsam-
ple. Ages were estimated from the multiple re-
gression model of section age (Table 4) and com-
pared with conventionally determined section age
35rT
14 16 18 20 22 24 26 28 30 32 34 36 38 40
FORK LENGTH (cm)
FIGURE 4. — Comparisons of mean whole otolith ages at length
for the confirmation subsample of Sebastes diploproa . Trian-
gles represent age from reader A, circles the age estimated by the
model, and squares the age determined by another laboratory.
109
FISHERY BULLETIN: VOL. 83, NO. 2
Table 6. — Results of one-way analysis of variance and multiple
range tests comparing deviations of age from the standard age in
Sebastes diploproa females. Group 1 = between-agency variabil-
ity; group 2 = model-induced variability: group 3 = within-
agency, within reader variability.
Source
df
Sum of
squares
Mean
squares
Analysis of variance
Table 7. — Results of one-way analysis of variance and multiple
range tests comparing deviations of age from the standard age in
Sebastes diploproa males. Group 1 = between-agency variabil-
ity; group 2 = model-induced variability; group 3 = within-
agency, within reader variability.
Source
df
Sum of
squares
IVIean
squares
Analysis of
variance
Between
groups
2
207.30
103.65
Within groups
147
1,118.30
7.61
Total
149
1.325,60
Group
n
Mean
SD
1
50
2.360
3.306
2
50
0.108
2 294
3
50
-0320
2.575
13.62 <0.001
Multiple range lest (least significant difference, a = 0.05)
Group 3 ^ Group 2 ■ Group 1
(Fig. 6). Ages were close to those predicted from
the model with the notable exception of the
maximum age for both males and females. In each
instance, the maximum ages were greater than
the maximum otolith section age in the calibra-
tion subsample; the estimated section age is there-
fore an extrapolation from the model. For the
overall subsample, however, the estimated section
ages were not significantly different from those
determined by conventional methods (paired
^test, a = 0.05). The observed and predicted ages
comparing the confirmation subsample with the
predicted ages from the hybrid model are not pre-
sented graphically, but the form of the curves for
both males and females is virtually identical to
that for the section age model (Fig. 6).
Sebastes p/tjurger
Sebastes pinniger were collected from lat. 43°ir
to 49°26'N at depths from 58 to 375 m (Fig. 7).
110
to
<
Between groups
Within groups
Total
2
147
149
707,77
2.247.93
2.955.70
353.89
15.29
23.14
•0.001
o
>
UJ
Group
n
Mean
SD
1
2
3
50
50
50
4.000
-0.51
-0.700
4.686
4.134
2.613
Multiple range test (least significant
Group 3 = Group 2 - Group 1
difference, «
= 0.05)
MALES
12 14 16 18 20 22
WHOLE OTOLITH AGE (YEARS)
Figure 5. — Mean deviations of whole otolith ages from the
confirmation subsample of Sebastes diploproa. Triangles rep-
resent model-induced variability, circles within-agency variabil-
ity, and squares between-agency variability.
Pairs of otoliths from a total of 519 male and 369
female specimens were taken from the survey.
Length frequencies for S. pinniger show a mode at
50 cm for males and 52 cm for females. Age fre-
quencies of the entire sample (based upon whole
otoliths) demonstrate a mode for both males and
females at 12 to 13 yr Whole otolith ages from the
collections ranged from 2 to 25 for males and 2 to
22 for females.
Subsampling every third pair of otoliths from
the whole collection resulted in 171 male and 121
female specimens of S. pinniger. Again, this sub-
sample was representative of the latitudinal dis-
tribution, age range, and length range of the
whole sample. Capture, otolith, and age data from
these specimens are summarized in Table 8.
Otolith section ages in larger fish are generally
greater than whole otolith ages, but not to the
BOEHLERT: AGE DETERMINATION IN FISHES
90
80
70-
— 60
(/>
<
uj 50
<0 40
<
z
< 30
20-
10
T I I
MALES
' T I I
1
-
-
J
\\
-
_
I
\
_
-
/
9
-
-
A'
-
1 1 1
1
1 1 1
1
-
14 16 18 20 22 24 26 28 30 32 34 36 38 40
FORK LENGTH (cm)
Figure 6. — Comparisons of mean otolith section ages at length
from the confirmation subsample of Sebastes diploproa.
Triangles represent otolith section age and circles the model
estimated section age.
Figure 7. — Locations of 1980 West Coast Survey collections
from which otoliths of Sebastes pinniger were taken for the
current study. Samples from the FV Pat San Marie and the FV
Mary Lou are included.
Table 8. — Summary of biological and otolith data from the subsampled groups of Sebastes pinniger
used in developing the age models.
Females (A/ = 121)
Males (N = 171)
Variable
Minimum Maximum Mean
SD
Minimum Maximum
Mean
SD
Depth of capture (fathoms) 32 100 69.8 12.66 37 103 73.3 14.39
Fork length (mm) 152 610 497.8 69.25 170 579 481.64 64.20
Otolith length (mm) 8.00 23.40 19.62 2.27 8.59 22.89 19.56 2.31
Otolith width (mm) 4.45 12.02 9.60 1.06 4.69 11.07 9.46 1.01
Otolith thickness (mm) 0.83 2.01 1.54 0.19 0.79 2.41 1.64 0.29
Otolith dry weight (mg) 53 821 486.7 135.5 58 867 517.0 160.69
Whole otolith age (yr) 2 19 12.4 3.16 2 25 13.2 3.79
Otolith section age (yr) 2 33 14.83 5.09 2 54 20.02 9.77
extent seen for S. diploproa. Otolith weight is
again an exponential function of length, particu-
larly for males. For females, however, this rela-
tionship was nearly linear. Of the ages determined
in the calibration subsample, otolith weight has
the strongest linear association with whole otolith
age for females and whole otolith age and section
age for males (Table 9).
The multiple regression models constructed to
predict whole otolith age were based upon fewer
variables than for S. diploproa , but included vari-
ables were highly significant (Table 10). The coeffi-
111
FISHERY BULLETIN: VOL. 83. NO. 2
Table 9. — Correlation matrix for selected otolith morphometric, weight, and age data
for the calibration subsample of Sebastes pinniger.
Whole
Otolith
Otolith
Otolith
Otolith
Otolith
otolith
section
weight
length
width
thickness
age
age
Females (W = 121)
Fork length
0.915
0.948
0.923
0.779
0.895
0.755
Otolith section age
0.825
0.735
0.757
0.718
0.795
Whole otolith age
0.890
0.887
0.851
0.756
Otolith thickness
0.826
0.765
0.756
Otolith width
0.920
0.902
Otolith length
0.917
Males (W = 171)
Fork length
0.844
0.940
0.909
0.754
0.847
0 682
Otolith section age
0 898
0.694
0.696
0.883
0,809
Whole otolith age
0.892
0.837
0.815
0.830
Otolith thickness
0.910
0 769
0.750
Otolith width
0.869
0.901
Otolith length
0.879
Table 10. — Regression coefficients and associated
statistics on the multiple regression models of whole
otolith age for Sebastes pinniger.
Variable Coefficient
SE
P
Females (N = 121)
(Otolith length)^ 0.00095
(Otolith width)2 0.0448
0.00011
0.0126
■0.001
0.001
SD = 1.30
Multiple correlation. R = 0 913
Males (W = 171)
Otolith weight 0.0280
(Otolith weight)^ -0.845 x lO-«
0.00214
0.241 X 10-8
<0.001
0.001
SD = 1.665
Multiple correlation, R = 0,900
cient of determination (R ) suggests that the mod-
els of whole otolith age explain 83.4% of the varia-
tion in age for females and 81.0% for males. For
both males and females, the constant in the re-
gression was not significantly different from zero
and was not included in the models. The residuals
from the models show no distinct trend with the
exception of a slight increase at ages >17 yr for
males; this included 11.1% of the sample.
The variables included in the otolith section age
models, their coefficients, standard errors, and
significance levels are presented in Table 11. As in
the whole otolith age models, there are fewer vari-
ables included than for S. diploproa; for the male
section age model, for example, there is only one
variable and the constant included for prediction
of age. All variables are highly significant and the
coefficients of determination suggest that the
otolith section models explain 70.2% of the varia-
tion in age for females and 84.6% for males. Mean
residuals show a strong trend of increase at ages
past 26 yr for male otolith section age models; this
represented 23% of the sample.
A model incorporating both otolith section age
and whole otolith age was developed using the
same criteria for age as in S. diploproa. These
models were based upon more independent vari-
ables but were not significantly better (as based
upon the coefficient of determination) than the
otolith section models (Table 12). Based upon the
multiple correlation coefficients, the best models
for S. pinniger would be the hybrid model for
males and the whole otolith model for females.
For analyzing the precision of the models, sub-
Table 11. — Regression coefficients and associated
statistics on the multiple regression models of otolith
section age for Sebastes pinniger.
Variable Coefficient
SE
P
Females (N = 121)
(Otolith weight)^ 0.272x10-'
0.382 X 10-5
<0.001
Otolith width 0.8368
0.4586
0.071
SD = 2.80
Multiple correlation, R = 0.838
Males (A/ =171)
(Otolith weight)^ 0.546x10-"
0.179 X 10-5
< 0.001
Constant (a) 4.0297
0.6022
• 0.001
SD = 3.85
Multiple correlation, R = 0.920
Table 12. — Regression coefficients and associated statistics on
the multiple regression models of age in Sebastes pinniger. The
ages used for the calibration of these models are based upon
either whole otoliths or otolith sections as described in the text.
Variable
Coefficient
SE
P
Females (N = 121)
(Otolith weight)^
0.2621 X 10-"
0.4518 X 10-5
0.001
(Otolith width) 3
0.4038 X 10-2
0.2186 X 10-2
0.067
Constant (a )
3.2137
1.1296
0.005
SD = 2.8239
Multiple correlation, R
= 0.840
Males (W = 171)
(Otolith weight)^
0.1306 X 10-3
0.2359 X 10-"
<0.001
(Otolith length)^
-0.2044 X 10-2
0.5456 X 10-3
<0.001
(Otolith weight) 3
-0.6026 X 10-'
0.2197 X 10-'
0.007
Otolith length/width
9.7349
4.1381
0.020
Constant (a )
-12.8239
7.4064
0.085
SD = 3.9989
Multiple correlation, R =
0.924
112
BOEHLERT: AGE DETERMINATION IN FISHES
samples of 50 male and 50 female S. pinniger were
taken from the remaining 1980 samples not used
in the calibration subsample. These subsamples
were representative of the length and age ranges
in the overall collection. Ranges of whole otolith
age, NMFS age, and otolith section age in these
subsamples were 4-26, 4-25, and 4-29 for females
and 7-35, 7-32, and 8-45 for males, respectively.
Whole otolith age was estimated from the ap-
propriate whole otolith age model for males and
females. Values of model estimated age, whole
otolith age, and NMFS age as a function of length
are plotted in Figure 8. Female S. pinniger ages
are similar for all three age determination
methods. For males, model-estimated age is simi-
lar to the whole otolith age but both are less than
the NMFS age (Fig. 8). Deviations from the whole
otolith age by the otolith reader whose ages were
used to calibrate the model are shown in Figure 9.
26
24
22
20
18
16
14
12
10
8
6-
D— Q
MALES
10
8
6
4
«
a:
<
2
Ul
>-
0
7
o
1-
-2
<
■>
III
-4
o
V)
<
UJ
-6
-8
-lOf-
"I 1 1 1 1 r
MALES
9 °
>
Q -2
-3
-4
-5
6 8 10 12
1 1 1 1 r
FEMALES
16 18 20 22 24
1 1 ' r
ntxv.
■A ^/
J \ L
_L
_!_
J_
6 8 10 12 14 16 18 20 22 24
WHOLE OTOLITH AGE (YEARS)
Figure 9. — Mean deviations of whole otolith ages from the
confirmation subsample oi Sebastes pinniger. Triangles repre-
sent model-induced variability, circles within-agency variabil-
ity, and squares between-agency variability.
0
22
J I I I I I
J I L
36 38 40 42 44 46 48 50 52 54 56
in
<
UJ
>
UJ
<
z
<
UJ
S
oL
T r
25 30 35 40 45 50
FORK LENGTH (cm)
55
J
60
Figure 8. — Comparisons of mean whole otolith ages at length
from the confirmation subsample of Sehastes pinniger. Trian-
gles represent age from reader B, circles the age estimated by the
model, squares the age determined by another laboratory.
The explanation of these deviations is the same as
for S. diploproa with the exception that the within-
agency variability is a between-reader rather than a
within-reader variability. One-way ANOVA within
these deviations shows significant differences among
the groups for both females (Table 13) and males
(Table 14). Multiple range testing (least significant
difference, a = 0.05) demonstrates that for females,
mean between-agency variability and model-induced
variability are equal but are both less than within-
agency variability (for S. pinniger this was based
upon two different readers). For males, between-
agency variability is less than model-induced vari-
ability which is less than within-agency variability.
For the purposes of this comparison, however, the
model-induced variability is significantly closer to
zero than either of the other sources of variability
(Table 14).
In the confirmation subsample, section ages
estimated from the multiple regression model are
113
FISHERY BULLETIN: VOL. 83, NO. 2
Table 13. — Results of one-wa.v analysis of variance and multi-
ple range tests comparing deviations of age from the standard
age in Sebastes pinnlger females. Group 1 = between-agency
variability; group 2 = model-induced variability; group
3 = within-agency, between reader variability.
Source
df
Sum of
squares
Mean
squares
Analysis of vanance
Between groups 2 88.69
Within groups 147 751.84
Total 149 840 53
Group n Mean SD
44.34
5.11
8.67
0,001
50
50
50
-0.320
-0.021
1.44
2.817
1.516
2 260
Multiple range test (least significant difference, a = 0.05)
Group 1 = Group 2 Group 3
Table 14. — Results of one-way analysis of variance and multi-
ple range tests comparing deviations of age from the standard
age in Sebastes pinniger males. Group 1 = between-agency var-
iability; group 2 = model-induced variability; group
3 = within-agency, between reader variability.
Source
df
Sum of
squares
Mean
squares F
Analysis of
variance
Between
groups
2
1,840.42
920.21
Witfiin groups
147
2.006.21
13.65
Total
149
3.846.63
Group
n
Mean
SD
1
50
-4.280
4.427
2
50
-0 111
2 107
3
50
4 300
4 112
67.43 -0.001
Multiple range test (least significant difference, a = 0.05)
Group 1 Group 2 • Group 3
compared with conventional section ages in Fig-
ure 10. The two ages are similar and as a whole are
not significantly different for females but are sig-
nificantly different for males (paired ^-test,
a = 0.05). This is presumably a result of the con-
sistently overestimated otolith section age for S.
pinniger males. The ages estimated from the hy-
brid model (Fig. 11) are not significantly different
from those determined by the appropriate conven-
tional age (paired /-test, a = 0.05).
DISCUSSION
The results of this research demonstrate the
potential for using objective criteria and mul-
tivariate models to determine age in fast- and
slow-growing members of the genus Sebastes . Past
studies have used weight of the eye lens for esti-
mates of age in fishes, amphibians, and certain
mammals (Crivelli 1980; Malcolm and Brooks
1981). In fishes, however, this technique is only
114
good for fast-growing species and provides poor
estimates of age after several years when length at
age becomes highly variable (Crivelli 1980); the
same problems exist in estimating age from modal
lengths. Growi;h of most body parts, including the
eye lens, is allometric with length rather than age.
Growth of the otolith, however, as described above,
is a complex function of age as well as length. After
a certain size is reached, the fish otolith does not
increase in length or width, but continues to in-
crease in thickness, and therefore weight, with
age (Fig. 3). The increasing thickness is a function
of addition of aragonite crystals only on the inter-
nal surface of the otolith (Fig. 1).
Similar patterns of otolith growth in length,
width, thickness, and weight have been observed
1 1 ;
1
I
1 i 1
1
1
32
MALES
A
-
28
A
A
jj
^^^?
v>
jp
rr
Cfi^
<f
24
-
Q J '
-
UJ
l\ 1 '
>-
/ \ 1 1
tij
<•>
20
m
<
z
<
/ ''
UJ
16
~
0/
-
z
•^,
/ ■
12
L
^
"
B
7
•
38 40 42 44 46 48 50 52 54 56
30
35 40 45
FORK LENGTH (cm)
50
55
60
Figure lO. — Comparisons of mean otol ith section ages at length
from the confirmation subsample of Sebastes pinniger. Trian-
gles represent otolith section age and circles the model esti-
mated section age.
BOEHLERT: AGE DETERMINATION IN FISHES
in other species offish, but the information has not
been applied to the estimation of age, with the
exception of preliminary tests using discriminant
techniques by Brander (1974). Templeman and
Squire (1956), however, noted the importance of
this information: "In many fishes, in which accu-
rate age reading is doubtful, otolith weights,
which are more factual, may offer a better separa-
tion of fish populations than growth rates which
are dependent on the judgement of the scale- or
otolith-reader." Weight and otolith measurements
are valid criteria for age determination based
upon the models (Tables 3-5, 10-12) and provide
good estimates of age compared with other reading
methods (Tables 6, 7, 13, 14; Figs. 4-6, 8-11). Based
upon published patterns of otolith growth, these
techniques should work for other species of
Sebastes (Sandeman 1961; Beamish 1979b), Pacific
hake (Beamish 1979a), haddock (Templeman and
Squire 1956), plaice, sole, turbot, and horse
mackerel (Blacker 1974a), and cod (Trout 1954;
Blacker 1974a), among others. This technique
may therefore be amenable to a wide variety of
species of fishes.
Ages determined by scale or otolith readers are
generally based on subjective decisions by the age
reader, who reads annuli but must distinguish
from "false checks", "metamorphic checks", and
"spawning checks" (Trout 1961; Bailey et al. 1977).
FORK LENGTH (cm)
Figure ll. — Comparison of ages determined from otoliths and
those predicted by the hybrid regression model for Sebastes pin-
niger males. Otolith ages were based upon whole otolith ages if
the difference between section and whole otolith ages were s5;
otherwise, otolith sections were used. Triangles represent
whole otolith or section age and squares the model estimated age.
With experience comes reduced individual vari-
ability, but aging variability among different
otolith readers and especially among different
agencies is great; such variability can have impor-
tant effects upon the estimates of growth
parameters important for fisheries management
(Sandeman 1961; Brander 1974; Hirschhorn 1974;
Kimura et al. 1979). While otolith or scale ex-
changes are occasionally made between agencies
for calibration purposes, this represents addi-
tional time spent for gaining greater consistency
in ages (Westrheim and Harling 1973; Blacker
1974b), and difficulties may remain if disagree-
ment in aging techniques cannot be resolved.
Blacker (1974a) noted that "Recent progress in the
use of otoliths for age determination has been lim-
ited mainly to the development of new techniques
for preparing otoliths for reading and for photog-
raphy so that aging methods can be readily com-
pared." The techniques described in the present
study represent a new approach to the systematic
and repeated age determination in species for
which continued age determination is necessary;
once calibrated and implemented, the models
would reduce between-reader and between-agency
variability in age determination. Further re-
search, however, should be conducted on varia-
tions in thg models over seasons, regions, and dif-
ferent years to determine to what extent repeated
calibration is necessary.
Ancillary benefits of the proposed methodology
include its simplicity. Reliable, repeatable esti-
mates of age require a great deal of experience on
the part of an otolith or scale reader using conven-
tional aging methodology (Blacker 1974a). It is
often difficult to maintain a staff of trained otolith
readers and retraining may require a large time
commitment. The techniques described here re-
quire no special training, since the criteria (otolith
length, otolith width, and otolith dry weight) are
objective and can be measured with simple dial
calipers and balance. Time expended for age de-
termination by different methods is as follows: An
experienced otolith reader averages about 17
ages/h on whole otoliths, but only 6 to 8 ages/h
when otolith sections are used due to the addi-
tional preparation necessary. An untrained tech-
nician, however, can determine the measurements
necessary for the model-based age estimates at a
rate of about 40 otoliths/h on a long-term basis.
Since the criteria for age are measurable, the
techniques will be amenable to automation. Sev-
eral attempts have been made in the past to auto-
mate or semiautomate age analysis using imaging
115
FISHERY BULLETIN: VOL. 83, NO. 2
systems based upon differential light transmis-
sion (Fawell 1974; Mason 1974). These techniques
have generally not been implemented, however,
due to the subjective and variable nature of the
criteria. Implementation of these techniques with
automated systems could result in even further
savings of time.
Since estimating the age distribution of
exploited fish populations remains an important
part of fishery biology, new and improved
techniques of age determination are desirable. For
shorter lived species, length-based methods are
proving important (Pauly and David 1981). Age-
length keys are also used quite extensively. Sam-
ple sizes necessary for accurate age-length keys,
however, must be quite large, particularly for
long-lived species such as Sebastes. In my rela-
tively small calibration subsamples, for example,
there are up to 15 age classes in a single 1 cm
length interval (Table 15). Considering the
Table 15. — Number of age classes within single 1 cm length
intervals from the calibration subsample. A'^ = number of
Sebastes specimens in the subsample.
Whole
Otolith
otolith
section
Species
Sex
N
age
age
S diploproa
Female
290
14
14
Male
246
12
14
S. pinniger
Female
121
6
11
Male
171
9
15
maximum age of S. diploproa (Bennett et al. 1982),
there could potentially be up to 50 age classes in a
single length interval if a sufficient sample size
were taken. For such species, age-length keys will
be difficult to extrapolate meaningfully to the en-
tire population without very large sample sizes,
which must accordingly be aged. Similar, but more
severe, problems will apply to techniques which
attempt to extract growth parameters from
length-frequency data for such long-lived species.
The techniques developed by Pauly and David
(1981) for faster growing species would be com-
plemented by the current technique for slow-
growing, difficult-to-age species. Otoliths could be
collected by station, sex, and species without re-
gard, to size. From each otolith, after calibration of
an age model, the available information could in-
clude both fish length and age. This approach to
length data collection is not new and has been used
by the International Pacific Halibut Commission
for several years to estimate length (Southward
1962; Quinn et al. 1983). These techniques could
therefore streamline not only the collection of
otoliths at sea but also the analysis of age in the
laboratory.
The difficulty in age determination described
above and the resulting variability between
laboratories may have a negative impact upon ac-
curacy of fishery models, particularly those using
cohort or virtual population analysis (Brander
1974; Alverson and Carney 1975). The new
methodology can provide significant time and cost
savings over conventional methods and also de-
crease variability in age estimates. Implementa-
tion of these aging techniques, however, will re-
quire careful calibration with ages determined by
a consensus of expert otolith readers from all
management agencies with an interest in each
species for which a model is developed.
ACKNOWLEDGMENTS
This research was supported by Cooperative
Agreement No. 80-ABH-00049 from the North-
west and Alaska Fisheries Center, National
Marine Fisheries Service, NOAA, Seattle, Wash. I
thank Tom Dark, Mark Wilkins, and other partic-
ipants in the 1980 West Coast Survey for assis-
tance in specimen collection; particular thanks
are extended to Captains Bernie and Tom Hansen
of the FV Pat San Marie and MV Mary Lou, re-
spectively, and their capable crews. Technical as-
sistance and otolith reading were provided by
Mary Yoklavich, Dena Gadomski, and Robert
McClure. I thank Jack Lalanne for providing the
NMFS age estimates. Finally I thank W H.
Lenarz and D. R. Gunderson for critically review-
ing the manuscript.
LITERATURE CITED
Alverson, D. L., and M. J. Carney.
1975. A graphic review of the growth and decay of popula-
tion cohorts. J. Cons. Int. Explor. Mer 36:133-143.
BAILEY, R. F. J., K. W. ABLE, AND W. C. LEGGETT.
1977. Evidence for the presence of a metamorphic check in
capelin {Mallotus villosus) otoliths and implications for
age determination. J. Fish. Res. Board Can. 34:2008-
2014.
BEAMISH, R. J.
1979a. Differences in the age of Pacific hake (Merluccius
productus) using whole otoliths and sections of
otoliths. J. Fish. Res. Board Can. 36:141-151.
1979b. New information on the longevity of the Pacific
ocean perch (Sebastes alutus). J. Fish. Res. Board Can.
36:1395-1400.
BENNETT, J. T, G. W. BOEHLERT, AND K. K. TUREKIAN.
1982. Confirmation of longevity in Sebastes diploproa
(Pisces: Scorpaenidae) using ^"*Pb/"*Ra measurements in
otoliths. Mar. Biol. (Berl.) 71:209-215.
116
BOEHLERT: AGE DETERMINATION IN FISHES
BINGEL, F.
1981. Growth of a cod otolith on the crystal level. Meeres-
forschung 28:212-215.
BLACKER, R. W.
1974a. Recent advances in otolith studies. In F. R. Har-
den Jones (editor), Sea fisheries research, p. 67-90. John
Wiley and Sons, N.Y.
1974b. The ICNAF cod otolith photograph exchange
scheme. In T. B. Bagenal (editor). The ageing of fish, p.
108-113. Unwin Brothers, Ltd., Surrey
BOEHLERT, G. W.
1980. Size composition, age composition, and growth of the
canary rockfish, Sebastes pinniger, and the splitnose
rockfish, S. diploproa, from the 1977 Rockfish survey
Mar. Fish. Rev. 42(3-4):57-63.
BOEHLERT, G. W, AND R. F KAPPENMAN.
1980. Variation of growth with latitude in two species of
rockfish {Sebastes pinniger and S. diploproa) from the
northeast Pacific Ocean. Mar. Ecol. Prog. Ser. 3:1-10.
BRANDER, K.
1974. The effects of age-reading errors on the statistical
reliability of marine fishery modelling. In T. B. Bagenal
(editor), The ageing of fish, p. 181-191. Unwin Brothers,
Ltd., Surrey.
Crivelli, a.
1980. The eye lens weight and age in the common carp,
Cyprinus carpio L. J. Fish Biol. 16:469-473.
Fawell, J. K.
1974. The use of image analysis in the ageing of fish. InT.
B. Bagenal (editor), The ageing offish, p. 103-107. Unwin
Brothers, Ltd., Surrey.
GUNDERSON, D. R., AND T. M. SAMPLE.
1980. Distribution and abundance of rockfish off Washing-
ton, Oregon, and California during 1977. Mar. Fish. Rev.
42(3-4):2-16.
HIRSCHHORN, G.
1974. The effect of different age ranges on estimated Ber-
talanffy growth parameters in three fishes and one mol-
lusk of the northeastern Pacific Ocean. In T. B. Bagenal
(editor), The ageing of fish, p. 192-199. Unwdn Brothers,
Ltd., Surrey.
KIMURA, D. K., R. R. MANDAPAT, AND S. L. OXFORD.
1979. Method, validity, and variability in the age determi-
nation of yellowtail rockfish (Sebastes flavidus), using
otoliths. J. Fish. Res. Board Can. 36:377-383.
Malcolm, J. R. and R. J. Brooks.
1981. Eye lens weight and body size as criteria of age in
beaver {Castor canadensis). Can. J. Zool. 59:1189-1192.
Maraldo, D. C, and H. R. MACCRIMMON.
1979. Comparison of ageing methods and growth rates for
largemouth bass, Micropterus salmoides Lacepede, from
northern latitudes. Environ. Biol. Fish. 4:263-271.
Mason, J. E.
1974 . A semi-automatic machine for counting and measur-
ing circuli on fish scale. In T. B. Bagenal (editor). The
ageing offish, p. 87-102. Unwin Brothers, Ltd., Surrey.
NIE, N. H., C. H. HULL, J. G. JENKINS, K. STEINBRENNER, AND
D. H. BENT.
1975. Statistical package for the social sciences. 2d
ed. McGraw-Hill, N.Y, 675 p.
Pauly, D., and N. David.
1981. ELEFAN 1, a basic program for the objective extrac-
tion of growth parameters from length frequency
data. Meeresforschung 28:205-211.
POWER, G.
1978. Fish population structure in Arctic lakes. J. Fish.
Res. Board Can. 35:53-59.
Quinn, T J., n, E. A. Best, L. Bijsterveld, and L R.
McGregor.
1983. Sampling Pacific halibut {Hippoglossus stenolepis)
landings for age composition: History, evaluation, and
estimation. Int. Pac. Halibut Comm. Sci. Rep. 68, 56 p.
Sandeman, E. J.
1961. A contribution to the problem of age determination
and growth-rate in Sebastes. Rapp. P-V Reun. Cons.
Perm. Int. Explor. Mer 150:276-284.
1969. Age determination and growth rate in redfish,
Sebastes sp., from selected areas around Newfound-
land. Int. Comm. Northwest Atl. Fish. Res. Bull. 6:79-
106.
Six, L. D., and H. F Horton.
1977. Analysis of age determination methods for yellow-
tail rockfish, canary rockfish, and black rockfish off Ore-
gon. Fish. Bull., U.S. 75:405-414.
SOUTHWARD, G. M.
1962. A method of calculating body lengths from otolith
measurements for Pacific halibut and its application to
portFock-albatross grounds data between 1935 and
1957. J. Fish. Res. Board Can. 19:339-362.
Templeman, W, and H. J. Squire.
1956. Relationship of otolith lengths and weights in the
haddock Melanogrammus aeglefinis (L.) to the rate of
growth of the fish. J. Fish. Res. Board Can. 13:467-487.
TROUT, G. C.
1954. Otolith growth of the Bamets Sea cod. Rapp. R-V.
Reun. Cons. Perm. Int. Explor. Mer 136:89-102.
1961. The otolith of group-O Sebastes mentella Tra-
vin. Rapp. P-V. Reun. Cons. Perm. Int. Explor. Mer
150:297-299.
WESTRHEIM, S. J., AND W R. HARLING.
1973 . Report on the 1972 comparison of Pacific ocean perch
otolith and scale interpretations. Fish. Res. Board Can.
Manuscr. Rep. Ser. 1259, 24 p.
Williams, T, and B. C. Bedford.
1974. The use of otoliths for age determination. In T. B.
Bagenal (editor), The ageing offish, p. 114-123. Unwin
Brothers, Ltd., Surrey.
117
RATES OF ATRESIA IN THE OVARY OF CAPTIVE AND WILD
NORTHERN ANCHOVY, ENGRAULIS MORDAX
J. Roe Hunter and Beverly J. Macewicz '
ABSTRACT
The process of ovarian atresia was described for northern anchovy using a laboratory group in which
atresia was induced by starvation. Atretic characteristics of the ovary were described and illustrated,
atretic ovarian states defined, and the rate that the ovary passed from one atretic stage to another was
measured. The ovaries of starved females regressed rapidly; 3 days after the onset of starvation the
ovaries of about half of the females contained yolked oocytes undergoing resorption of yolk (alpha stage
of oocyte atresia) and by 23 days after the onset of starvation no yolk remained in the ovaries of any of
the females. Gamma+delta stages of atretic follicles persisted in the ovary for over a month, but their
decline in abundance indicated that eventually all signs of past reproductive activity would be lost in
regressed ovaries.
In the natural population, rates of ovarian atresia increased seasonally from only a few percent of the
females showing some atresia in peak spawning months to over 50% near the end of the season.
Females with low levels of alpha stage atresia (<50% yolked oocytes affected) spawned about half as
frequently as did those with no alpha stage atresia. Spavraing was rare (1% of the females) or absent in
females with high levels of alpha stage atresia (>50% yolked oocytes affected). Late in the spawning
season, it may be possible to forecast the end of spawning in the populations using the frequency of
females in the populations with high levels of alpha stage oocyte atresia. Throughout the spawning
season atretic rates were higher in small females (standard length <10 cm) than in larger ones
indicating that 1-year-old females spawning for the first time have a much shorter spawning season
than do older females.
Four approaches commonly used to determine the
reproductive state of female fishes are 1) staging
of ovaries using gross anatomical criteria such as
the international Hjort scale (Bowers and Holli-
day 1961); 2) calculation of the gonosomatic index
(GSI), i.e., gonad weight divided by female weight
or the equivalent (de Vlaming et al. 1982); 3) es-
timating the mean diameter of the oocytes in the
most advanced mode of oocytes (Hunter and
Goldberg 1980; Hunter and Leong 1981); and 4)
classifying ovaries histologically. Histological
classification is superior to all other methods. Two
of its great strengths are that the frequency of
spawning of multiple spawning fish populations
can be accurately estimated using the presence of
postovulatory follicles (Hunter and Goldberg
1980) and that regressing ovaries can be distin-
guished from immature and from postovulatory
ovaries. The histological criteria used to identify
regressing ovaries is the presence of many oocytes
and follicles undergoing resorption, a process
known as atresia.
'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038.
Manuscript accepted April 1984.
FISHERY BULLETIN: VOL. 83, NO. 2, 1985.
The interpretive power of histological analysis
could be enhanced if the process of ovarian atresia
were better documented. Specifically, ovarian
atretic stages need to be defined, rates of atresia
and duration of stages estimated, and the relation
between ovarian atretic state and the probability
of spawning determined. Such information would
facilitate process oriented field studies on re-
productive biology, and increase the accuracy of
estimates of size at first maturity and size- or
age-specific duration of the annual spawning sea-
son.
This study provides the laboratory and field
calibration necessary for the assessment of the
reproductive state of northern anchovy, Engraulis
mordax, using the atretic condition of the ovary.
We identify a range of ovarian atretic characteris-
tics that define the atretic condition of the ovary,
estimate rates of atresia, and estimate the dura-
tion that atretic characters persist in the ovaries of
starving females in the laboratory. We use this
information to classify ovaries of sea-caught
females and estimate the probability of spawn-
ing for females with various levels of ovarian atre-
sia.
We know of no similar work. A large descriptive
119
FISHERY BULLETIN: VOL. 83, NO. 2
literature exists on follicular atresia in fishes (re-
viewed by Saidapur 1978) and stages of atretic
oocytes and follicles have been defined
(Bretschneider and Duyvene de Wit 1947; Lambert
1970a), but only the atretic rates in the guppy have
been measured (Lambert 1970a). Considerable at-
tention has been devoted to stages of atretic folli-
cles (corpora atretica or "preovulatory corpora
lutea") because of a presumed endocrine function
(see reviews by Hoar 1965; Byskov 1978). The sea-
sonal occurrence of atretic oocytes and follicles is
often discussed as part of a general description of
seasonal changes in the ovary of marine fish; see,
for example, cycles described for the gobiid, Gil-
lichthys mirabilis (de Vlaming 1972); plaice,
Pleuronectes platessa (Barr 1963); Paracentropris-
tis cabrilla (Zanuy 1977); and three species of
Epinephelus (Bouain and Siau 1983). The propor-
tion of females with atretic ovaries or the numbers
of atretic oocytes within the ovary is given less
often, but a few reports exist. For example, atresia
ranged from 0 to 69c of the oocytes in female had-
dock, Melanogrammus aeglefinus (L.) (Robb
1982); corpora atretica increased to about 39c of the
oocytes during the postspawning period of the dab,
Limanda limanda (L.) (Htun-Han 1978); and atre-
tic oocytes varied from 13% of yolked oocytes dur-
ing the prespawning period to 100% during the
postspawning period of the snapper, Chrysophrys
auratus (F.) (Crossland 1977). Some attention has
been given to the issue of whether or not atretic
rates can account for differences in fecundity
among females fed high and low rations. It ap-
pears that ration-related differences in fecundity
are more closely tied to production rates of oocytes
rather than atretic rates (Tyler and Dunn 1976;
Wootton 1979). In summary, our literature review
indicates that ovarian atresia has yet to be used for
quantitative estimation of any reproductive pro-
cesses in marine fish populations, although it has
been used in general descriptions of the seasonal-
ity of reproduction for many years.
METHODS
Laboratory Experiment
Adult northern anchovy captured by commer-
cial bait fishermen on 23 February 1982 were kept
in a live car in San Diego Bay. Three days later
about 1,000 fish averaging 104 mm SL (9.50 g)
were taken to the laboratory and held in a 4.6 m
diameter pool (1 m deep ) at which time the first fish
sample was taken. Over the first 34 d in captivity,
120
samples of 18-24 females were taken at 3-4 d inter-
vals with the final sample taken after 62 d in
captivity. The temperature of the seawater ranged
from 15.5° to 16.5°C.
The fish were not fed during the first 27 d in
captivity because starvation was used to trigger
the resorption of the ovary; thereafter they were
fed daily. On the 27th day of starvation the ovaries
had regressed from A9c of female body weight to
0.8% and feeding was resumed because we wished
to learn how long the atretic characters would last
once the fish began to feed.
In our calculations of atretic rates of laboratory
females, we assumed that all the females at the
time of capture had active ovaries without atresia,
although no samples were taken until 3 d after the
fish were captured. Only 3% of the 1,680 females
taken in a survey conducted at the same time (28
January-8 March 1982) had atretic ovaries, and it
was prominent in only 0.1% of the females (50% or
more of yolked oocytes were affected). Ninety-six
percent of the females in our first sample (taken 3
d after capture) had yolked eggs, and half of them
had no atresia.
All females sampled during the course of the
laboratory experiment were weighed and mea-
sured, and the ovary removed, weighed, and a sec-
tion removed for histological analysis. Ovaries
were fixed in 10% neutral buffered Formalin^ and
embedded in Paraplast. Histological sections were
cut at 6 /um and stained with Harris hematoxylin
followed by eosin counterstain.
Sea Data
The ovaries of northern anchovy taken in trawl
surveys used for biomass estimation (Stauffer and
Picquelle^) and various other collections from
commercial seiners and midwater trawls were his-
tologically examined. The number of females
examined per catch (trawl, purse seine, or lam-
para net) has varied from 10 to 20. Some collec-
tions were quite small, especially those taken out-
side the main spawning season in the Southern
California Bight; these small collections may con-
sist of only two catches, whereas those taken dur-
ing the main spawning months (February-March)
^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
■■'Stauffer, G., and S. Picquelle. The 1980 and 1981 egg produc-
tion estimates of anchovy spawning biomass. Unpubl. manu-
scr. Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038.
HUNTER and MACEWICZ: ATRESIA IN NORTHERN ANCHOVY OVARY
were large, often consisting of 100 or more catches
of 10-20 females each. In all collections ovaries
were classed according to atretic characteristics as
well as on the basis of the presence of postovula-
tory follicles (age 0 and age 1 d) and hydrated eggs
according to the method described by Hunter and
Goldberg (1980). All but two of the collections were
from the Southern California Bight or northern
Baja California, the region where the Central
subpopulation of the northern anchovy is concen-
trated (Vrooman et al. 1981). Two collections were
from the vicinity of Monterey and San Francisco
Bays. Fish from these areas appear to have a dif-
ferent spawning season from those of fish to the
south so they are listed separately in our seasonal
tabulations. All collections were classified using
histological criteria to determine the incidence of
ovarian atretic states as a function of female size,
season, and reproductive state.
Histological Characteristics
We describe below the histological characteris-
tics of four oocyte classes and four stages of atresia
in the northern anchovy. These stages and classes
are subsequently used to define various ovarian
atretic states in laboratory and sea-caught female
anchovy.
Oocyte Classes
The northern anchovy is a multiple spawning
fish (Hunter and Goldberg 1980) with asynchro-
nous oocyte development (oocytes in many stages
of development occurring simultaneously in re-
productively active ovaries; Wallace and Selman
1981). During the spawning season oocyte devel-
opment is a continuous process involving all
stages with a new spawning batch maturing every
week to. 10 d (Hunter and Leong 1981). Oocyte
development and maturation in teleosts, reviewed
recently by Wallace and Selman (1981), has fre-
quently been subdivided into many stages (An-
drews 1931^ Yamamoto 1956; Lambert 1970b), but
our work required a simpler histological classifi-
cation system. We have combined the stages of
past authors into four oocyte classes (unyolked
oocytes, partially yolked oocytes, yolked oocytes,
and hydrated oocytes), and we describe the his-
tological characteristics of each class below.
"Andrews, C. B. 1931. The development of the ova of the
California sardine (Sardina caerulea). Unpubl. manuscr., 88
p. Stanford Univ., Stanford, CA 94305.
1) Unyolked Oocytes — This class includes all
oocytes without yolk that are about 0.04 mm or
larger and range upward in size to about 0.35 mm
(U, Fig. la, b). Oocytes <0.04 mm are excluded
because they consist mostly of "oogonium nests",
do not have a true follicle layer, and do not seem to
undergo degeneration (o, Fig. lb). The smaller
oocytes within this class (0.04-0.15 mm) are spher-
ical, have a large nucleus with a narrow homoge-
nous very densely staining cytoplasm (Fig. lb). A
very thin single layer of elongated, spindlelike
cells (the beginning of the granulosa layer) sur-
rounds these small oocytes. The large oocytes in
this class are oval, the C5rtoplasm stains faintly
with hematoxylin and has a cloudy, mottled ap-
pearance (Fig. Id). The oval nucleus of these oo-
cytes contains several nucleoli and is surrounded
by a granular perinuclear zone. In these larger
oocytes a thin, definite, faintly eosinophilic stain-
ing, hyaline membrane (precursor of the zona
radiata) appears between the oocyte and the grow-
ing follicle. The follicle consists of a narrow single
inner layer of cuboidal granulosa cells and a single
outer layer of flat elongated thecal cells with some
blood capillaries. The larger oocytes also may have
some small vesicles in the periphery of the cyto-
plasm. These vesicles are at times difficult to dis-
tinguish and they seem to disappear in yolked
oocytes. No oil vacuoles exist as northern anchovy
eggs do not contain oil droplets.
2) Partially Yolked Oocytes — Oocytes in this
class are in the early stages of yolk deposition
(vitellogenesis) and range in size from 0.3 to 0.5
mm (major axis) (P, Fig. Id, g). The class includes
oocytes in the initial stage of yolk deposition up to
and including those in which yolk granules or
spherules extend three-fourths of the distance
from the periphery to the perinuclear zone. Yolk
deposition starts at the periphery of the oocyte
cytoplasm as small eosinophilic staining granules
and then subsequently spreads internally until
they nearly reach the finely granular perinuclear
zone. Usually by this time the granules have be-
come small spherules. The oval-shaped nucleus of
oocytes in this class contains several nucleoli.
Delicate striations appear on the hyaline mem-
brane between the oocyte and follicle layer at the
time yolk appears in the oocyte. As maturation
proceeds, the follicle layer becomes wider due to an
increase in the width and proliferation of
granulosa cells. The thecal cells do not increase in
size but remain elongated, flat cells with occa-
sional blood capillaries and form a thin outer cov-
121
FISHERY BULLETIN; VOL. 83, NO. 2
Figure l. — Development of northern anchovy ovary at various magnifications (stain = H & E, bar = 0.1 mm), a) Immature ovary
consisting of unyolked oocytes and no atresia, b i Enlargement of (a I showing small spherical unyolked oocytes (U) with a large central
nucleus and "oogonium nests" (o). c) Normal mature ovary with many fully yolked oocytes (Y). d) All stages of oocytes: unyolked (U),
partial yolked (Pi, and yolked (Y), are present in normal mature ovaries, (g = granulosa cell layer, z = zona radiata, n = nucleus, y =
yolked globules.) e) Prespawning ovary showing migration of nucleus to the animal pole, f) Enlargement of a migratory nucleus
oocyte (M). (n = nucleus, y = yolk globules.) g) Imminent (• 12 h) spawning ovary with hydrated oocytes (H) still within the follicle
layer (U = unyolked, P = partial yolked. ) h ) Enlargement of a hydrated oocyte. Note that the yolk globules have fused into yolk plates
(yp) and there is no prominent nucleus due to disintegration of the nuclear membrane.
122
HUNTER and MACEWICZ: ATRESIA IN NORTHERN ANCHOVY OVARY
ering to the follicle. The thecal cells do not change
until hydration when they become even flatter and
have a stringy appearance.
3) Yolked Oocytes — Oocytes in this class range
from 0.45 to 0.80 mm (major axis), and all contain
yolk spherules or globules throughout the region
between the periphery of the oocyte and the
perinuclear zone (Y, Fig. Ic, d). As vitellogenesis
continues, the yolk varies from spherules in the
smaller oocytes to large globules in the larger
ones. Just prior to spawning (<24 h) the globules
fuse to form yolk plates (Fig. Ih). Such oocytes are
excluded from this oocyte class, this characteristic
being diagnostic of the last class (hydrated oo-
cytes). The nucleus of oocytes in the yolked oocyte
class is oval with numerous nucleoli. The
granulosa cells have a wide rectangular shape in
cross section and a large oval nucleus; their walls
are clearly evident in sagittal section where they
form polyhedrons. The zona radiata is a wide,
striated, eosinophilic band until hydration when it
stretches thin and the striations disappear.
4) Hydrated Oocytes — These oocytes range in
size from 0.75 to 1.2 mm (major axis) (H, Fig. Ig, h).
Hydration (rapid uptake of fluid by the follicle,
Fulton 1898) begins when the nucleus has mi-
grated to the animal pole (M, Fig. le, f) and yolk
globules first fuse to form yolk plates, and it ends
when the hydrated oocyte is ovulated. The nucleus
of hydrated oocytes is not visible except in the
earliest phase because after the nucleus migrates,
the nuclear membrane disintegrates dispersing
its contents into the cytoplasm. During hydration
all yolk globules fuse into plates and the oocyte
expands greatly, stretching the granulosa and
thecal cell layers. At this time, the granulosa cells
in cross section appear as long, thin rectangles, the
thecal cells are extremely flat and have a
stringlike appearance, and the zona radiata is
very thin and lacks striations. Hydrated oocytes
are the most ephemeral of all oocyte classes since
this stage lasts for less than a day, whereas the
other stages are always present in reproductively
active anchovy ovaries. Migratory nuclei may be
seen as early as 24 h before ovulation, but hy-
drated oocytes in which all globulues are fused to
form yolk plates do not occur earlier than 12 h
before spawning. We have never observed atre-
sia in hydrated oocytes; apparently, in northern
anchovy, nearly all hydrated oocytes are ovu-
lated.
Atretic Stages
The nomenclature and general characteristics
used for the four atretic stages given below follow
those of Bretschneider and Duyvene de Wit (1947)
and Lambert (1970a). In the initial stage of the
atretic process (alpha (a)), the entire oocyte is
resorbed including the yolk, if present, by the
hypertrophying granulosa cells of the follicle. In
the next stage (beta (^)), the major degeneration
and resorption of the follicle (granulosa and thecal
cells) occurs. In the third (gamma (y) ) and fourth
(delta (8)) atretic stages, regression of the theca
and granulosa cells continues, greatly reducing
the size of the follicle, and a yellow-brown pigment
appears. The histological characteristics used to
identify these stages are outlined below.
1) Alpha (a) Stage Atresia — In the alpha stage
of atresia the oocyte is resorbing leaving only the
follicular layers. The early phase of alpha stage
atresia is characterized by the disintegration of
the nucleus, evident by an irregular shape, and a
granular, dark basophilic staining, and the disin-
tegration of some of the yolk globules, indicated by
less refractive globules, fused globules, or globules
expanded and of less regular shape (Fig. 2a, b, c).
The zona radiata slowly dissolves as indicated by
the loss of striations and uneven diameter (Fig.
2b). In subsequent phases of alpha atresia,
granulosa cells enlarge and, upon rupture of the
zona radiata, invade the degenerating oocyte (Fig.
2d). Yolk adjacent to the invading granulosa cells
liquifies (loses all structural integrity and appears
as a homogeneous eosinophilic area) and becomes
phagocytized by the granulosa cells as indicated
by the presence of yolk in the vacuoles of these
cells. The basophilic staining cytoplasm is also
resorbed by the granulosa cells. In the alpha stage
of atresia, blood capillaries and vessels are numer-
ous in the thecal connective layer which does not
proliferate or invade the oocyte but remains as a
thin layer covering the granulosa cells. The alpha
stage ends when resorption of the oocyte is com-
plete (all cytoplasm and yolk are gone). The result-
ing structure (beta stage) is usually much smaller
than the original oocyte. The subsequent atretic
stages (beta-delta) are steps in the resorption of
the remaining follicle and the structure at this
point is called an atretic follicle, the term atretic
oocyte being reserved for only the alpha stage of
atresia.
In unyolked oocytes the alpha stage process is
similar but without yolk (Fig. 2e, f). The nucleus
123
FISHERY BULLETIN: VOL. 83, NO. 2
Figure 2. — Alpha (a) stage atresia in yolked ( Y) and unyolked (U) oocytes (bar = 0.1 mm), a) and b) Yolked oocyte undergoing alpha
atresia (Ya). Notice dark irregular nucleus (n), uneven dissolving zona radiata (z), and hypertrophic granulosa cells (g); iUa = alpha
atresia of a large unyolked oocyte), c) and d) Only remnants of yolk (y) remain among the invasive phagocytizing granulosa cells in
this late phase of alpha atresia (!« ). Note also the thecal layer (t) and the closely associated red blood cells ( b). e) and f) Unyolked oocytes
in the alpha stage of atresia (Ua), note enlargement of granulosa (g) and disintegration of nucleus (n). (Ya = alpha yolked atretic oocyte,
/3 = beta atresia.)
124
HUNTER and MACEWICZ: ATRESIA IN NORTHERN ANCHOVY OVARY
disintegrates, the thin prezona radiata (if present)
dissolves and the granulosa cells enlarge, and,
with only a slight proliferation, phagocytize the
unyolked oocyte. When resorption is complete, all
that remains is the follicle.
2) Beta ((3) Stage Atresia — Initially the beta
stage atretic follicle is a compact structure com-
posed of numerous disorganized granulosa cells
surrounded by a thin thecal and blood vessel layer.
The nucleus of some of the granulosa cells is pyc-
notic and many of the cells contain a large in-
tracellular vacuole that may be empty or contain
amorphous particles. Occasionally one or more
large intercellular cavities may exist among the
granulosa cells (Fig. 3b, d). Preovulatory beta
stage atretic follicles containing such cavities may
easily be confused with postovulatory follicles
(older than 48 h) and, as a consequence, we do not
age postovulatory follicles older than 48 h (Hunter
and Goldberg 1980). In addition, small (older) beta
stage atretic follicles from yolked oocytes (Fig. 3c,
d) are indistinguishable from beta stage atretic
follicles from unyolked oocytes. Thus, we do not
identify the original oocyte type undergoing at-
resia in beta or subsequent atretic stages; such
distinctions are made only for alpha stage atretic
oocytes.
Three different patterns of atresia may occur at
the conclusion of the beta stage: 1) The follicle
may follow the classic pattern outlined by
Bretschneider and Duyvene de Wit (1947) and pass
through subsequent gamma and delta stages (both
characterized by increased pigmentation, see be-
low); 2) the follicle may be completely resorbed
during the beta stage leaving no histological
characteristics that can be identified; and 3) the
follicle may pass directly from a beta stage struc-
ture to a delta stage structure without passing
through the intervening gamma stage. In north-
ern anchovy, either the duration of the gamma
stage is very short or few follicles pass through the
gamma stage into the delta stage, because in re-
gressing ovaries the incidence of gamma stages is
very low compared with those of either beta or
delta stages.
3) Gamma (y) Stage Atresia — The gamma
stage atretic follicle is usually much smaller than
the typical beta stage follicle (Fig. 3e). The
granulosa cells contain flocculent material of
light-yellow hue and have nuclei of very irregular
shape. The granulosa cells are surrounded by
many fewer thecal cells and blood vessels than
occur in the beta stage atretic follicles. Occasion-
ally we see an atretic follicle of quite different
appearance in anchovy ovaries which we classify
as a gamma stage atretic follicle; they are included
in the gamma stage because they also contain
flocculent material of light-yellow hue. In this
case, the flocculent yellow material is extracellu-
lar rather than intracellular, and the material is
encapsulated by a layer of granulosa and thecal
cells. It is possible that the extracellular flocculent
material is produced by the disintegration of
granulosa cells.
4) Delta (6) Stage Atresia — The diagnostic
characteristic of this stage is the presence of a dark
yellow-brown, finely granular pigment in the
granulosa cells (Fig. 3f). The delta stage atretic
follicles are normally very small structures typi-
cally composed usually of 2-20 granulosa cells in
the ovarian connective tissue stroma. Thecal cells
and blood vessels no longer encompass the
granulosa cells.
In our laboratory work 3-4 levels of abundance
were recorded for each of three atretic classes seen
in anchovy ovaries (alpha, beta, and gamma +
delta stages). The gamma and delta stages were
combined since gamma stages were rare. In addi-
tion, the alpha stage atretic class was further sub-
divided into three groups depending on the type of
oocyte undergoing atresia (unyolked, partially
yolked, and yolked oocytes). In the discussion that
follows we have combined some of the abundance
levels and have considered only what we believe to
be the most diagnostic atretic characteristics, al-
though all atretic characteristics as originally
tabulated are given in Tables 1 and 2. The system
of atretic classifications was further simplified in
our presentation of the analysis of sea-caught
specimens, but that will be discussed sub-
sequently.
RESULTS
Rates of Atresia in the Laboratory
The speed at which yolked oocytes were resorbed
was striking. In the first sample (elapsed time
from onset of starvation = 3 d) the ovaries of 11 of
the 24 females (46%) had yolked ooc5d;es in the
alpha stage of atresia (Table 1). By the 13th day,
half of the females no longer had yolked oocj^s,
and in the rest of the females 50% or more of their
yolked oocytes were in the alpha stage of oocyte
125
FISHERY BULLETIN: VOL. 83, NO. 2
lt3k
Figure 3. — Stages of atresia following after complete yolk absorption (bar = 0.1 mm), a) and b) Typical beta (/i) stage atresia. Note the
disorganized granulosa cells with some pycnotic nuclei (p) or intracellular vacuoles (v) (t = outer layer of thecal cells, c = intercellular
cavities), c) and d) Disintegration of granulosa continues in these older beta (fi) stage atresia. Note the large intercellular cavity (c)
and the prominent, contracted thecal cell layer (t). Also present is an unyolked oocyte in early alpha (Ua) stage and several delta (8)
stage atresia cells, ei Two types of gamma (y) atresia seen in northern anchovy ovaries. Note flocculent material (f) and the thecal
layer (t). f) Delta (6) stage atresia characterized by dark yellow fine granular pigment and an irregular nucleus (n).
126
HUNTER and MACEWICZ: ATRESIA IN NORTHERN ANCHOVY OVARY
Table l. — Percentage of northern anchovy females with ovaries containing various levels of alpha stage atresia
during starvation and after the resumption of feeding.'
Feedi
ing
Percentage of
ovaries
with levels of alpfia stage atresia
Partially yolked
Elapsed time
condition
Unyoll<ed oocytes^
oocytes^
Yolked oocytes^
(d)
Starved
Fed
N
None
N -=5
N >5
None
N -=5
N >5
None
F
■50%
F =
50-90%
F ^91%
3
X
24
79
13
8
46
29
25
50
33
0
13
6
X
21
19
14
67
14
14
62
5
10
19
48
9
X
24
12
17
71
0
58
34
0
8
17
42
13
X
20
10
15
75
20
15
20
0
0
5
40
16
X
24
0
12
88
4
17
17
0
0
0
8
20
X
22
0
36
64
0
0
4
0
0
0
4
23
X
23
9
39
52
0
4
13
0
0
0
0
27
X
23
4
57
39
0
0
0
0
0
0
0
34
X
23
70
17
13
4
0
0
0
0
0
0
41
X
18
83
17
0
17
0
0
17
0
0
0
62
X
22
90
5
5
64
9
9
36
23
0
0
' Feeding begins on the 28th day.
^N = mean number of atretic oocytes per 6 fim section.
^F = mean percentage of atretic oocytes per 6 /um section.
Table 2. — Percentage of northern anchovy females with ovaries containing various levels of beta and gamma+delta
stage atresia and yolked oocytes during starvation and after the resumption of feeding.'
Feeding
condition
N
Percentagi
3 of ovaries with levels of atresia
Go
Beta
stage atresia^
Beta stage atresia
with no yolked
oocytes^
Gamma -rdelta
stage atresia^
icyte types
Elapsed time
from capture
(d)
Yolked
oocytes
present
Only partial
Starved
Fed
None
N -=5
W >5
None
A/ 5=5
N >5
None
N s5
N >5
and unyolked
oocytes present
3
X
24
71
21
8
0
4
0
92
4
4
96
4
6
X
21
24
24
52
0
5
14
71
24
5
81
19
9
X
24
4
8
88
0
0
33
88
8
4
67
33
13
X
20
0
15
85
0
10
45
60
25
15
45
55
16
X
24
0
12
88
0
12
79
16
46
38
8
92
20
X
22
0
9
91
0
9
86
9
36
55
4
96
23
X
23
0
17
83
0
17
83
13
26
61
0
100
27
X
23
0
44
56
0
44
56
26
35
39
0
100
34
X
23
35
48
17
35
48
17
4
13
83
0
100
41
X
18
88
6
6
78
0
6
0
28
72
17
83
62
X
22
82
18
0
35
5
0
0
50
50
59
41
' Feeding begins on the 28th day.
^N = mean number of atretic follicles per 6 /xm section.
resorption (Fig. 4). None of the females sampled on
the 23d day had yolked oocytes, indicating that all
yolked oocytes had passed through the alpha stage
of atresia by this time.
The resorption of unyolked and partially yolked
oocytes began just as rapidly as did the resorption
of yolked oocytes. The percentage of females with
atretic unyolked oocytes in the alpha stage in-
creased sharply from 21% on the 3d day of starva-
tion to 90% on the 13th day. Throughout the rest of
the 27-d starvation period nearly all of the females
(90-100% ) had some unyolked oocytes in the alpha
stage of atresia, indicating a continual recruit-
ment of atretic follicles from the unyolked and
partially yolked oocyte classes. Thus, alpha stage
unyolked and partially yolked oocytes are present
in regressing ovaries for a much longer period
than is the alpha stage of yolked oocytes. This
difference probably is due to the greater number of
unyolked and partially yolked oocytes in mature
ovaries. Yolked oocytes constitute <1% of the total
number of oocytes present in mature ovaries.
The incidence of beta stage atretic follicles also
increased sharply over the first 9 d of the starva-
tion period and followed a pattern similar to that
described for the incidence of alpha atresia from
unyolked eggs (Fig. 4). After attaining a high
value on the ninth day the incidence of beta
atresia remained high until the end of the starva-
tion period as atretic follicles from yolked and un-
yolked oocytes degraded from the alpha to the beta
stage of atresia. Incidence of gamma -I- delta stages
(the third and fourth stages of follicle degenera-
tion) increased later than did alpha and beta
stages and remained high after the onset of
feeding.
Once feeding resumed (day 28), rapid resorption
of yolked and unyolked follicles ceased and the
127
FISHERY BULLETIN: VOL. 83, NO. 2
STARVED
FED
lOOr
YOLKED EGGS PRESENT
50% OR MORE YOLKED
OOCYTES a ATRESIA
• p ATRESIA PRESENT
A a ATRESIA OF UNYOLKED
OOCYTES PRESENT
30 40
ELAPSED TIME (days)
FIGURE 4. — Percentages of captive female northern anchovy
with ovaries having various atretic characteristics during a 27-d
starvation period and after the onset of feeding. Each percentage
is calculated from a sample of 18-24 females (see Tables 1 and 2);
alpha, beta, and gamma through delta stages of atretic follicles
are those defined by Bretschneider and Duyvene de Wit (1941).
dominant process became maturation rather than
resorption. This was indicated by sharp declines in
the percentages of females with alpha stage atre-
sia of unyolked oocj^es and beta stage atretic folli-
cles, and the reappearance of yolked oocytes (day
41). After only 1 wk of feeding the percentage of
females with alpha stage atresia from partially
unyolked oocytes dropped from 96 to 30%.
Some inferences can be drawn from these data
regarding the duration of atretic stages. The sharp
and simultaneous decline in beta stage atretic fol-
licles and alpha stage atresia of unyolked oocytes
(following the onset of feeding) indicates that
alpha and beta stages must have a short and simi-
lar duration. The duration of alpha and beta atre-
sia probably is <2 wk, since the incidence of
these two stages dropped to very low levels 2 wk
after the onset of feeding; a lag of about 1 wk
existed between the first high incidence of females
with beta atresia (9 d) and that for gamma -H delta
(16 d), indicating that the duration of the beta
stage may be about 1 wk. The continued high inci-
dence of gamma -I- delta stages of atretic follicles
long after the onset of feeding indicates that these
late atretic stages must persist in the ovary for
much longer periods than alpha or beta stages.
Although gamma -I- delta stages were present in all
ovaries on the last day of the experiment their
abundance within an ovary had decreased indicat-
ing that even the delta stage would eventually
disappear, eliminating the last histological sign of
past reproductive activity. We conclude from these
inferences that the alpha and beta stages persist
in the ovary for 1 wk or less whereas gamma -i-
delta stages persist for over a month, but eventu-
ally all signs of past reproductive activity are lost.
The occurrence of alpha stage atresia of yolked
oocytes is the best characteristic to use to back-
calculate the time of past reproductive activity in
field-caught specimens because the stage is of
relatively short duration and the time required to
resorb all yolked oocytes is relatively short. On the
other hand, alpha stage atresia of unyolked oo-
cytes, and beta and gamma -^ delta stages are less
useful for back-calculations because these stages
may occur in an ovary for extended periods while
atretic oocytes are recruited from the large reser-
voir of unyolked oocytes in the ovary. In addition,
estimates of the time since the onset of atresia in
ovaries without yolked oocytes (using the inci-
dence of beta or gamma + delta atretic stages) will
always be uncertain because atresia of unyolked
oocytes may occur at low levels in immature or
developing ovaries as well as in regressing
ovaries.
For the laboratory specimens, we calculated the
average elapsed time from the onset of ovary re-
sorption using various classes of alpha stage atre-
sia of yolked oocytes and beta atresia in ovaries
without yolked oocytes (Table 3). We prefer the
criteria of 50% or more of the yolked oocytes with
alpha stage atresia because it is likely that no
spawning will occur in such females. The average
duration of this stage (alpha, yolked, ^ 50% ) in the
starving laboratory females was about 9 d and
ranged from <3 to 20 d from the onset of starva-
tion.
Starvation may have induced a higher rate of
128
HUNTER and MACEWICZ: ATRESIA IN NORTHERN ANCHOVY OVARY
TABLE 3. — Mean and maximum duration of various
atretic characteristics of the ovaries of starved northern
anchovy.
Mean
Metximum
duration
duration
Atretic characteristics
(d)
(d)
Alpha atresia of yolked
oocytes present
8.0
20
Alpha stage atresia in:
<50% of yolked oocytes
4.5
9
50-90% of yolked oocytes
8.1
13
91% or more of yolked oocytes
9.3
20
50% or more of yolked oocytes
9.0
20
No yolked oocytes present and
beta atresia present
>16
>27
oocyte resorption than usually occurs under
natural conditions. Variation in the female nutri-
tional state, food ration, water temperature, day
length, and a host of other variables may affect
rates of atresia. In addition, field data indicate (see
next section) that some spavming may occur in
females with low to moderate levels of alpha
(yolked) atresia, indicating that such stages may
persist under natural conditions for extended
periods. Despite these uncertainties we believe
that our laboratory estimates of atretic rates are
useful for making a rough estimate of the mini-
mum time elapsed since the end of the spawning
season in sea-caught females.
Natural Rates of Atresia
In this section we analyze sea data taken since
1977 for the occurrence of four ovarian atretic
states in a northern anchovy population:
Atretic state 0 — no alpha atresia of yolked oo-
cytes (yolked oocytes present).
Atretic state 1 — alpha atresia of yolked oo-
cytes where <50% of the yolked oocytes are af-
fected.
Atretic state 2 — alpha atresia of yolked oocytes
where 50% or more of the yolked ooctyes are af-
fected (Fig. 5a, b).
Figure 5. — Northern anchovy ovaries wath increasing atresia
states (bar = 0.1 mm), a) 50% of all yolkfed oocytes (Y) are in an
alpha (a) stage of atresia (both early and late are counted). This
is the division point between atretic state 1 and atretic state
2. b) 100% (all) yolked oocytes are in an alpha stage of atresia
(Ya). Also present are a few unyolked alpha atretic oocytes and
several beta (j8) stage atretic follicles. This is still in atretic
state 2. c) All yolk has been resorbed leaving only unyolked
oocytes (U) and many beta (/3) stage atretic follicles. This is
atretic state 3.
Atretic state 3 — ovaries with no yolked oocytes
present and beta stage atresia present (Fig. 5c).
In addition to the atretic condition of the ovary,
we also include histological evidence of recent or
imminent spawning using the system of Hunter
'>S
/3
129
FISHERY BULLETIN: VOL. 83, NO. 2
and Goldberg (1980), i.e., presence of hydrated
eggs (imminent spawning), day 0 or new post-
ovulatory follicles (spawning on the night of cap-
ture), and 1-d-old postovulatory follicles (spawn-
ing on the night before capture). We also include
the number of females judged to have inactive or
immature ovaries with no evidence of atresia. All
data on the incidence of reproductive states are
given in Table 4. In the discussion that follows we
select and regroup these data in various fashions
to test hypotheses and document trends.
Incidence of Spawning in Atretic Females
An important assumption underlying interpre-
tation of ovarian atresia is that the spawning sea-
son has or is going to cease, in other words, the
probability of spawning in females with atretic
ovaries would be expected to be low. To test this
assumption we selected from Table 4 the females
which had alpha stage atresia of yolked oocytes
(atretic states 1 and 2) or yolked oocytes without
alpha atresia (atresia state 0) and calculated the
percentage of these females that had hydrated
oocytes, new (day 0) postovulatory follicles, and
1-d-old postovulatory follicles. Of the females
classed in atretic state 1 (females with <50% of the
yolked oocytes in alpha stage of atresia), 14%
showed evidence of recent or imminent spawning
(postovulatory follicles or hydrated oocytes); 29%
of the females without atresia showed evidence of
spawning (Table 5). Only 1% of those in atretic
state 2 (females 50% or more atretic yolked oo-
cytes) had recently been reproductively active.
That 1.8% of females in atretic state 1 had hy-
drated eggs and 3.7% had age 0 d postovulatory
TABLE 4. — Numbers of female northern anchovy in various atretic and reproductive states
northern California
Postovulatory
Collection dates
number of mature
Atretic
Hydrated
follicles
Yolked
No
yolked
Immature
no
females/collection
state'
oocytes
0 day2 1
day3
oocytes
oocytes
histology"
Total
1977
0
1
2
13
4
20
09/09-09/10
1
2
0
0
(10)
3
3
3
X
1
2
0
13
7
0
23
1978
0
1
1
05/07-05/1 1
1
2
1
5
4
6
4
(10)
3
6
6
X
0
0
1
10
6
0
17
1979
0
39
44
52
279
89
110
613
01/26-02/16
1
2
1
1
1
1
(10)
3
2
2
X
39
44
53
280
91
110
617
1979
0
16
51
45
284
27
18
441
03/22-04/14
1
2
1
5
36
6
42
6
(10)
3
16
16
X
16
52
50
326
43
18
505
1979
0
1
8
4
13
06/09-06/19
1
2
3
1
3
1
(12)
3
16
16
X
0
0
1
12
20
0
33
1979
0
9
31
40
09/19-09/23
1
2
5
0
5
(10)
3
25
25
X
0
0
0
14
56
0
70
1980
0
25
72
52
241
390
03/20-04/10
1
2
9
1
9
1
(20)
3
2
2
X
25
72
52
251
2
0
402
1980
0
4
9
63
B
6
90
04/24-04/27
1
2
11
14
11
14
(20)
3
63
63
X
0
4
9
88
71
6
178
'Atretic state 0 = no alpha stage atresia of yolked oocytes.
state 1 = alpha stage atresia of yolked oocytes present but • 50% oocytes affected,
state 2 = alpha stage atresia of yolked oocytes present, 50% or more oocytes affected
state 3 = no yolked oocytes present and beta stage atresia present.
130
HUNTER and MACEWICZ: ATRESIA IN NORTHERN ANCHOVY OVARY
follicles indicate that some of the females in atretic
state 1 spawn despite the atretic condition of their
ovaries. On the other hand, only two females
classed in atretic state 2 had a recent history of
spawning. These two females had few yolked
oocytes remaining, all but one was in alpha
atresia. This atresia may have increased or even
started during the time elapsed between hydra-
tion and capture. In short, the females in atretic
state 2 probably did not spawn in the highly
atretic state in which they were captured. No
doubt exists that females with moderate levels of
ovarian atresia are capable of spawning because
they often are hormonally induced to do so in the
laboratory. In summary these data indicate that
significant numbers of females in atretic state 1
may continue to spawn under natural conditions,
although the probability of spawning appears to
be about half that offish without ovarian atresia.
Few or none of the females in atretic state 2 con-
tinue to spawn indicating that this stage is proba-
bly the best one to use to calculate cessation of
spawning in the population.
Forcasting the end of Spawning
Using Ovarian Atretic States
In our laboratory study atretic state 1 had an
average duration of about 5 d and atretic state 2, 9
d; state 3 was in excess of 16 d and probably per-
sists for 30 or more days (Table 3). In the sea,
linear projections of the end of the spawning sea-
son from early incidence of atresia is not realistic
since the numbers of females with regressing
ovaries would be expected to increase sharply at
the end of the season.
listed in order of collection dates for southern and Baja California (1977-82) and for
(1979, 1982).
Rostov
/ulatory
Collection dates
number of mature
Atretic
Hydrated
folli
icles
Yolked
No
yolked
Immature
no
females/collection
state'
oocytes
Oday^
1 day 3
oocytes
oocytes
histology"
Total
1980
0
3
32
11
46
05/15-05/28
1
2
1
5
2
6
2
(20)
3
16
16
X
0
1
3
39
27
0
70
1981
0
119
122
148
862
58
1,309
02/05-03/06
. 1
2
2
1
19
3
22
3
(15)
3
10
10
X
119
124
149
884
68
0
1,344
1981
0
77
96
113
559
7
852
04/01-04/19
1
2
3
1
2
57
45
62
46
(15)
3
19
19
X
77
100
115
661
26
0
979
1981
0
2
1
7
10
04/15-04/30
1
2
5
8
5
8
(15)
3
7
7
X
0
2
1
20
7
0
30
1982
0
104
101
189
1,172
52
8
1,626
01/28-03/08
1
2
2
2
10
32
2
46
2
(15)
3
6
6
X
106
103
199
1,206
58
8
1,680
1979^
0
1
42
43
03/20-03/22
1
2
1
40
41
41
41
(30)
3
25
25
X
0
2
0
123
25
0
150
19825
0
2
27
2
11
42
01/22-01/25
1
2
3
2
1
14
5
19
6
(15)
3
13
13
X
5
0
3
45
16
11
80
^New postovulatory follicles <24 h old,
^Postovulatory follicles about 24 h old
"Female not examined histologically, ovary ^1% of body weight.
^Female northern anchovy from northern California; rest of females were from southern and Baja California.
131
FISHERY BULLETIN: VOL. 83, NO. 2
TABLE 5. — Percentage of northern anchovy females taken from 1977 to 1982' that were
classed in three atretic states that occurred in each of five reproductive classes.
Reproductive state
Atretic
state
Percent yoltced
oocytes
with alpha stage
atresia
Postovulatory
follicles
Hydrated
oocytes
(%)
Oday
(%)
1 day
(%)
Spawning No evidence
recent or of recent Total
imminent^ spawning^ number
(%) (%) of females
0
0
7.5
9.7
12.0
29.3
70.7
5.090
1
<50
1.8
3.7
8.1
13.6
86.4
273
2
=50
0
0.7
0.7
1.4
98.6
140
' Calculated from data given in Table 4; only females with yolked oocytes are considered.
^Females with either hydrated oocytes or postovulatory follicles ages 0 or 1 d (the sum of the first three
columns).
^Females with yolked oocytes but without hydrated oocytes or postovulatory follicles.
This nonlinearity becomes obvious when the
end of the spawning season is extrapolated from
numbers of females classed in atretic state 2. For
example, of the 1,620 mature females taken dur-
ing the peak of spawning (28 January-18 March
1982) in southern California (Table 4), only two
were in atretic state 2 and 1,612 had yet to pass
through state 2. Since laboratory data indicate
that about 9 d are required to pass through atretic
state 2, it would require (1,612/2) x 9, or over
7,000 d for the entire population to become atretic
at the rates of atresia observed in February, which,
of course, is nonsense. Projections of the end of the
spawning season using higher rates of atresia
taken in April in southern California (24-27 April
1980) give a more realistic projection ((87/
14) X 9 = 56 d). Such an arithmetic projection
may be inappropriate for collections which have a
very high rate of atresia such as those taken in
Monterey in March 1979 ((84/41) x 9 = 18 d), and
a geometric model might be preferable. The point
we wish to emphasize is that atretic rates are
nonlinear over the season with the rate increasing
markedly as the season closes. Thus only samples
taken near the close of the spawning season are of
value for forecasting the end of spawning for the
population.
Seasonal Changes in Atresia
Among Females of Different Lengths
To evaluate how atretic rates change among
females of different lengths, we segregated our
data into two length classes (females ^ 10 cm SL
and those >10 cm SL) and calculated the percent-
age of mature females that had atretic ovaries
(atretic states 1-3 combined). Mature is defined
here as all females except those which have yet to
reach first maturity (small females with small
immature non-atretic ovaries). We also calculated
the fraction of females in each length class with
1-d-old postovulatory follicles, a measure of the
percentage of females spawning daily (Hunter and
Goldberg 1980).
In every case, regardless of cruise or season,
small females (^10 cm SL) consistently had a
higher rate of ovarian atresia than did larger ones
(>10 cm SL) (Table 6). This is a strong trend as the
probability of such an event (9 pairs of the same
sign) is (1/2)^. In addition, the difference between
pairs was statistically significant (chi-square test)
even when the levels of atresia were quite low. For
example, in February-March 1981, only 4.1% of the
small females and 1.9% of the large females were
atretic, yet this difference was significant at P <
0.05 using the chi-square test. As would be ex-
pected, the percentage of females with atretic
ovaries increased in both length classes as the
season progressed from January through June.
The consistency of the differences in the inci-
dence of atresia between large and small females
indicates that the smaller ones must have a much
shorter spawning season than larger ones.
Females <10 cm long are typically about 1-yr-old
and are in their first spawning season whereas
those longer than 10 cm are predominantly 2-3 yr
old and have spawned during the previous sea-
sons. These data indicate that the first spawning
season of females may be quite short with signifi-
cant numbers of females leaving the spawning
population in early April, while the older fish con-
tinue to spawn. That the rates of atresia in young
fish were always higher even in the peak months of
spawning such as February and March indicates
that a small percentage of small females may only
spawn a few times during the season in contrast to
the older females which appear to be spawning at
about weekly intervals for months. The fraction of
small females spawning per day would be expected
to be less than larger females since the small
females have a higher incidence of ovarian atresia.
We calculated the fraction of females spawning per
132
HUNTER and MACEWICZ: ATRESIA IN NORTHERN ANCHOVY OVARY
TABLE 6. — Percentage of mature northern anchovy females in two length classes with
atretic ovaries. Females from north of Point Conception and groups with fewer than nine
females per length class excluded.
Percent of
Fraction mature
Number of
mature females
females spawning
Cruise period
mature females'
with atretic
ovaries^
per day percent^
From to
year -
10 cm
>10cm
^10 cm
>10cm
■ilOcm >10cm
01/26 -»02/ 16
1979
121
297
1.7
0.7
8.0 15.9
01/28^03/18
1982
97
1,523
14.6
2.6
14.1 12.2
02/05 ->03/06
1981
462
824
4.1
1.9
10.2 13.7
03/20—04/10
1980
68
334
8.8
1.8
11.7 15.2
03/22—04/14
1979
30
430
23.3
13.3
3.8 11.8
04/01 —04/19
1981
102
870
39.2
10.0
10.5 12.9
04/24—04/27
1980
64
100
969
26.0
0 8.6
04/15—04/30
1981
10
20
80.0
60.0
0 5.3
05/15-05/28
1980
15
44
73.3
29.5
6.2 4.4
'All females given in Table 4 except those with immature ovaries and those not examined histoloqicallv.
^Ail females in atretic states
,1,2, and 3 combined.
^Fraction of females spawnii
nq = F.
where F =
m^.
2m,
m ■ = mature nonspawning females, and m = females with 1-d-old postovulatory follicles.
day for the two length classes to test this assump-
tion. We used the Stauffer and Picquelle (footnote
3) method for estimating spawning fraction as it
corrects for biases in the numbers of females with
hydrated eggs, i.e.,
M,
F =
2M, + m
li ni
where F = fraction of females spawning per day,
M^^ = number of females with 1-d-old postovula-
tory follicles, and m = number of mature females
with no recent spawning history (females with
postovulatory follicles or hydrated eggs are
excluded). Examination of Table 6 indicates that
differences in spawning fraction between the two
size classes of females were much less distinct
than were the differences in ovarian atresia.
Using only the 8 cruises in which the numbers of
females in each of the two length classes exceeded
10, the mean difference in spawning fraction (frac-
tion for large females — fraction for small females)
for the set of 8 cruises was +3.76% with 95% C.I.
±3.50% indicating a small difference in spawning
frequency between the two length classes that is
just barely significant at the 5% level. We believe
the reason that differences in atretic fraction be-
tween large and small females are much more
consistent than those in spawning fraction is that
spawning fraction has a greater variability and a
much more limited dynamic range than does the
atretic fraction. Spawning fraction varies from 0 to
about 16% and may be affected by time of day and
schooling behavior (Hunter and Goldberg 1980).
Atretic fraction varies from 0 to nearly 100%,
is not linked to reproductive behavior, and conse-
quently, is probably not affected by time of day or
schooling.
DISCUSSION
Evaluation of Atretic Classification
Our objective was to evaluate the use of ovarian
atretic states to characterize the reproductive bi-
ology of northern anchovy populations. We in-
cluded in our analysis of laboratory data many
atretic characteristics not used to construct the
three atretic states utilized in the analysis of sea
data. These additional characters could be used to
create additional states or to more precisely de-
limit the existing ones. Our selection of charac-
teristics was based in part on ease of identification
since for population work thousands of histologi-
cal sections were examined. Other considerations
include the fact that statistical analysis indicated
that classifiers frequently confused beta stage
atretic follicles in yolked ovaries with postovula-
tory follicles older than 24 h, and, as a conse-
quence, beta atresia was not used as a diagnostic
character in ovaries with yolked oocytes. Alpha
stage atresia was the most useful atretic stage
because the type of oocyte (yolked) undergoing
atresia is still discernible. In addition, alpha stage
atretic oocytes can be easily distinguished from
postovulatory follicles whereas this is not the case
for later atretic stages.
Three atretic states were defined and applied to
sea data. The incidence of all three atretic states
combined was a sensitive index of the reproductive
state of the population over the spawning season.
133
FISHERY BULLETIN: VOL. 83, NO. 2
In fact, the atretic condition of the ovary was a
more sensitive index of seasonal changes in the
reproductive rate among size classes of females
than was the incidence of spawning based on the
presence of postovulatory follicles.
Atretic state 1 (<50% of yolked oocytes in the
alpha stage of atresia) was not useful for estimat-
ing atretic rates in an absolute sense since this
state appeared to persist in natural populations
for extended and probably variable periods. Some
spawning occurred among females classed in
atretic state 1, although the frequency of spawning
was less than half of that of females without
ovarian atresia. Batch fecundity might also be
reduced in females classed in atretic state 1, a
speculation worth further study. Atretic state 1
was a useful index of atretic rates during peak
spawning months. At such times it was the most
common atretic condition and detection of differ-
ences in atretic rates among length classes was
largely a function of the number of females in this
state.
Atretic state 2 (5(y7f or more of yolked oocytes in
alpha atresia) persisted for about 9 d in the
laboratory, and judging by its low frequency in
field collections this state may have a similarly
short duration in natural populations. Females
with ovaries in this state rarely or never spawn, as
might be expected, since more than half of the
yolked oocytes are not viable. In addition, a short
duration of this state also might be expected on the
grounds that it seems maladaptive to prolong such
a threshold condition. For the above reasons
atretic state 2 seems to be the best absolute mea-
sure of the rates of ovary resorption in the popula-
tion and the only state that might provide an accu-
rate forecast of the end decline of reproduction in a
population. Unfortunately, accurate forecasts of
the end of spawning for a population can be made
only near the end of the spawning season.
Atretic state 3 (no yolked oocytes with beta at-
resia present) identifies females in late post-
spawning condition. Such females cannot be sepa-
rated from immature females on the basis of gonad
weight or using gross anatomical criteria. This
state persisted for about 30 d in the laboratory, but
it may last much longer under natural conditions
while the numerous small oocytes are resorbed.
The laboratory data indicate that the duration of
this state could be increased if the definitions were
changed to include gamma + delta stages of atresia
which have a longer life in the ovary than the beta
stage. The laboratory data also indicated that
even gamma + delta stages of atresia would even-
tually disappear from the ovary so that no signs of
previous spawning activity would exist in a re-
gressed ovary. It is doubtful that the duration of
atretic state 3 or any late postspawning state will
ever be accurately estimated because it is depen-
dent on too many environmental circumstances.
Nevertheless, this state is very useful in separat-
ing females in postspawning condition from
females with no previous reproductive history.
This is an essential distinction for estimating
spawning biomass (Stauffer and Picquelle foot-
note 3) and for determining the size or age at first
reproduction (Hunter and Macewicz 1980).
Possibly the most important future application
of atretic classification of ovaries is for process
oriented sea work on the reproductive biology of
multiple spawning fish such as the northern an-
chovy. Such work does not require a large sample
as do estimates of reproductive characteristics for
an entire population. The reproductive state of an
individual female can be accurately defined by the
atretic criteria we have discussed, and the spawn-
ing state criteria described by Hunter and
Goldberg (1980). The reproductive characteristics
of a female can be related to its physiological state
(age, fat content, biochemical composition, and in-
stantaneous growth rate from otoliths or RNA/
DNA ratios) and functional relationships estab-
lished between reproduction and the environ-
ment. In this way the factors controlling the
duration of the spawning season, and the total
fecundity during the season, can be identified
under natural conditions.
Biological Implications
Several important biological conclusions can be
drawn from this work. Only a few attempts have
been made to estimate the time needed for a folli-
cle to disappear by atresia in vertebrates and no
information exists for fishes (Byskov 1978). Our
focus was on atretic rates of all oocytes in the
ovary and not on an individual follicle; neverthe-
less, the striking speed with which all yolked oo-
cytes passed through the initial stages of atresia
indicate that the rate for individual follicles must
be high. Similar rates were observed in the guppy
by Lambert (1970a). In the guppy, alpha stage
atresia of yolked oocytes appears about 1 d after
parturition, and beta stage atresia appeared about
2 d after the first alpha stages were detected; beta
stages persisted for only 11 d. In the anchovy, the
average time for all yolked oocytes in the ovary to
pass through alpha atresia was 8.0 d and the
134
HUNTER and MACEWiCZ: ATRESIA IN NORTHERN ANCHOVY OVARY
maximum time was 29 d. Thus the effect of atresia
on fecundity may be underestimated since the du-
ration of atretic stages is short and a small stand-
ing stock of atretic oocytes could be an indication
of a high loss rate. On the other hand, laboratory
studies seem to indicate that atretic rates are not
sufficiently high to account for the differences in
fecundity observed when fish are fed high and low
rations (Tyler and Dunn 1976; Wootton 1979). The
duration of the atretic stages in these studies was
unknown, however.
Additional evidence for the volatility of the re-
productive state of anchovy is an important con-
tribution of this study. Our laboratory data indi-
cated that given a shortage of food the ovary can be
rapidly resorbed leaving no trace of former repro-
ductive activity in a few months or less, but when
given sufficient food atresia stopped, maturation
and vitellogenesis resumed, and a reproductively
active ovary was rapidly reformed within 35 d.
Clearly, in such multiple spawning fishes as the
anchovy, more than one spawning season per year
is possible given the appropriate environmental
conditions. This may explain the occurrence of a
second annual spawning period in the Peruvian
anchoveta (Santander and Castillo 1976) and the
occasional heavy fall spawning of the northern
anchovy ( Smith 1972 ). That active ovaries are con-
sistently produced from small, inactive ones in
30-60 d in the laboratory (Leong 1971; Hunter and
Leong 1981) and that some reproductively active
females are found the year around also supports
this view.
Food shortage does not always lead to regression
of the ovary in anchovy or any other multiple
spawning fishes. In addition to food ration, regres-
sion of the ovary also depends upon the level of
energy reserves, the timing of the reproductive
cycle, and perhaps certain environmental condi-
tions such as temperature and day length. For
example, starvation of 40-80 d did not block the
initial increase in the size of ovaries of the goby
Gillichthys at the start of the reproductive cycle in
July but only 23 d of starvation resulted in ovarian
regression in January when active vitellogenesis
was occurring (de Vlaming 1971). Similarly we
noted in a preliminary experiment that starving
anchovy of 25^f greater wet weight than those
used in this study produced a slower regression of
the ovary over a 36-d period than occurred in the
present study. The present study is more represen-
tative of natural conditions since the fish were
taken in midspawning season when their ovaries
were active whereas in the preliminary study the
fish were taken out of season and fed heavily for 30
d to induce gonad maturation before the onset of
the 36-d starvation period.
Another important conclusion from this study
was that young female anchovy spawning for the
first time probably have a much shorter reproduc-
tive season than do older females. Hunter and
Leong (1981) estimated that the average female
spawns about 20 times per year. Thus the older
females must spawn considerably more often than
20 times per year, and probably contribute a much
larger fraction of the reproductive output of the
population than a proportionate share by weight.
This indicates the importance of maintaining
older fish in the population and that danger may
exist if older fish are overharvested.
ACKNOWLEDGMENTS
We thank Roderick Leong (Southwest Fisheries
Center (SWFO) for providing and maintaining
the northern anchovy used in the laboratory study.
We thank Kenneth Mais (California Department
of Fish and Game) for providing some specimens.
Pedro Paloma (SWFC) and Eric Lynn (SWFC) as-
sisted in histological classifications. Carol Kim-
brell (SWFC) and Susan Picquelle (SWFC) pro-
vided valuable assistance in analyzing the data.
LITERATURE CITED
barr, w. a.
1963. The endocrine control of the sexual cycle in the
plaice, Pleuronectes platessa iL.) I. Cyclical changes in
the normal ovary. Gen. Comp. Endrocrinol. 3:197-204.
BOUAIN, A., AND Y. SlAU.
1983. Observations of the female reproductive cycle and
fecundity of three species of groupers iEpmephelus^ from
the southeast Tunisian Seashores. Mar. Biol. (Berl.)
73:211-220.
BOWERS, A. B., AND F. G. T. HOLLID.W.
1961. Histological changes in the gonad associated with
the reproductive cycle of the herring iClupea harengus
L.). Dep. Agric. Fish. Scotl.. Mar Res. 5:1-16.
BRETSCHNEIDER, L. H., AND J. J. DUYVENE DE WIT.
1947, Sexual endocrinology of non-mammalian verte-
brates. Monogr. Prog. Res., Vol. II, Elsevier, N.Y.
BYSKOV, A. G.
1978. Follicular atresia. In R. E. Jones (editor), The ver-
tebrate ovary: Comparative biology and evolution, p.
533-562. Plenum Press, N.Y.
CROSSLAND, J.
1977. Seasonal reproductive cycle of snapper Chrysophrys
auratus (Forsten in the Hauraki Gulf N.Z. J. Mar.
Freshwater Res. 11:37-60.
DE VLAMING, V. L.
1971. The effects of food deprivation and salinity changes
on reproductive function in the estuarine gobiid fish, Gil-
lichthys mirabilis. Biol. Bull. (Woods Hole 1 141:458-471.
135
FISHERY BULLETIN: VOL. 83, NO. 2
1972. Reproductive cycling in the estuarine gobiifish Gil-
lichthys mirabihs. Copeia 1972:278-291.
DE VLAMING, V., G. GROSSMAN, AND F. CHAPMAN.
1982. On the use of the gonosomatic index. Comp.
Biochem. Physiol. 73A:31-39.
FULTON, W.
1898. On the growth and maturation of the ovarian eggs
of Teleostean fishes. Annu. Rep. Fish. Board Scotl. 16:
88-124.
HOAR, W. S.
1965. Comparative physiology: hormones and reproduc-
tion in fishes. Annu. Rev. Physiol. 27:51-70.
HTUN-HAN, M.
1978. The reproductive biology of the dab Limanda
limanda (L.) in the North Sea: seasonal changes in the
ovary J. Fish Biol, 13:351-359.
Hunter, J. R., and S. R. Goldberg.
1980. Spawning incidence and batch fecundity in north-
em anchovy, Engraulis mordax. Fish. Bull., U.S. 77:
641-652.
Hunter, J. R., and r. Leong.
1981. The spawning energetics of female northern an-
chovy, Engraulis mordax. Fish. Bull., U.S. 79:215-230.
Hunter, J. R., and b. J. Macewicz.
1980. Sexual maturity, batch fecundity, spawning fre-
quency, and temporal pattern of spawning for the north-
em anchovy, Engraulis mordax, during the 1979 spawn-
ing season. Calif. Coop. Oceanic Fish. Invest. Rep.
21:139-149.
Lambert, J. G. D.
1970a. The ovary of the guppy, Poecilia reticulata. The
atretic follicle, a Corpus atreticum or a Corpus luteum
praeovulationis. Z. Zellforsch 107:54-67.
1970b. The ovary of the guppy Poecilia reticulata . The
granulosa cells as sites of steroid biosynthesis. Gen.
Comp. Endocrinol. 15:464-476.
Leong, r.
1971. Induced spawning of the northern anchovy, En-
graulis mordax Girard. Fish. Bull., U.S. 69:357-360.
ROBE, A. R
1982. Histological observations on the reproductive biol-
ogy of the haddock, Melanogrammus aeglefinus (L.). J.
Fish Biol. 20:397-408.
SAIDAPUR, S. K.
1978. Follicular atresia in the ovaries of non-mammalian
vertebrates. Int. Rev Cytol. 54:225-244.
Santander, h., and O. S. de Castillo.
1979. El ictioplancton de la costa Peruana. Inst. Mar
Peru Bol. 4:69-112.
Smith, R E.
1972. The increase in spawning biomass of northern an-
chovy, Engraulis mordax. Fish. Bull., U.S. 70:849-874.
Tyler, a. v., and r. S. Dunn.
1976. Ration, growth, and measures of somatic and organ
condition in relation to meal frequency in winter flounder,
Pseudopleuronectes americanus, with hypotheses regard-
ing population homeostasis. J. Fish. Res. Board Can.
33:63-75.
VROOMAN, A. M., P A. PALOMA, AND J. R. ZWEIFEL.
1981. Electrophretic, morphometric, and merisitic studies
of subpopulations of northern anchovy, Engraulis mor-
dax. Calif Fish Game 67:39-51.
WALLACE, R. A., AND K. SELMAN.
1981. Cellular and dynamic aspects of oocyte growth in
teleosts. Am. Zool. 21:325-343.
WOOTTON, R. J.
1979. Energy costs of egg production and environmental
determinants of fecundity in teleost fishes. Symp, Zool.
Soc. Lond. 44:133-159.
YAMAMOTO, K.
1956. Studies on the formation of fish eggs. 1. Annual
cycle in the development of ovarian eggs in the flounder,
Liopsetta obscura. J. Fac. Sci. Hokkaido Univ., Sen 6,
Zool. 12:362-373.
ZANUY, S.
1977 . Induccion a la puesta y estudio de la ovogenesis en un
teleosteo marine: Paracentropristis cabrilla L. Invest.
Pesq. 41:337-384.
136
EGG PRODUCTION OF THE CENTRAL STOCK OF
NORTHERN ANCHOVY, ENGRAULIS MORDAX, 1951-82
Nancy C. H. Lo'
ABSTRACT
A model was developed for estimating daily production of eggs of northern anchovy from counts of the
total numbers of eggs and size-frequency distribution of larvae. Estimates of egg production using this
model were compared with three estimates based on the mortality rates of staged (aged) eggs. The
model was used to calculate daily egg production of anchovy for a 24-year time series (1951-82) (data
were collected each year from 1951 to 1966 and 1979 to present and every 3 years from 1966 to 1979).
Comparisons of this index of stock abundance with ones based on the standing stock of larvae indicate
that the present model is a better index of spawning biomass. It was found from the 1979-81 data that
the eggs and larvae (< 20 days) have different forms of instantaneous mortality rate (IMR): The larval
IMR was age dependent, i.e., zit) = pit for tc < t whereas the egg IMR was constant 2(n = a for t < tc
where tc is incubation time or yolk-sac absorption. Based upon this model, the daily egg production,
and egg-larval mortality rates for larvae <20 days (<8 mm preserved length), were estimated for
1951-82 from data collected with 1 m ring nets and bongo nets. Egg production varies with stock size
proportionally if the reproduction effort remains constant. The egg production is a better index of stock
size than the larval abundance because the latter is subject to the inherent egg and larval mortality in
addition to reproductive output.
Ichthyoplankton data have been used extensively
for estimating biomass (or spawning biomass) of
marine fish stocks (Murphy 1966; Ahlstrom 1968;
Smith 1972). One of the tacit assumptions under-
lying most of the methods used for estimating
biomass from ichthyoplankton data is that egg or
larval mortality is constant among years. In
recent years, however, it has become increasingly
evident that egg and larval mortality is quite
variable among years and among life stages (Ahl-
strom 1954; Marr 1956; Colton 1959; Burd and
Parnell 1972; Gushing 1973; Fager 1973; Harding
and Talbot 1973). As a result, biomass indices
based on standing stock of eggs or larvae are
subject to a considerable bias if the interannual
variability in mortality is not taken into account.
In order to eliminate the bias, attempts were made
to estimate the spawning biomass by using the egg
production and reproduction parameters (Saville
1964; Beverton and Holt 1965; Ciechomski and
Capezzani 1973). The basic model is
Po = BaRiE/W)
where Po = egg production at age zero,
Ba = spawning biomass,
(1)
'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, PO. Box 271, La Jolla, CA
92038.
R =
E =
W =
proportion of spawning biomass be-
ing female,
average batch fecundity,
average mature female weight.
Equation (1) is adequate for species that spawn
only once during a season. But for the multiple
spawners, like northern anchovy, Engraulis mor-
dax, one needs to include another adult parameter,
the proportion of mature spawning female (F), in
the equation (Parker 1980). Moreover, Parker
chose to use egg production per day, as this could
be easily estimated from a single cruise. Thus, the
egg production model (EPM) for northern anchovy
(or any multiple spawning stock) becomes
Po = BaRF{E/W).
(2)
Manuscript accepted April 1984.
FISHERY BULLETIN: VOL. 83, NO. 2, 1985.
Staged eggs are used to estimate the daily egg
production (number of eggs per day) of the popula-
tion (Po) while adult fish are sampled to estimate
the number of eggs produced per fish weight
(E/W), sex ratio (i?), and proportion of mature
spawning female iF). This method is, without
doubt, the best of all ichthyoplankton biomass
estimation techniques. It is, however, a data rich
method requiring both ichthyoplankton and adult
sampling plus staging of eggs and various labora-
tory measurements which may not be available.
In this report, I present an alternative method for
137
FISHERY BULLETIN: VOL. 83, NO. 2
estimating biomass using conventional ichthyo-
plankton data rather than the extensive sets of
specialized information required by the EPM
method. This alternative method provides esti-
mates of the daily egg production (Pq) and is
referred to as the historical egg production (HEP)
to distinguish it from the current EPM. This
model for HEP requires only the standing stock of
unstaged eggs, and the numbers of larvae in
various length classes subsequently transformed
into age classes using Gompertz growth curve
(Zweifel and Hunter"; Methot and Hewitt^; Lo
1983). Daily egg production varies proportionally
with the stock size if the reproduction effort of the
population remains constant. The production of
eggs by a stock is certainly a better index of stock
size than the standing stock of larvae (Smith 1972 )
because both egg and larval mortality rates are
considered in the former case.
In addition to development of the model, I
provide a time series of northern anchovy HEP for
1951-82. This historical record of daily egg produc-
tion rather than the EPM i Equation (2) ) was used
to estimate anchovy biomass for these past years
because data were not available for all the female
reproductive parameters until 1980 and none of
the eggs have been staged. It would be unpractical
and take years to do all the staging of eggs that
would be required for all the years. The HEP is an
unbiased index for the spawning biomass (Ba ) of
the anchovy population for those years if the
annual reproductive output per fish weight has
remained constant. I do not have sufficient data
to validate the assumption of constant reproduc-
tive output although 1981-82 data do indicate so.
peak spawning season of northern anchovy was
usually February- April, daily egg production for
the central stock northern anchovy was computed
from egg and larval data (CalCOFI'^) collected in
January-April within these eight regions. The
CalCOFI survey was conducted each year until
1966 after which the survey was conducted every
3 yr. Owing to various improvements in the design
of the plankton nets over the past 20 yr (Smith and
Richardson 1977; Stauffer and Picquelle 1980*^),
different calibration factors were necessary to
standardize the catch of eggs and larvae taken in
different nets: Aim ring net with 0.55 mm silk
mesh was used until 1969 when it was replaced by
aim ring net with 0.505 mm nylon mesh; this net
was used until 1978 when it was replaced by the
bongo net of 0.505 mm nylon mesh. Beginning in
1979, a vertical tow of the 0.333 mm mesh, 25.23
cm diameter CalVET net (CalCOFI vertical egg
net) (Hewitt 1983) was used along with the 0.505
mm mesh bongo net to collect egg and larval
samples in order to estimate the northern anchovy
spawning biomass using the egg production meth-
od (EPM) (Parker 1980). In addition to the bias in
catch caused by the different mesh sizes, biases
also existed due to avoidance of the net, water
volume filtered through the net (measured by
water flowmeter readings), growth rate of larvae,
temperature dependent incubation time (in days),
and proportion of larvae from each plankton
sample sorted (Zweifel and Smith 1981; Lo 1983).
All data (counts of eggs and larvae) were adjusted
for the above biases, when it was appropriate,
following the procedures outlined by Zweifel and
Smith (1981).
ASSEMBLY AND BIAS CORRECTION OF
EGG AND LARVAL DATA
The northern anchovy spawning area lies off
central and southern California and Baja Califor-
nia. The sampling area was divided into 23 regions
covering 17.556 x 10" m" (Fig. 1). The central
anchovy stock is enclosed by eight regions (4, 5, 7,
8, 9, 11, 13, and 14) with a total of 5.703 x 10" m^
(Duke 1976^ Huppert et al. 1980). Because the
Egg Data
The counts of unstaged eggs from each tow were
adjusted to a standardized volume of water filtered
per unit depth (0.05 m^/1 m depth = 0.05 m^ sea
surface area = area sampled by the CalVET net).
The adjusted egg counts per 0.05 m^ sea surface
area were then stratified by CalCOFI regions. A
weighted mean egg count per 0.05 m^ was com-
puted as
^Zweifel, J. R., and J. R. Hunter. Unpubl-. manuscr. Tem-
perature specific equations for growth and development of an-
chovy, Ertf^rciiilis mordax, during embryonic and larval stages.
^Methot, R. D., and R. R Hewitt." 1980. A generalized
growth curve for young anchovy larvae, derivation and tabular
example. Natl. Mar Fish. Serv, Southwe.st Fish. Cent. Admin.
Rep. LJ-80-17, 8 p.
•'Duke, S. 1976. CalCOFI station and region specifica-
tions. Natl. Mar. Fish. Serv., Southwest Fish. Cent. Admin.
Rep, LJ-76-3, 37 p.
^CalCOFI. California Cooperative Ocean Fisheries Investi-
gation, a program sponsored by the State of California. The
cooperating agencies in the program are California Department
of Fish and Game, National Marine Fisheries Service, and
Scripps Institution of Oceanography, University of California.
"Stauffer, G.D., and S.J. Picquelle. 1980. E.stimates of the
1980 spawning biomass of central subpopulation of northern
anchovy. Natl. Mar. Fish, Serv, Southwest Fish. Cent. Admin.
Rep. LJ-80-09,
138
LO: EGG PRODUCTION OF NORTHERN ANCHOVY
135°
130°
125"W.
/
V ^
/
y
0
o o
o o o o 0 o o oJo O OO f ~ ' ^ iff
o
o o
o o o o o o o /o o o of
35°
NORTHERN CALIFORNIA
/ /^
,_. ^ O
o o
ooooooA" « / CAPE MENDOCINO
1 INSHORE
3
x^ ^J ^^ \J ^^ t^ • ' '
2
C\ t\ f*t f\ C\ /\
2 NEARSHORE
. \
3 OFFSHORE
°°t 7
<
3 O O
o o o o o
o o o oy
3 O O
o o o o o
o o o oV
-
O O O
o o o o o
\
o o o \ A
V
/U SAN FRANCISCO
o o o
0 o o o o
o o o o / if
CENTRAL CALIFORNIA
{
4 INSHORE
o o o
6
o o o
o o o o o
5
o o o o o
o o o o^
4 /
o o o o\
5 NEARSHORE
30°
^ 6 OFFSHORE
\
o o o
o o o o o
o o o o\
.
o o o
o o o o o
o o o o^
( POINT CONCEPTION
o o o
O o o o o
o I o o o V^
\ ciV
SOUTHERN CALIFORNIA
o o o
o o o o o
o\
o ^ ^^0]
7 INSHORE
o o o
o o o o o
o o
o o o o o j "^
8 NEARSHORE
10
9
8
'^ A
9 OFFSHORE
O O 0
o o o o o
o o
o o o Q o odL
10 EXTENDED
o o o
o o o o o
o o o\o o o o o o/
\^ / SAN DIEGO
25°
o o o
O O O 0 o
o o o o ^
o o o
■v
I
o o o
o o o o o
o o o o o
o o oaJ -
BAJA CALIFORNIA
o o o
o o o o o
o o o o o
o o oJ <
II INSHORE
II A
12 BAY
13 NEARSHORE
14 OFFSHORE
o o o
15
o o o
o o o o o
14
o o o o o
o o o o ©yo oo/ / ^-^^
oooo/oooo) /
\
15 EXTENDED
o o o
o o o o o
ooooJooooV i
7 12 \ \ .
o o o
o o o o o
O 0
3/^0 0000 0[ \ ^
o o o
o o o o o
o o
D o 0*^*^ coo) L, •
SOUTH BAJA
o o
o o o o o
o o o.o o oo^\p^^^^ /
\ (EUGENIA /
20°
K 16 INSHORE
o o 1 o o o o o
o o o o\ o o oV. \
17 NEARSHORE
19
18
17 \ 16 l^ )
18 OFFSHORE
o o
o o o o o
o o o o o\o o o r u
19 EXTENDED
o o
O O 0 o o
O O 0 o o o\ O O O V i{\
o o
O O O 0 o
000000 0)0 o/ /
1 /
\r
o o
o o o o o
o o o o o
oo o^
) •
CAPE
o o
O O O O 0
o o o o o
.o o^S >
20 INSHORE
o o
O 0 o o o
o o o o o o o\o o o\ L-
21 NEARSHORE
23
22
2! \20V Al
22 OFFSHORE
O 0
o o o o o
oooooooo\oo\ I
15°
23 EXTENDED
o o o o o
oooo ooooloo <3L-*-<-^^
/
o o o o o
oooooooooXooo
/ /
40°
N.
35°
30°
25°
120^
1 15°
110°
Figure l. — Sampling area for estimating northern anchovy spawning biomass with CalCOFI sampling stations
denoted by the open circles, and CalCOFI regions denoted by numbers (from Duke text footnote 4).
139
FISHERY BULLETIN: VOL. 83, NO. 2
i. i
where xi is the adjusted mean egg count for re-
gion i and W, is the relative area weight for region
i.
Region
nmi^ xlO"^
m' xlO-'''
Wi
4
18
6.105
0.107
5
29
9.878
0.174
7
20
6.896
0.119
8
12
4.116
0.072
9
29
9.878
0.174
11
9
3.171
0.0538
13
21
7.122
0.126
14
29
9.866
0.174
Total
167
^57.031
1.00
^ Sum is not equal to the total due to rounding error.
Zero catch was assumed for regions where no
samples were taken because historical records
show those regions usually had low densities of
eggs and larvae. The weighted Xu's were also
corrected for extrusion through the mesh by mul-
tiplying the catch by the ratio of the catch in a
0.150 mm CalVET net to the catch in the net used
in a particular survey (r): r = 3.6 for 0.55 mm
mesh silk 1 m ring net 1 1951-68), r = 3.04 for 0.505
mm mesh Nitex' 1 m ring net (1969-76), r = 12.76
for 0.505 mm mesh Nitex bongo net (1978-present)
(Lo 1983). The 0.505 mm mesh bongo net seems to
catch 4 times that of a 1 m ring net. The reason is
unknown. (A field experiment was conducted in
April 1983 to reestimate the extrusion rate of
anchovy eggs from 0.505 mm mesh bongo net. The
data have not been analyzed at the time of writing.
Although the egg samples from bongo nets were
u.sed to compute the HEP, the bongo net is pri-
marily used for catching anchovy larvae, whereas
the CalVET net is the egg sampler The discrep-
ancy between bongo and 1 m ring net is not of
major concern for the current anchovy biomass
estimation. ) The standing stock of eggs per 0.05
m^ is then
and
mt, = Xu- r
var (mil ' = var ixw )r + xfr var(r)
where mt is the standing stock ofeggs( and larvae)
Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
140
up to age t days from fertilization. Here ti is the
duration of incubation.
The size of standing stock of eggs depends on not
only egg production rate and mortality rate but
also the duration of incubation (or the incubation
time), which is a function of sea temperature. The
average temperature for all positive egg tows
(tows which contain one or more anchovy eggs)
over January-April in each year was used to
estimate incubation time {ti) using the equation
(Lo 1983)
ti - (18.73 e"°^25^^"^P)
where ti = incubation time in days,
temp = temperature in degrees centigrade.
Both the standing stock of eggs imii') and the
incubation time (ti) are essential in computing
the time series of daily egg production. The
temperature in January- April ranges from 11° to
19° C. The long-term average temperature from
January to April is 14.25° C, thus the average
incubation time is 3.15 d.
Larval Data
The anchovy larvae from all years were mea-
sured to the nearest 0.5 mm preserved length. For
the purpose of estimating mortality rate, larval
data were grouped into 2.5 mm, ranging 2-3.0 mm;
3.75 mm, 3.5-4.0 mm; 4.75 mm, 4.5-5.0 mm: ... for
larvae < 30 mm. Each preserved length was first
converted to a live standard length using a shrink-
age formula based on the tow duration (Theilacker
1980), and then converted to age (,t days) using a
two-cycle Gompertz growth curve. The first cycle
is from hatching to yolk-sac absorption, a temper-
ature-dependent growth curve, and the second
cycle is from yolk-sac absorption to 22 mm larvae,
a food-dependent growth curve (Zweifel and Hunt-
er footnote 2; Methot and Hewitt footnote 3; Lo
1983). Larval abundance by length (age) group
was estimated using a negative binomial weighted
model (Bissell 1972; Zweifel and Smith 1981)
which incorporates the "effective sampler size"
(relative sampler bias). All larval abundance data
were adjusted to conform to the following standard
conditions: no extrusion, no day-night difference
in avoidance, and a constant water volume filtered
per unit depth. These data were converted to daily
production (Pt) by dividing the total number of
larvae in each length group by the duration (the
number of days larvae remain within each length
LO: EGG PRODUCTION OF NORTHERN ANCHOVY
group). It was necessary to compute a weighted
mean of larval production (wPt) because the
number of net tows was not proportional to the
area size: The daily larval production [Ptj , tj ) was
estimated first for each of the three subareas {j -
1: inshore = regions 7 and 11; 7 = 2: nearshore =
regions 4, 8, and 13; and j = 3: offshore = regions
5, 9. and 14) (Fig. 1). The data set (u-Pt , t ) was used
for final fitting of the mortality curve where w Pt =
S Ptj uj , and uj = 0.17, 0.31, and 0.52 for^ = 1, 2,
and 3, the relative area sizes. The unweighted
average age t over three areas was used because
little variation exists among tj's (Fig. 2).
DAILY LARVAL
PRODUCTION
PER 0.
(t)
05
m2 (^Pj) AT AGE t,
(wP,)
1979
PRESERVED
LIVE SIZE
AVE, AGE
DAILY LARVAL
SIZE (mm)
(mm)
(day)
PROD 70.05 m2
2.50
3.26
4 91
0.518
3.75
4.57
8 60
0.121
4 75
5.69
1 1 58
0.0838
5.75
6.27
14 15
0 0665
6.75
7.83
16 4 1
0.0481
7.75
8.87
18.62
0.036
P,= 1.364 (t/3.16)-2-2i'
- 0.45
0 30
O
3
a
o
cc
a.
-I
<
>
<
_i 0.15 -
<
0 00
2.0 3.0 4.0 5.0
AGE/3.16 (t/th)
6.0
FIGURE 2.— Weighted daily larval production (wPt) and age in
days (t) of northern anchovy and the fitted larval mortality curve
based upon Equation (8B) for larvae < 20 d old, 1979.
MODEL
If a cohort of eggs (larvae) is followed and Nt
is defined as the number of eggs (larvae) at age
t (days), then the ratio Nt/No measures the
survival probability at age t: Sit; zit)) = P(T
> t; z (t)). The sample ratio m/no estimates
the survival probability Sit) where zit), the in-
stantaneous mortality rate (IMR), is defined as
lim PU:Si:^l±Al^:>i) If the sample data
At^O A^
{nt,t) are taken from a single cohort and the form
of Sit) is known, both No and zit) can be esti-
mated through nt = no Siit); zit)). Assuming
that the standing stock of eggs and larvae repre-
sents a single cohort (with stable age distribution)
as it ages, then iNt , t ) can be estimated from the
number of eggs and larvae in various stages
(lengths) which are later converted to age in the
sample. Hewitt (1982) conducted a simulation
study to check for possible bias in larval mortality
rate caused by seasonal changes in the intensity of
spawning of northern anchovy which violates the
assumption of a stable age distribution. He found
that mortality was overestimated in the begin-
ning (January-February) of a season when spawn-
ing was increasing and underestimated at the end
(May-July) when spawning was decreasing. When
the larval numbers were accumulated over the
entire season, these two biases tended to cancel
out. Therefore, the stable age distribution is a
reasonable assumption if the egg and larval sam-
ple covers the entire season. To compute larval
mortality for each year, I chose larval data from
January to April to be consistent with the current
sampling scheme. According to Hewitt's study,
the larval mortality may be overestimated. How-
ever, because only young larvae (<8 mm pre-
served length) were considered in the model, the
upward bias is slight. The number of eggs and
larvae at various stages or length classes int, ), as
mentioned in a previous section, was further
adjusted for the duration in days that eggs ( larvae)
remained in a particular stage or length class (d; ),
i.e., Pt, = nt.ldi. The quantity Pt, is egg (larval)
production per day per unit area (e.g., 0.05 m^ ) at
age ti , the average age of eggs (larvae) in the iih
stage (length) class (Farris 1960; Saville 1964;
Harding and Talbot 1973; Ciechomski and Capez-
zani 1973). (In later sections, the subscript / is
dropped, thus iPt, t) is used in place of (P^, , ti).)
The model is based on the form of the mortality
curves of northern anchovy eggs and those for
anchovy larvae, the form of the curve for eggs and
larvae being distinctly different. The daily egg
and larval production Pt is modeled by three
survivorship functions Si, S2, and S.3:
{PoSiit;ziit))
\ t^tc
(3A)
Pt = PoSit) = {Ptc S2 it; Z2 it)\ T > tc)
1 tc<t<20d
(3B)
[Ptk Szit;zzit)\T> tk)
tk < t
(3C)
with the IMR
141
FISHERY BULLETIN: VOL. 83, NO. 2
Zit) ={z2it)
Zzit)
t< tc
tc<t<20d
tk < t
where 52^; zit) \T>tc)-= PiT > t; zit) \T >tc),
tc is the age when the form of IMR changes,
tk is max ti for ti < 20 d where ti is the average
age for the iih. length class.
The quality of larval data for larvae older than 20
d is questionable because older larvae avoid the
net (Hewitt 1982). The forms ofzz{t) and Szit) for
^ > 20 d are unknown at the present time.
Therefore, only the mortality of eggs and larvae
< 20 d old was assessed.
The IMR, zU), relates to the survivorship func-
tion S{t), by definition, in the form of
-I z\(u)du
(4)
-Si(0 t^tc
-Jo-("
)du
rtc
-I zi(u)du
•'0
•'tc
Z2(u)du
tc<t<20
= Siitc)S2(t\T> tc)
= S2it).
The critical age tc was defined as the age before
which z{t) = ziit), after which zit) = Z2it). Pt
and t from larval data were used to estimate both
Ptc and Z2(t) through Equation (3B) after Sit) is
specified. Both larval production iPt^ ) and the
standing stocks of eggs and larvae up to age tc
imtf) were then used to estimate Po and ziit)
through Equation (3A) as below:
and
mt,= r Pf dt = f^' Po Slit; Ziit)) dt (5A)
*'0 •'0
Pt, = PoSiitc;zi{t)).
(5B)
Now I have two Equations (5 A) and (5B) to be
solved simultaneously for the unknowns Po and
the parameters in ziit). An iterative procedure
was used to obtain estimates of Po and ziit).
Clearly, the selection of the function forms of 21 it)
and Z2it) are important in obtaining accurate
estimates of Po and Ptc ■
Anchovy Mortality Curves and
Estimation of Egg Production
Daily egg and larval production per 0.05 m^ and
their ages iPt , t) were estimated for 1979-81
to model the mortality curves Po Siit) and Pt^
S2it\T > tc) (Equation (3)). The egg data were
collected in vertical net tows from 70 m with the
Table L — Daily egg and larval production per 0.05 m^ (Pt) at various ages in days
( t ) sampled from Cal VET and bongo tows, and the estimates of five parameters: egg
production at age zero (Po *. egg mortality id), larval mortality coefficient (/3 ), larval
production at hatching (P/ ) and incubation time in days ( </ ) in CalCOFI regions 4,
7, 8, and 11, January-April 1979-81.
1979
1
Live
standard
length (mm)
1980
1981
Live
ctgnHarH
t
Pt
t
Pt
t
Pt
length
mm)^
. 0.4167
10.79
0.4167
9.34
0.4167
5.64
\
( 0.9167
4.36
0.9167
9.22
09167
7.66
j
; 1.4167
4.91
1.4167
6.34
1.4167
4.87
1
LU
\ 1.9167
4.58
1.9167
4.71
1.9167
6.05
1
0
1 2.4167
6.87
2.4167
5.14
2.4167
4.84
I
<
^ 2.9167
3.63
}
m
/ 3.73
2.64
3.03
2.94
2.26
3 14
3.23
3 03i
4.08
2.39
4.35
2.99
3.59I
"
i
5.91
0.99
6.25
2.10
4.13 1
01
7.69
0.86
8.08
1.84
4.66y
^ <
472
1.96
3.26
3.05
2.35
3.10
5.29
2.97 \
-1
I 8.32
0.48
4.17
5.65
1.04
5.86
1.96
4.00 J
1 11.49
0.35
5.69
8.90
0.49
9.22
1 10
5 13 f
03
0
' 13.90
0.25
6.77
11.47
0.39
11.79
0.72
6.23 )
3
(O
16.24
019
7.83
13 83
0.26
14.01
0.54
7.30 (
0
3
^18.31
0.13
8.87
15.91
17.99
0.21
0.15
16.01
18.22
053
0.41
8.35 }
9,38 7
(B
^c
976
^(2.82)
11.46
(1.27)
6.73
(1.32)
a
0.33
(0.28)
0.38
(0.09)
0.11
(0 13)
P
1.83
(0.14)
1.24
(0.17)
1.19
(0.17)
Pi
3.59
(0.18)
2.51
(0.19)
4.81
(0.42)
tl
3.21
2.96
2.85
' Not weighted by area size
^For both 1980 and 1981 larval data.
^Asymptotic standard error in parentheses.
142
LO: EGG PRODUCTION OF NORTHERN ANCHOVY
CalVET net, and the larval data were collected
with both bongo oblique tows and the CalVET
nets. The egg and larval catches by age group were
standardized, that is, corrected for possible biases
caused by extrusion through the mesh, day-night
difference in avoiding the net, variation in the
amount of water filtered, and the variation of
larval growth rates which is both temperature and
food dependent (Methot 1981; Lo 1983). The stan-
dardized daily egg and larval production esti-
mates per 0.05 m^ sea surface area in CalCOFI
regions 4, 7, 8, and 11 for January-April 1979-81
are given (Table 1, Fig. 3).
The IMR for the egg stage was believed to be
constant, zi(t) = a, (Stauffer and Picquelle foot-
note 6), whereas the IMR for larval stage was
found to be age dependent Z2it) = pit (a Pareto
hazard function, Johnson and Kotz 1970). I first
calculated sample IMR z{ti ) = iPn-i - Pt, )l{ti -
ti-i)IPti which is an approximation of dS{t)ldtl
Sit) at various ^ for 0 < ^ < 20 d using 1980
standardized egg and larval data listed in Table 1.
The 1980 egg and larval production and age data
were further combined so that 2 (^) > 0 for all t.
The relationship between zit) and t determined
the function form of 2(0 (Table 2). The zitYs were
19791
T9801
^ 12.0
H 90 h
O
Q 6.0 |-
O
CC
^ 3.0 h
<
c
o
u
3
■D
O
w
Q.
>•
"(5
"O
0.0
^
12.0
9.0
6.0
3.0
Q I Q Q— I 0.0
J]
19811
o , o
12.0
9.0
6.0
3.0
g IQ Q I 0.0
DD
. ° °.° °
3.0
2.0
1.0
0.0
-1.0
0.0 5.0 10.0 15.0 20.0 0.0 5.0 10.0 15.0 20.0 0.0 5.0 10.0 15.0 20.0
AGE (in days) AGE (in days) AGE (in days)
■J
- a
£ -2.0
3.0
2.0
1.0
0.0 h
-1.0
a
-2.0
3.0
2.0
1.0
0.0
-1.0
' o ' -2.0
■o
o o
0.0 5.0 10.0 15.0 20.0 0.0 5.0 10.0 15.0 20.0 0.0 5.0 10.0 15.0 20.0
3.0
2.0
1.0
0.0
-1.0 I-
J -2.0
-2.0 -1.0 0.0 1.0 2.0 3.0 -2.0 -1.0 0.0 1.0 2.0 3.0 -2.0 -1.0 0.0 1.0 2.0 3.0
In (age) In (age) In (age)
Figure 3. — Daily egg and larval production of northern anchovy per 0.05 m* (Pt) by age in days (t) and their log transformations
(ln(Pt ) ), 1979-81. A linear relationship between ln(Pt ) and t indicates a constant instantaneous mortality rate (IMR) and a curvilinear
relationship between ln(Pt ) and t indicates an age dependent IMR. Squares are egg data and open circles are larval data.
^
AGE (in days)
c
3.0
r
o
a
o
2.0
-
o
3
■o
D D D
D
o
1.0
-
O
Q.
O
>.
0.0
-
(0
o
3
-1.0
o
o
c
-2.0
o
J 1 1 1 1
3.0
D
AGE (in
days)
2.0
1.0
-
a
D D a
3
O
O
0.0
-
1.0
-?.o
-
J 1 1
o
o
o
o
1 1
r-
AGE (in
days)
o
a
o
o
o
1
.._I 1
(
1 1 —
3
CD
O
143
FISHERY BULLETIN: VOL. 83, NO. 2
TABLE 2.— The instantaneous mortality rates of anchovy eggs
and larvae < 20 days (ziti ) ) by age in days (ti ) computed from
the daily egg and larval production estimates (P<, ) and age (<, ),
1980. z(t) = 0.0060 + 1.63/t is the function fitted to the data in
the last two columns for f > 4.5 d.
Daily egg
and larval
production
ti (d) Pti
Pti^
ti =
-Pti ti-ti-^ {ti+ti--[)i2 z(tjy
1
2
3
4
5
6
7
8
9
10
11
12
0.67
1.67
2.60
3.57
5.65
5.91
7.69
8.90
11.47
13.83
15.91
17.99
9.28
5.53
3.70
2.37
1.04
0.99
0.86
0.49
0.39
0.26
021
0.15
3.75
1.83
1.33
2.28
0.05
0.13
0.37
0.10
0,13
0.05
0.06
1.00
0.93
0.97
2.08
0.26
1.78
1.21
2.57
2.36
2.08
2.08
1.17
2.14
3.09
4.61
5.78
6.80
8.30
10.19
12.65
14.87
16.95
0.40
0.36
0.37
0.46
0.18
0.07
0.36
0.08
0.14
0.09
0.14
'Z(f,) = (Pti-^ - Pti)l(ti - ti-A)IPti.
quite constant for egg and larvae <4.5 d old and
decreased thereafter. For t values >4.5 d, the
function z{t) = a + hit fit the data best. Based
upon the function relationship z{t) = bit (the
intercept a is not distinguishable from zero and
thus w^as dropped), I have the IMR z{t):
zit) =
\a
^filt
t ^ tc
tc<t< 20.
(6)
Applying Equation (6) to Equation (4) leads to
Si(0=e~"^ t^tc
-/3
Sit)=<
(7)
S2it) =
-'-"it)
tc<t< 20.
Combining Equations (3) and (7) one has
Pt =
t ^ tc
tc<t<20
-Pt
(8A)
(8B)
To validate both Equations (8A) and (SB), loga-
rithms of P^ and t were plotted: IniPt ) against t
should be a straight line for t '-- tc (Equation (8A) )
and \r\{Pt ) against Xnit) should be a straight line
for tc <t <20 (Equation (8B) ) (Fig. 3). This was
true for egg and larval production from 1979 to
1981. The determination of tc , the age at which
IMR changes, was subjective. Two values of tc
were used: One was the time of hatching or the
duration of incubation (^7) which is temperature
dependent and the other was the average age of
yolk-sac larvae (embryonic period) tc = tys : ^2.5 mm
= age at preserved length 2.5 mm (about 5 d old).
When tc was considered equivalent to the incuba-
tion time (tc = ti ), the egg stages were considered
as one group with constant IMR; and when tc was
equivalent to average age of the yolk-sac larvae
{tc = tys ), egg stages and yolk-sac length class(es)
were considered as one group with constant IMR.
In either case, Pt^ was estimated from the fitted
curve
Pt = Ptj(^^~''M.,Ptc = Pti(^A
-n
Substitution of Equation (7) in Equation (5) gives
'/' Po e ~"^ c/^ - Pod - e-«'0/«
mtc^\^ «>0 (9A)
^c ■ Po a = 0
Ptc =Poe
■ate
(9B)
where mtc is the standing stock of eggs and larvae
up to age tc ■ Equation (9A) divided by Equation
(9B) results in
mf,/Ptc = (e"'"-l)/a = h(a) a>0
tc
a = 0
(10)
where tc = ti or tys and q is the ratio of standing
stock of eggs and larvae up to age tc to the larval
production Pt^- The estimated IMR, a, was ob-
tained by an iterative procedure using Equation
(10). The estimated egg production obtained by
rearranging the terms in Equation (9B):
Po ^ Ptc-e
ate
The approximate variance of a and j8 were com-
puted in the appendix.
TIME SERIES ESTIMATES OF
HISTORICAL EGG PRODUCTION (HEP)
The HEP per 0.05 m^ (Po ) and the egg IMR (a)
for the central stock of northern anchovy in the
first 4 mo of the year, 1951-82, were estimated
based upon Equations (9B) and (10). For years
after 1978, catch data were available for CalVET
and bongo nets, but I chose to use samples from
144
LO: EGG PRODUCTION OF NORTHERN ANCHOVY
bongo nets because only bongo or similar nets (1 m
ring nets) were used for sampling eggs and larvae
prior to 1978.
Two series of HEP estimates were constructed.
Series 1 assumed a constant IMR for the egg stage
with tc = ti , whereas series 2 with tc = tys
assumed a constant IMR throughout the embry-
onic period (Table 3). Both Ptj and Pty, , the daily
larval production at hatching and yolk-sac stage,
were obtained from the fitted line of Equation (8B)
with tc = ti .
Under series 1, nearly half of the egg IMR (a)
were negative (11 out of 24 yr). This was because
the egg IMR depended on the value of q through
Equation (10) where q = mtj/Ptj. However, judg-
ing from Equation (10), q = ti for a = 0. Therefore
for those years where q < ti , egg IMR would be
less than 0. The small ^'s could result from the
underestimated mt/ or overestimated Ptj or both.
The poor results of IMR (a) were likely due to the
underestimation of m</ . As a result, the standing
stock of eggs and that of yolk-sac larvae were
combined into one group in series 2, to eliminate
the negative IMR's.
Table 3.— Two time series of estimated historical egg production {Pq), and egg mortality (a), larval
mortality coefficient (/3), mean egg abundance (mti), mean egg and yolk-sac larval abundance
(mtys '- January- April, and mean larval abundance (La ) per 0.05 m^ 1951-82 with standard error
in parentheses.
'Series
1
' Senes
.2
Larval
Mean
Mean
yolk-sac
Daily
Daily
Mean
egg
Egg
egg
Egg
mortality
egg
larval
larval
production
mortality
production
mortality
coeff.
abundance
abundance
abundance^
Year
Po
a
Po
a
/3
mti
n^tys
La
1951
0.006
0.03
0.012
0.23
0.85
0.02
0.03
0.04
(0.024)
(1.34)
(0.116)
(2.18)
(0.15)
(0.03)
(0.03)
1952
0.002
-0.57
0.017
0.09
0.88
0.02
0.07
0.04
(0.003)
(0.35)
(0.107)
(1.27)
(0.20)
—
(0.01)
1953
0.026
-0.08
0.066
0.19
0.95
0.11
0.21
0.011
(0.019)
(0.20)
(0.180)
(0.54)
(0.10)
(0.03)
(0.03)
1954
0.031
-0.48
0.168
0.12
1.16
0.24
0.61
0.17
(0.026)
(0.26)
(0.188)
(0.24)
(0.07)
(0.08)
(0.08)
1955
0.026
-0.77
0.316
0.07
1.01
0.39
1.27
0 19
(0.028)
(0.32)
(0.393)
(0.26)
(0.17)
(0.12)
(0.14)
1956
0.122
0.33
0.146
0.33
0.88
0.25
0.36
0.11
(0.114)
(0.26)
(0.647)
(0.88)
(0.24)
(0.12)
(0.12)
1957
0.148
-0.12
0.364
0.20
0.94
0.54
1.09
0.26
(0.040)
(0.31)
(0.423)
(0.25)
(0.10)
(0.23)
(0.24)
1958
0.966
0.40
1.274
0.43
0.88
1.61
2.44
0.33
(0.481)
(0.18)
(1.182)
(0.23)
(0.08)
(0.45)
(0.93)
1959
0.444
-0.11
0.992
0.23
1.18
1.47
2.68
0.34
(0.267)
(0.21)
(0.822)
(0.20)
(0.16)
(0.36)
(0.38)
1960
0.678
-0 18
1.765
0.24
1.80
2.78
4.85
0.34
(0.535)
(0.26)
(0.774)
(0.10)
(0.06)
(0.99)
(0.99)
1961
0446
0.25
0.653
0.29
1.55
0.94
1.59
0.26
(0.669)
(0.43)
(0.635)
(0.22)
(0.16)
(0.28)
(0.28)
1962
0.443
-0.18
1.314
0.19
1.08
2.09
4.15
0.67
(0.297)
(0.18)
(1.171)
(0.18)
(0.23)
(0.50)
(0.58)
1963
1.404
0.16
2.275
0.28
0.81
3.57
5.92
0.95
(0.690)
(0.15)
(0.991)
(0.09)
(0.04)
(0.93)
(0.93)
1964
3.681
0.43
4.147
0.42
1.44
6.39
8.55
0.65
(1.956)
(0.15)
(2.681)
(0.13)
(0.21)
(1.80)
(1.81)
1965
0.778
-0.45
4.019
0.19
2.42
6.48
12.78
1.04
(0.559)
(0.21)
(1.176)
(0.06)
(0.12)
(1.75)
(1.75)
1966
3.540
0.26
5.256
0.42
1.84
7.82
10.61
0.80
(1.660)
(0.14)
(1.799)
(0.07)
(0.04)
(2.11)
(2.11)
1969
0.876
-0.42
3.821
0.19
2.15
6.16
12.14
0.67
(0.557)
(0.19)
(1.062)
(0.06)
(0.08)
(1.53)
(1.53)
1972
0.639
-0.09
1.657
0.25
1.73
2.56
4.52
0.62
(0.356)
(0.16)
(0.804)
(0.11)
(0.11)
(0.66)
(0.67)
1975
15.320
0.36
19.691
0.44
1.88
30.06
39.14
0.81
(11.608)
(0.22)
(10.364)
(0.11)
(0.20)
(4.40)
(14.41)
1978
10.524
0.64
10.738
0.59
1.66
13.58
16.60
0.29
(4.566)
(0.15)
(4.484)
(0.10)
(0.10)
(3.67)
(3.67)
1979
4.258
0.36
5.426
0.48
2.22
8.06
10.05
0.39
(2.215)
(0.16)
(2.616)
(0.10)
(0.15)
(2.39)
(2.39)
1980
2.338
0.37
2.671
0.36
1.22
4.12
6 48
0.40
(1.427)
(0.22)
(1.260)
(0.08)
(0.03)
(1.46)
(1.46)
1981
3.95
0.36
4.376
0.38
1.53
6.88
10.29
0.63
(2.658)
(0.24)
(2.084)
(0.08)
(0.03)
(2.70)
(2.70)
1982
1.941
0.15
3.294
0.36
1.81
4.93
7.33
0.46
(1.230)
(0.20)
(1.367)
(0.09)
(0.04)
(1.70)
(1.70)
' Series 1 and 2 are two methods used for estimating daily egg production (Pq)
stage whereas series 2 assumed a constant IMR for egg through yolk-sac larval
^Computed from annual larval abundance for the central subpopulation (Table
Sehes 1 assumed a constant IMR tor egg
stage.
2, Stauffer and Charter 1982).
145
FISHERY BULLETIN: VOL. 83, NO. 2
Under series 2, Po and a were estimated based
upon q = mtys IPtys (Equations (9B) and (10) ), with
tc = tys . The average age of yolk-sac larvae {tys =
^2.5 mm) was 4.7 d. All q's were greater than tys ,
thus as were all positive.
The HEP (Po) for both series have the same
trend: a gradual increase from the early 1950's to
middle 1960's, thereafter fluctuating until 1975
when it reached the peak value at 15.32/day per
0.05 m^ (series 1) or 19.69/day per 0.05 m^ (series
2). From 1978, HEP decreased to the present level
of 1.94/day per 0.05 m^ (series 1) and 3.29/day per
0.05 m^ (series 2) (Table 3, Fig. 4). The approxi-
mate standard error of the estimated HEP (Po)
and egg mortality (a) is large for the early years
and small for the recent years, possibly because
of the poor quality of early egg data, or an insuf-
ficiency of the delta method to estimate the
variance.
For the purpose of verification, HEP (Po) from
the two series based upon the egg-larval mortality
model and the egg production at age 0 estimated
from the current EPM (Stauffer and Picquelle
footnote 6) were compared for 1980-82 where
adequate egg and larval samples were available
(Table 4). The Po's from the two series of HEP and
the current EPM were not significantly different,
nor were the egg mortality rates. However, the
20 r
15
E
o
6
ffi
z
3
10
Daily egg production Pq
'n oi Larval abundance (LCE) La
1950
1960
1970
YEAR
\-r,-v<>r:
-^-M
1980
Figure 4. — Estimates of historical egg production of the central
stock of northern anchovy using the series 2 method (Po ) and the
larval abundance (La) of the larval census estimates, 1951-82.
Table 4. — Daily egg production per 0.05 m^ (Po), egg instan-
taneous mortality (a), egg abimdance (mtj) of northern an-
chovy, and number of tows in) in CalCOFI regions 4, 5, 7, 8, 9,
11, 13, and 14, January-April 1980-82.
1980
1981
1982
Po
a
^0
a
Pq
a
(SE)
(SE)
(SE)
(SE)
(SE)
(SE)
Historical egg production
Series 1
2.33
0.37
3.95
0.36
1.94
0.15
(1.46)
(0.21)
(2.70)
(0.24)
(1.70)
(0.20)
Series 2
2.67
0.36
4.37
0.38
3.29
0.36
(1.46)
(0.08)
(2.70)
(0.08)
(1.70)
(0.09)
Current egg pro-
2.29
0.45
1.82
0.14
1.18
0.15
duction method'
(0.51)
(0.11)
(0.31)
(0.08)
(0.32)
(0.104)
1980
1981
1982
Egg abundance per
(SE)
(Sl)
mti
(S^)
0.05 m^imti)
n
n
n
CalVET (0.333 mm)^
961
3.20
(0.52)
1,134
4.72
(0.72)
992
3.48
(0.62)
Bongo (0.505 mm)
97
4.12
(1.46)
403
6.88
(2.70)
113
4.93
(1.70)
' Picquelle, see text footnote 8.
2 Mesh size.
point estimates of Pq's from the current EPM were
lower than those estimated from the two series.
The reason for the lower values is unknown at the
moment. This could be due to random fluctuation
of the statistics. The current EPM estimates of Po
were much more precise than those derived from
the historical egg-larval mortality model, where-
as the precision of egg mortality rate from both
methods was similar.
As to the estimates from the two series of HEP,
the point estimates of Pq from series 2 were always
higher than those estimated from series 1. Recall
that the assumption of series 2 was that the egg
through yolk-sac larval stage suffers a constant
mortality rate. However, if in fact the yolk-sac
larvae suffer a higher mortality rate than eggs,
the mortality rate of eggs and larvae when com-
bined (series 2) would overestimate egg mortal-
ity as well as egg production (Po) (Equation
(9B)).
DISCUSSION
Historical production (Po) and egg IMR (a) of
the central stock of northern anchovy for the first
4 mo of the year from 1951 to 1982 were estimated
based upon the information of total number of
eggs and yolk-sac larvae per 0.05 m^ and the egg-
larval mortality model. Two series of Po and a
were produced. Series 1 assumed a constant IMR
for only the egg stage whereas series 2 assumed a
constant IMR for the entire embryonic period.
Both series of Po showed the same trend (Table 3,
Fig. 4) with a peak in 1975. The high daily egg
146
LO: EGG PRODUCTION OF NORTHERN ANCHOVY
production estimate (Po ) in 1975 was caused by the
high standing stock of eggs {mti = 30.06/0.05 m^
per m depth) which was more than 10 times that of
other years, and the high egg IMR {a = 0.36)
(Table 3). The high daily egg production in 1975
reflects either a high fecundity (high spawning
frequency) or a high spawning biomass or some
combination of these effects. The present level of
egg production is the same as that in the middle
1960's. Both egg IMR (a) and larval IMR coeffi-
cient )8, 2(0 = pit, vary from year to year (Fig. 5).
In addition to providing a 24-yr time series of
HEP for the northern anchovy, two important
conclusions can be drawn from this analysis:
1. The form of IMR of eggs (and yolk-sac larvae) is
different from that of older larvae (6-20 d).
2. Egg production is a better index of stock
abundance than is the standing stock of larvae.
Little doubt exists that mortality rates change
sometime between the hatching of the eggs and
the onset of feeding. Analysis of the daily egg and
larval production by age for 1979-81 (Fig. 3)
suggested a constant IMR for eggs (or eggs and
yolk-sac larvae) and an age-dependent IMR of
Pareto form for older larvae {z{t) = fB/t for tc < t <
20 d) (Table 2). The age tc in Equation (3) could be
2.5 r
2.0
- 1.5
I
U
A
V
1 /
I;
H
Larval IMR coefficient (/3)
1950
1960
1970
1980
YEAR
Figure 5. — Estimated egg instantaneous mortality rate (EMR)
(a) from series 2 method of estimating egg production and the
larval mortality coefficient (y3) of the central stock of northern
anchovy, 1951-82.
considered to mark the end of the critical period
after which mortality decreases (Ahlstrom 1954;
Marr 1956; Farris 1960; Saville 1964). Series 1
assumed tc = incubation time and series 2 as-
sumed tc - average age of yolk-sac larvae. From
the existing data, I could not ascertain which
assumption was the more likely, but it was evi-
dent that larvae at hatching or near first-feeding
(yolk absorption) suffer higher mortality than do
older larvae.
The HEP (Po) is certainly preferable to larval
standing stock (larval census estimate - LCE) for
use as an index of spawning biomass. Egg produc-
tion is related to the spawning biomass through
Equation (2), i.e., Po = Ba'C, where the propor-
tionality C is the reproductive output (R-F-EIW).
If the reproductive output remains constant be-
tween years, as shown by 1980-82 anchovy data
(Picquelle^), the HEP will be an unbiased index of
the spawning biomass. The LEG assumes Ba -
K-La where La is the larval abundance and K is
a constant proportionality (Smith 1972; Stauffer
and Charter 1982) (Table 3, Fig. 4). Thus to
provide an unbiased index of biomass, the method
requires that not only the reproductive output be
constant from year to year but also the egg and
larval mortality must remain constant as well.
Using Equation (8), the larval abundance (age
< 30 d old) can be written as
30
La=J Ptdt
'ti
I PoSit;z(t))dt
•>ti
'ti
= Ba
, - atl tl
/3
-k w\
where g{a, /3, ti) —'
for /3 7^ 1
.e-«'^(ln30- \nti)
a is the egg IMR and /3 is the larval mortality
coefficient.
The larval abundance (La) is proportional
to the spawning biomass (Ba) with constant
proportionality only if the reproductive output
*S. J. Picquelle, Statistician, Northwest and Alaska Fisheries
Center, National Marine Fisheries Service, NOAA, 2725 Mont-
lake Boulevard E, Seattle, WA 98112, pers. commun. July 1983.
147
FISHERY BULLETIN: VOL. 83, NO. 2
(R-F-E/W) and the egg and larval mortality rates
through the function g {a, 13, tj) remain constant
from year to year It is clear that from 1951 to 1982
time series (Table 3) that the assumption of
constant egg and larval mortality has not been
met by the central California anchovy population.
The HEP requires constant reproductive output.
The validity of this assumption can only be tested
with future data.
In addition to the ichthyoplankton data, several
other indices of anchovy biomass exist: acoustic
trawl surveys conducted by California Depart-
ment of Fish and Game, aerial survey records from
aircraft associated with the fishery, catch-effort
analysis (CPUE), and cohort analysis from the
catch of the United States and Mexican fishery. In
a recent management plan, all of these indices
except cohort analysis have been calculated and
compared with the time series of egg production
presented in this paper (MacCall et al.^). The
estimates of egg production covaried with these
other indices from year to year and appeared to be
the most consistent index of spawning biomass
among these indices (Table 5).
Selection of the appropriate method for esti-
mating biomass depends upon the data availabil-
ity and knowledge of the growth of eggs and
larvae. If nothing is known of the age of eggs and
larvae and no information exists on reproductive
parameters, the LCE is the only method available
'MacCall, A. D., R. D. Methot, D. D. Huppert, H. W. Frey, and
O. Mathisen. 1983. Northern anchovy second draft revised
fishery management plan incorporating DEIS/RIR.
Manage. Counc.
Pac. Fish.
Table 5. — Correlations among various indices of an-
chovy spawning biomass. Upper value is correlation
coefficient, lower value is number of observations. (Repro-
duced from table 4.3-2 of MacCall et al. (text footnote 9). )
Historical egg production
0.458
Larval
(23)
census
0.807
0.708
Acoustic
(8)
(7)
survey
0.818
0.327
0.659
Aerial
(9)
(9)
(9)
index
0.791
0.004
0.512
0.379 Spring
(4)
(4)
(10)
(9) CPUE
0.395
0.865
0.290
0.655 0.256
Fall
(4)
(4)
(10)
(10) (9)
CPUE
Spawning biomass index
Consistency'
Rank
Historical egg production
0.654
1
larval census
0.480
5
Acoustic survey
0.606
2
Aerial index
0.583
3
Spnng CPUE
0.388
6
Fall CPUE
0.517
4
'Consistency is average of correlation coefficients.
although subject to major biases. If egg and larval
age data exist but no data on reproductive param-
eters are available, then the HEP is the preferable
method. The EPM is the best method; it requires
not only knowledge of egg mortality but accurate
estimates of adult reproductive parameters as
well. In many time series, both growth and abun-
dance of eggs and larvae are available but repro-
ductive parameters are not. In these cases, the
HEP is probably the most accurate means of
creating a historic time series of biomass.
ACKNOWLEDGMENTS
I thank John Hunter, Roger Hewitt, Paul
Smith, Rick Methot, Alec MacCall, Jay Barlow,
National Marine Fisheries Service; David Farris,
San Diego State University; Grace Yang, Uni-
versity of Maryland; two referees for reviewing
the manuscript and making valuable suggestions.
I also thank Barry Finzel, Cynthia Meyer, Carol
Miller, and Richard Charter for compiling his-
torical egg and larval data files, and Mary DeWitt
and Debra BrowTi for typing the manuscript.
LITERATURE CITED
AHLSTROM, E. H.
1954. Distribution and abundance of egg and larval popu-
lations of the Pacific sardine. U.S. Fish Wildl. Serv.,
Fish. Bull. 56:83-140.
1968. An evaluation of the fishery resources available to
California fishermen. In D. Gilbert (editor), The future
of the fishing industry of the United States. Univ. Wash.
Publ. Fish. New Ser. 4:65-80.
BEVERTON, R. J. H., AND S. J. HOLT.
1965. On the dynamics of exploited fish populations.
Fish. Invest. Minist. Agric. Fish. Food (G.B.) Ser. II, 19:
1-533.
BISSEL, A. F
1972. A negative binomial model with varying element
sizes. Biometrika 59:435-441.
BURD, A. C, AND W. G. PARNELL.
1972. The relationship between larval abundance and
stock in the North Sea herring. Rapp. R-v. Reun. Cons.
Perm. int. Explor Mer 164:30-36.
CIECHOMSKI, J. D. DE, AND D. A. CAPEZZANI.
1973. Studies on the evaluation of the spawning stocks of
the Argentinean anchovy, Engraulis anchoita, on the
basis of egg surveys. Rapp. R-v. Reun. Cons. Perm. int.
Explor. Mer 164:293-301.
COLTON, J. B.
1959. A field observation of mortality of marine fish larvae
due to warming. Limnol. Oceanogr. 4:219-222.
CUSHING, D. H.
1973. Dependence of recruitment on parent stock. J.
Fish. Res. Board Can. 30:1965-1976.
Eager, E. W.
1973. Estimation of mortality coefficients from field sam-
148
LO: EGG PRODUCTION OF NORTHERN ANCHOVY
pies of zooplankton. Limnol. Oceanogr. 18:297-301.
KARRIS, D. A.
1960. The effect of three different types of growth curves
on estimates of larval fish survival. J. Cons. Perm. Int.
Explor Mer 25:294-306,
HARDING, D., AND J. W. TALBOT.
1973. Recent studies on the eggs and larvae of the plaice
(Pleuronectes Platressa L.) in the southern Bight. Rapp.
P-v. Reun. Cons. Perm. int. Explor. Mer 164:261-269.
HEWITT, R. P
1982. Spatial pattern and survival of anchovy larvae:
implications of adult reproductive strategy. Ph.D. The-
sis, Univ. California, San Diego, 187 p.
1983. Roll, heave and vertical ichthyoplankton tows.
Ocean Sci. Eng. 8(1):41-51.
HUPPERT, D. D., A. D. MACCALL, G. D. STAUFFER, K. R.
PARKER, J. A. MCMILLAN, AND H. W. FREY.
1980. California's northern anchovy fishery: Biological
and economic basis for fishery management. U.S. Dep.
Commer,, NOAA Tech. Memo., SWFC-TM-NMFS-1,
234 p.
JOHNSON, N. L., AND S. KOTZ.
1970. Distributions in statistics: continuous univariate
distributions. Houghton Mifflin Co., Boston, 300 p.
LO, N. C. H.
1983. Re-examination of three parameters associated with
anchovy egg and larval abundance: Temperature depen-
dent of incubation time, yolk-sac growth rate and egg
larva retention in mesh nets. U.S. Dep. Commer,
NOAA Tech. Memo., SWFC-TM-NMFS-31, 32 p.
Marr, J. C.
1956. The critical period in the early life history of marine
fish. J. Cons. Perm. Int. Explor. Mer 21:160-170.
METHOT, R. D.
1981. Growth rates and age distributions of larval and
juvenile northern anchovy, Engraulis mordax, with infer-
ences on larval survival. Ph.D. Thesis, Univ. California,
San Diego, 203 p.
Murphy, G. I.
1966. Population biology of the Pacific sardine (Sardinops
caerulea ). Proc. Calif Acad. Sci., Ser. 4(34):l-84.
Parker, K.
1980. A direct method for estimating northern anchovy,
Engraulis mordax, spawning biomass. Fish. Bull., U.S.
78:541-544.
Saville, a.
1964. Estimation of the abundance of a fish stock from egg
and larval surveys. Rapp. P-v. Reun. Cons. Perm. int.
Explor. Mer 155:164-170.
SEBER, G. a. F
1973. The estimation of animal abundance and related
parameters. Hafner Press, N.Y., 506 p.
SMITH, P E.
1972. The increase in spawning biomass of northern an-
chovy, Engraulis mordax. Fish. Bull., U.S. 70:849-874.
Smith, P E., and S. L. Richardson.
1977. Standard techniques for pelagic fish egg and larva
surveys. FAO Fish. Tech. Pap. 174, FIR/T175, 100 p.
STAUFFER, G. D., AND R. L. CHARTER.
1982. The northern anchovy spawning biomass for the
1981-82 California fishing season. CalCOFI Rep. 23:
15-19.
THEILACKER, G. H.
1980. Changes in body measurements of larval northern
anchovy, Engraulis mordax, and other fishes due to
handling and preservation. Fish. Bull., U.S. 78:685-692.
ZWEIFEL, J. R., AND P E. SMITH.
1981. Estimates of abundance and mortality of larval
anchovies (1951-75): application of a new method. Rapp.
P-v Reun. Cons. Perm. int. Explor. Mer 178:248-259.
APPENDIX
The approximate variances of 6c and Pq were derived from the delta method
(Seber 1973):
var[fixi,..., xi)]= X
1 = 1
_d_
dxi
fixi,..., XI )
warixi )
+ 2S -^fixi,...,xi)-^f{xi,...,xi)coyixi,xj)
i<j dxi dxj
Exi, i = i,...,I
var (a) was computed based upon Equation (10), i.e.,
•(9)^(^)'var(a).
var(
149
FISHERY BULLETIN: VOL. 83, NO. 2
Thus var(n:) = wariq)
= warimtrlPtc)
_ var(mfc) + g^ var(Ac) -2qcov{mtc,Ptc)
Ptc'
[aV {e«'
'■(a^c-D + l
1^]
where cov {mtc, Ptc^ was estimated from the 1951-82 time series. Var (Po) was
computed based upon Equation (9B)
Po = Ptce""''
var(Po)=-(^
da
%ar(a)+^^^o
\^Ptc
waiiPtr ) + 2
/dPo\ (m
\da) \dPt,
cov(Ac , a)
a,^^c
- e^a/c [^j;^2 p^^2 ^^j.^^) + var(Ac ) + 2Ac -tc -covCAe , a)]
where cov (Ac . «) was estimated from the 1951-82 time series.
150
VERTICAL STRUCTURE OF NEARSHORE PLANKTON
OFF SOUTHERN CALIFORNIA:
A STORM AND A LARVAL FISH FOOD WEB
M. M. MuLLiN, E. R. Brooks, F. M. H. Reid,
J. Napp, and E. E Stewart'
ABSTRACT
Samples of zooplankton and phytoplankton were taken at 5 m depth intervals in the upper 50 m of
water off Dana Point, California, in the spring of 1980, just before and just after a local storm. Most of
the 43 zooplanktonic taxa, many phytoplanktonic taxa, and chlorophyll were vertically stratified. After
the storm, naupliar copepods, chlorophyll, and a few phytoplanktonic taxa were more abundant, and
several zooplanktonic taxa were more concentrated in the upper layers. The storm did not decrease the
vertical stratification of larval fish food, so the feeding environment after the storm was at least as
favorable as that before the storm, but larval fish were less abundant.
Studies in the laboratory have provided data on
the kinds and abundances of food which are re-
quired for survival and growth of some types of
zooplankton found in the surface waters of the
Southern California Bight (e.g., Mullin and
Brooks 1970; Paffenhofer 1976) and of the larvae of
the anchovy, Engraulis mordax, (e.g.. Hunter
1976; Lasker et al. 1970) and jack mackerel,
Trachurus symmetricus , (Devonald 1983). The an-
chovy has overwhelmingly dominated the larval
fish assemblage of the area in recent years (e.g.,
Gruber et al. 1982). Direct experimentation
(Lasker 1975) and indirect comparison of
metabolic requirements and observed concentra-
tions of likely food (Mullin and Brooks 1976; Cox et
al. 1983) have shown examples of situations where
only in layers or patches of anomalously high con-
centration of food can larval fish or copepods ob-
tain enough nutrition to grow. Field data on verti-
cal distributions indicate that extensive, sharply
defined layers with elevated abundances of
phytoplankton often exist within the euphotic
zone (e.g., Cullen and Eppley 1981, for chlorophyll;
Kiefer and Lasker 1975, for Gymnodinium splen-
dens; Cullen et al. 1982, for several species).
There is also more indirect evidence of the im-
portance of unusually rich layers of food for the
survival and growth of planktonic predators: The
greater size of "wild" copepods relative to those
raised in the laboratory (Mullin and Brooks 1970),
the limitation of egg production of a copepod popu-
lation (Checkley 1980b), and the failure of year
classes of anchovy when storms or upwelling were
thought to disrupt layers of food (Lasker 1981).
However, direct field evidence concerning starva-
tion or growth limitation by food of larval anchovy
is both limited and contradictory (Arthur 1976;
Methot and Kramer 1979; O'Connell 1980).
The population of the large copepod, Calanus
pacificus, is sometimes concentrated in those
layers where autotrophic phj^oplankton is most
abundant (Mullin and Brooks 1972, 1976). How-
ever, there also are cases where no such correla-
tions were found (Mullin and Brooks^) or where
Calanus and other herbivores actively avoided a
layer of abundant dinoflagellates (Fiedler 1982),
and where feeding in such a layer was depressed
relative to other parts of the water column (Fiedler
1982; Huntley 1982). In the present study we
examined the vertical relations between several
zooplanktonic taxa and chlorophyll, a measure of
the autotrophic, phytoplanktonic biomass. Since
the nutrition of zooplankton governs growth and
fecundity, the vertical relations between zooplank-
ters and their food can affect the future supply of
food for fish if the zooplankton is food-limited.
Small-bodied species of zooplankton (or larval
stages of larger species), some large-celled, non-
thecate dinoflagellates, and protozoans were of
particular interest as representing potential lar-
'Institute of Marine Resources, A-018, Scripps Institution of
Oceanography, University of California — San Diego, La Jolla,
CA 92093.
Manuscript accepted May 1984.
FISHERY BULLETIN: VOL. 83, NO. 2, 1985.
^Mullin, M. M., and E. R. Brooks. 1976. Unpubl.data. In-
stitute of Marine Resources, Scripps Institution of Oceanog-
raphy, University of California — San Diego, La Jolla, C A 92093.
151 - 7fi
FISHERY BULLETIN: VOL. 83, NO. 2
val fish food. Larger zooplankters represent poten-
tial competitors with larval fish for dinoflagellate
and protozoan prey, or even potential predators of
the larvae themselves.
The vertical distribution of larval anchovy
within the euphotic zone is less well known than is
that of zooplankton, particularly with respect to
the vertical distribution of their food sampled con-
currently, because larval fish are so rare that nets
with large capacity must be used to capture sig-
nificant numbers of them. It was partly to provide
such data that we conducted the present study
concurrently with sampling by National Marine
Fisheries Service personnel from a second vessel
to determine the vertical distribution of larval
fish. Records of water temperature, concentration
of chlorophyll, and abundances of phytoplankton
at the depth of the chlorophyll maximum were also
taken from the second vessel, and are compared
with our results below.
We were fortunate, intellectually if not physi-
cally, to sample a fixed location before and after
passage of a local storm (cf. Lasker 1975), and we
therefore tried to examine the potential impor-
tance for the food web of turbulent rearrangement
of vertical distributions. We looked for changes
coincident with the storm in overall abundances
and in the intensity and patterns of vertical
stratification of many planktonic taxa, and in cor-
relations between the vertical distributions of
predators and their potential prey. We then made
predictions concerning the implications of these
changes for the nutrition of larval fish.
METHODS
From mid-March to mid-April 1980, spawning
of anchovy was concentrated in the inner portions
of the Southern California Bight, apparently con-
fined by plumes of cool water extending south of
Point Conception beyond Santa Catalina and San
Clemente Islands (Lasker et al. 1981). Between 29
March and 6 April, we took 13 vertical series of
samples at 5 m intervals in the upper 50 m of water
at lat. 33°28.5'N, long. 117°46.7'W (CalCOFI sta-
tion 90.28, 3.5 km offshore from Dana Point,
California), where the depth of water was —350 m,
using the pump and hose described by Mullin and
Brooks (1976) and Mullin (1979). Almost all of the
larval anchovy at this station occurred in the
upper 40 m (Pommeranz^). Because of the re-
stricted area of the anchovy's spawning at the
time, our results may be indicative of conditions
experienced by a considerable fraction of the lar-
vae produced in late March-early April in the
Bight. The volume of water filtered per quantita-
tive sample of zooplankton was typically 200-300 1;
for comparison, the rate at which a 1.5 cm larval
anchovy searches water for food is about 5 1/h
(Hunter 1972). In addition to quantitative, net-
concentrated samples of zooplankton and
fiberglass-filter concentrated samples of
chlorophyll, we preserved unconcentrated sam-
ples of water in 59c v:v Formalin"* for counts of
phytoplankton, and filtered nonquantitative sam-
ples of net-caught zooplankters onto fiberglass fil-
ters which were then frozen for later analysis of
plant pigments in the guts.
One profile was completed during 0900-1400 h
and another during 2030-0030 h each 24-h day
except from 0000 on 1 April to 0900 on 3 April,
when a local storm kept us in port. Profiles 1-6
were "prestorm", 7-13 "poststorm".
Analytical procedures for chlorophyll and net-
caught zooplankton followed Mullin and Brooks
(1976) and Mullin (1979). All recognizable zoo-
plankters were enumerated. For phytoplankton
and protozoans, we prepared a physically inte-
grated sample for each profile by mixing 50 ml of
water taken from each of the 11 depths. Fifty ml of
this integrated sample were settled for 48 h, and
cells were counted using the Utermohl method.
For cells —20 /u,m or greater (equivalent spherical
diameter), half the settled material was counted at
160 X magnification (equivalent to a 25 ml sam-
ple); for cells <20 /xm, one row across the diameter
of the settling chamber was studied at 625 x mag-
nification (0.33 ml).
Subsequently, 50 ml aliquots from each depth
for each profile were settled at least 24 h and
examined. Since the flora was very diverse, we
selected a short list of taxa using the following
criteria: Cells were clearly identifiable even
after preservation in Formalin, present in suffi-
cient numbers to provide reliable data, and (with
several exceptions) of interest as possible larval
fish food. We believe that all taxa usable as food
were satisfactorily preserved and counted. Most of
the cells were counted using 160 x magnification,
usually in an equivalent of a 12.5, 25, or 50 ml
sample. Chaetoceros spp., Nitzschia spp., and
Emiliania {Coccolithus ) huxleyi were enumerated
'Tilman Pommeranz, Institut fiir Meereskunde, Kiel, West
Germany, pers. commun. 1984.
■"Reference to trade names does not imply endorsement by the
National Marine Fisheries Service. NOAA.
152
MULLIN ET AL.: VERTICAL STRUCTURE OF PLANKTON OFF CALIFORNIA
at 250 X, usually in one or two rows across the
settling chamber (1.13 or 2.3 ml). A precipitate
developed in certain samples after several months
storage, so profiles 1, 2, 8, and 12 could not be
included in the analysis based on discrete depths;
profile 13 was also excluded in order to balance the
data.
To measure the amount of plant pigments in the
guts of selected zooplanktonic taxa, we used an
approach similar to that of Mackas and Bohrer
(1976). In a darkened room, the frozen contents of
each fiberglass filter were washed onto a circle of
Nitex mesh (180 /xm) and then sucked dry. The
mesh disk was transferred to a Petri dish, wetted,
and then examined visually using low magnifica-
tion and low-intensity green light. Organisms
were removed singly from each mesh, dipped in
filtered seawater, and then sorted into scintilla-
tion vials sitting in an ice bath and containing
small amounts of 90% reagent grade acetone.
After obtaining enough organisms, we in-
spected the contents of each vial visually to insure
that they were taxonomically homogeneous and to
record the number of individuals present. The con-
tents were then homogenized with a motor-driven
teflon pestle in a glass grinding vessel to which
MgCOg and acetone were added. The homogenate
was transferred by several rinses to a 15 ml
screw-cap test tube and the volume was adjusted
to 10 ml. All test tubes were stored in a light-tight
container in a refrigerator for —1 h, after which
the homogenates were given an additional half
hour to extract and to warm to room temperature.
The homogenate from each tube was first mixed
and then filtered through a fiberglass filter to re-
move the MgCOs and animal tissue/exoskeleton.
The amounts of chlorophyll a and phaeopigments
in the filtrate were determined fluorometrically
(Holm-Hansen et al. 1965) using a Turner Model
111 fluorometer equipped with a high-sensitivity
door.
In order to evaluate the method, we collected
copepods by oblique net hauls over the Scripps
Canyon (—2 km from shore), sorted them, and
placed them in filtered seawater to starve for 18-24
h. On other occasions copepods were similarly col-
lected, starved to void their guts, and then allowed
to become satiated on mixtures of cultured phyto-
plankton. All animals were frozen before pigment
extraction.
To assess (ex post facto) whether preservation of
pigments by freezing was complete, we took
oblique net tows (total duration ~2 h) over Scripps
Canyon. Each net haul was immediately strained
through pieces of Nitex (<100 ixm) netting and
then quick-frozen using dry ice. Twelve samples
thus obtained were stored in the same freezer as
the cruise samples and processed in a similar
manner. One sample (To) was processed the same
day, the other samples at various times thereafter
up to 700 d. We were unable to detect a decrease in
total pigments over this time period by linear re-
gression, and therefore believe the freezing to be
adequate.
The first group of hypotheses we wished to test
concerned temporal changes in patterns of verti-
cal distribution. One general procedure was to
treat several samples of one kind (e.g., all diurnal
samples from a particular depth before the storm)
as replicates accounting for variability due to
technique and to real patchiness, and then to look
for significant differences through an analysis of
variance (ANOVA) on log-transformed abun-
dances. Details are in Table 1. This was done for
those taxa for which the variances (of log-
transformed data) were homogeneous by
Bartlett's and/or Cochran's tests (Dixon and Mas-
sey 1957). Where the variances were heterogene-
ous (i.e., P < 0.01 of homogeneity), we tested
analogous hypotheses through nonparametric
tests, as indicated in Table 2. Taxa for which it was
necessary to employ the battery of nonparametric
tests are indicated by asterisks in the Appendix.
A second group of hypotheses concerned correla-
tions between measured properties, such as the
concentration of chlorophyll and the abundance of
a particular taxon. These hypotheses were tested
by nonparametric correlation or concordance
tests; details are in Section C below We also tested
for changes in overall community composition by
constructing dendrograms based on rank differ-
ence correlation coefficients. All nonparametric
tests are from Tate and Clelland (1957).
RESULTS
The overall abundances and vertical distribu-
tions of 43 zooplanktonic and 18 phytoplanktonic
and protozoan taxa in the upper 50 m are shown in
the Appendix, based on median abundances for
diurnal and nocturnal profiles, before and after
the storm, together with the distributions of
chlorophyll. Depending on dietary preferences of
the visually feeding larval anchovy (e.g., Arthur
1976), some combination of the diurnal distribu-
tions of several taxa represents the "typical" verti-
cal distribution of larval fish food (see Section D
below). We will discuss results in the following
153
FISHERY BULLETIN; VOL. 83, NO. 2
Table l. — Three-way analysis of variance on log-transformed abundances (m~ ) (see Appen-
dix). To balance the sampling design, the 13th profile for zooplankton and chlorophyll (6 April)
was omitted from the analysis. A significance level of P < 0.01 was used to compensate for
multiple testing of the same hypotheses for many taxa.
Classification of sample
1. Day vs. night
2. Before vs. after storm
3. Deptfi
Interaction 1 x 2
Interaction 1 x 3
Interaction 2x3
Interaction 1x2x3
Significance of ANOVA probably indicates:
Taxon migrated dielly from below 50 m into sampled range. Diel variation in
avoidance of hose intake would create spunous significance. For very short-lived
taxa, strong diel variation in birth, death, or maturation could also cause significant
differences.
Taxon changed in mean abundance coincident with storm. Cannot distinguish
advective from biological causes.
Taxon was nonuniformly distributed 0-50 m in a consistent manner (or avoidance
vaned with depth).
Taxon migrated dielly into sampled range from below 50 m before or after storm, but
not both.
Taxon had some kind of diel migration. If classification 1 was not significant, migra-
tion occurred within upper 50 m. Variation in avoidance both dielly and with dep'h
could create spunous significance.
Depth distribution of taxon changed coincident with storm. Change could either
result in greater or lesser uniformity with depth or a change in depth of the maximum.
Pattern of diel migration of taxon changed coincident with storm.
Table 2. — Questions, hypotheses, and nonparametric statistical tests for taxa with heterogeneous variances (designated by
asterisks in Appendix). A significance level of P < 0.01 was used to compensate for multiple testing.
Question
Null hypothesis (Hq)
Test and comments
No difference in abundance
(m~^), day vs. night.
No difference in depth of
median animal, day vs.
night.
No difference in abundance
(m ~^) before vs. after
storm.
No difference in range
of abundances (m~^)
0-50 m.
No relation between
strength of rank
correlation between two
profiles and timing of
these profiles with
respect to the storm.
What taxa migrated dielly
from below 50 m into
the sampled range?
What taxa migrated dielly
within the upper 50 m?
What taxa changed in
abundance coincident
with the storm?
What taxa became
more or less uniform
In vertical distribution
following the storm?
Did community
structure change
coincident with
the storm?
Mann-Whitney U test for difference in median abundances (m ) of each taxon, day vs. night.
Compare to ANOVA classification 1 .
For each taxon for which H,, 1 is accepted. Mann-Whitney U test for difference in depth of median
animal, day vs. night. Compare to ANOVA interaction 1 x 3.
For each taxon for which Ho 1 is accepted. Mann- Whitney U test for difference in median abun-
dances (m ~^), 29 March-1 April profiles vs. 3-6 April profiles. Compare to ANOVA classification 2.
For each taxon for which Ho 1 is accepted, short-cut F test on ranges in median profiles
(Appendix). Compare to ANOVA interaction 2x3.
From abundances (m ) of each taxon in each profile, profiles are grouped by dendrogram based
on rank correlation coefficients of abundances.
categories: A. Zooplankton; B. Phytoplankton
and protozoa; C. Relations between zooplankton
and phytoplankton; and D. Food for larval fish.
Figure 1 shows that the storm was not remark-
able in the wind records from San Diego, but was
quite apparent in the winds at San Clemente Is-
land and in records of wave height at La Jolla and
Oceanside. The generally lower wind speed and
greater variability in speed and direction within
each day at San Diego than at San Clemente Is-
land are general phenomena (Dorman 1982). The
wind at San Diego is probably more typical of the
actual wind off Dana Point, while the San
Clemente winds are more typical of the offshore
condition generating the swell arriving there.
Since the energy appearing as wind-induced tur-
bulence increases as the cube of the wind speed, a
doubling of wind speed increases turbulent energy
eightfold.
Following the storm, surface temperatures and
the thermal gradient in the upper 30 m were re-
duced at the sampling location off Dana Point,
though the change in thermal gradient was not
apparent until more than a day after the storm,
and water temperatures at La Jolla were higher
after the storm (Fig. 1). Minimal thermal gra-
dients in the upper 30 m were also observed by the
second vessel working at Dana Point on the night
of 4-5 April. Though there was pronounced day-
to-day variation in depths of isotherms, isotherms
tended to be shoaler after the storm. For example,
the poststorm median depths of 12°, 13°, and 14°C
isotherms all were shoaler by 4.7-5.9 m than were
the prestorm median depths (Pommeranz foot-
154
MULLIN ET AL,: VERTICAL STRUCTURE OF PLANKTON OFF CALIFORNIA
29 30 31
Thunderstorm Rain'
I 2 3 4 5 6
I I I I I
>C,Ji^, "■■^^ ■ i^^
Wind
Direction
N
W— I— E
Rom
Winds at Lindberg Field, San Diego
Winds at San Clemente Island
[10
m/sec
<_) 2 -
In Port
O
o
0
17
16
15 h
Temperature Difference, Onn — 30nn, Dana Point
1 1 1 1 1 1 r
Mean Temperature, 0 and 5m,
Dana Point x
■In Port
Mean Water Temperature, Scripps Pier, La Jolla
2 -
E I -
0
Swell Height at Scripps _|
Pier, La Jollo
I I I.I
2
e I
0
IIMIIIIMII
Significant Wave Height,
Oceanside
lliiiiiiiilinilll
29 30 31 ' I 2 3 4 5 6
MARCH APRIL
Figure l. — winds, water temperature, temperature gradient,
and wave height at Southern California locations during this
study. For temperature, dots are Dana Point, x's are La Jolla.
Wind direction is the direction from which the wind is blowing.
note 3), and these differences were each significant
by rank sum test (P < 0.05). This is not what one
would expect from simple mixing, in which the
nearsurface isotherms should shoal and the
deeper isotherms deepen.
A. Zooplanktonic Taxa and
Community Structure
We examined statistically the data on zoo-
plankton summarized in the Appendix for
answers to several questions concerning temporal
changes in the distributions, using the ANOVA or
nonparametric tests summarized in Tables 1 and
2. Daytime vertical distributions of many of these
taxa off Southern California in late spring and fall
are given by Fiedler (1983). As noted in the tables,
there are potential ambiguities in the interpreta-
tion of even statistically significant results, such
as the difficulty in distinguishing diel migration of
a zooplanktonic taxon from a diel variation in its
capability to avoid capture by the pump. More
serious, and applicable to phytoplankton as well as
zooplankton, is the impossibility of distinguish-
ing between 1) biological changes caused directly
by the storm (such as vertical redistribution,
changes in behavior, or changes in the balance
between birth and death of a taxon) and 2) storm-
driven advection into the area of water with
planktonic populations differing in abundances or
behavior from those present prior to the storm, but
neither the original nor the replacement popula-
tions having themselves changed in these proper-
ties. Advection undoubtedly occurred before, dur-
ing, and after the storm; the issue is whether
biologically caused changes associated with the
storm occurred as well.
L Diel Vertical Migrations
Based on results from ANOVA classification 1
(Table 1) or nonparametric Test 1 (Table 2), the
taxa migrating into the upper 50 m from deeper
water at night were the copepodites and adults of
Pleuromamma and Metridia. These are real mi-
grations, since sampling the water column of the
Southern California Bight to greater depths re-
veals a change in depth of maximal abundance
from below 100 m by day to within the upper 50 m
at night (Esterly 1912; Enright 1977; Brooks and
Mullin 1983). Euphausiid furcilia were also more
abundant at night than by day.
Of the remaining zooplanktonic taxa (which did
not have significant diel variation in total abun-
dance within the upper 50 m), the populations of
female, CV, and CIII Calanus, euphausiid calyp-
topes, and cyphonautes larvae were centered sig-
nificantly higher at night than by day in the water
column. Again, these results are consistent with
results of sampling to greater depths in nearby
waters (Esterly 1912; Enright and Honegger 1977;
Mullin 1979; Brooks and Mullin 1983). Other taxa
probably belonging to this category of behavior
are adult Rhincalanus and Eucalanus (numbers
too small for reliability). Curiously, when tem-
poral changes are removed from the analysis
(ANOVA classification 3 (Table 1) ), female and CV
Calanus a-nd SiduXt Rhincalanus , Eucalanus, and
Metridia tend to be uniformly distributed in the
upper 50 m.
2. Changes Following the Storm
Several taxa were significantly different in
abundance following the passage of the storm
[ANOVA classification 2 (Table 1) or nonparamet-
ric Test 3 (Table 2)], and most of these were larval
155
FISHERY BULLETIN: VOL. 83, NO. 2
forms. Acartia, "Paracalanus" , and "other" nau-
plii were significantly more abundant in 3-6 April
samples than in the prestorm set (Fig. 2), while
the abundance of larval fish in our samples de-
creased, as did that of adult and copepodid
Oithona. An increase in abundance of appen-
dicularians was almost significant. From the point
of view of a larval or young juvenile fish, there
were more items of desirable food {copepod nau-
plii and fewer siblings after the storm. No change
was detected in those taxa (adult Labidocera and
Corycaeus, chaetognaths) likely to be important
zooplanktonic predators on larval anchovy.
Some of these changes appear to be continua-
tions of trends evident before the storm (Fig. 2).
However, the fact that larval copepods of several
types were more abundant following the storm
suggests that the storm directly or indirectly
stimulated reproductive activity, though stimula-
tion of hatching of benthic eggs (cf. Uye and
Fleminger 1976; Landry 1978) or advection of
populations from an area of greater fecundity
250
A
200
-
/\
150
- /V
Vv
100
^
Adult and
Copepodid
50
—
"Paracalanus"
0
1 1 1
1 1 1 1
-| 300
200
100
Nauplior
"Paracalanus
ruu
600
-
A
500
-
rv \
400
-
/ ^
300
- 1^
\i
200
-^1
Other
100
-
Nauplii
n
1 1 1
1 1 1 1
UJ
o
<
z
03
<
500
Ncupliar
/\
400
Acartia
(\ \ \
300
-
\ \
200
-
/ V
100
\ n
0
V^
1 1 1
1 1 1 1
250
-
\
200
-
\ l\
150
-
\ M
100
- f^
^
50
kJ
0
Appendicularians
1 1 1
III 1
2.0
1.5
1.0
Female
- Calanus
as -
100
1 1 — — n 1 r
29 30 31 3 4 5 6
March
— I 1 n 1
29 30 31 3 4
March April
Morch
Figure 2. — Temporal change in total abundance (m ) of selected zooplanktonic taxa. The vertical line in each panel separates
"prestorm" on the left from "poststorm" on the right. "Paracalanus" includes some Clausocalanus spp.
156
MULLIN ET AL.: VERTICAL STRUCTURE OF PLANKTON OFF CALIFORNIA
would give the same result. Given the naupliar life
span of a few days, one would expect that, if repro-
duction were responsible, the ratio of nauplii to
adults would continue to increase for the 3 d fol-
lowing the storm (though such a finding would not
rule out advection). This is most readily tested for
Acartia (nauplii/female) and "Paracalanus"
(nauplii/adults and copepodites), since the older
stages remained within the 0-50 m water column
day and night (ANOVA classification 1 not sig-
nificant). The ratio, nauplii/female, for Acartia
increased dramatically; indeed, so much so that
published values of maximal fecundity (50 eggs/
female per day, Landry 1978; Uye 1981) are barely
sufficient over the 5-d period including the storm
(1-5 April) to account for the observed ratio on 6
April, even if no death or metamorphosis of
nauplii occurred. This is because female Acartia,
though unusually abundant immediately after the
storm on 3 April, declined dramatically from that
time until 6 April (Fig. 2). For "Paracalanus" ,
which has approximately the same maximal
fecundity as, Acartia (Checkley 1980a), the ratio of
nauplii to copepodites plus adults was slightly
greater on 6 April than during the preceding 2.5 d.
Evidence that the capacity of the environment to
sustain reproduction of "Paracalanus" increased
after the storm is presented in Section C below.
Hence, the results are qualitatively consistent
with the hypothesis that the storm stimulated
reproduction, especially in Acartia; but other
explanations cannot be ruled out. It is noteworthy,
however, that no "exotic" taxa appeared after the
storm.
Significance of ANOVA interaction 1x2 indi-
cated that for two taxa (euphausiid furcilia and
CV Calanus), the tendency to be more abundant in
the upper 50 m at night than by day was more
pronounced before the storm. Another migratory
taxon — cyphonautes larvae — showed both a
change in average depth distribution within the
upper 50 m and a change in pattern of diel migra-
tion (significance in ANOVA interactions 2x3
and 1x2x3). The nighttime distributions of
cyphonautes larvae were similar before and after
the storm, but the daytime distribution was
shifted to shallower water after the storm; adult
Corycaeus showed the same (but nonsignificant)
tendency, though they did not have a significant
diel migration over the whole period (cf., evidence
for a reverse migration by this species off Southern
California in Fiedler 1983). Pleuromamma was
virtually absent from the upper 50 m during the
day both before and after the storm, but at night
tended to occur shallower within this layer after
the storm.
Diel migration was not detected in Calanus CII
and cm copepodites (ANOVA interaction 1x3
not significant), nor did they change significantly
in total abundance after the storm (ANOVA clas-
sification 2 not significant). There was, however, a
shoaling of the distributions of both stages both
day and night after the storm (ANOVA interaction
2x3 significant). Larval fish were also shallower
in our samples by day after the storm.
The vertical distributions of these three taxa
were still stratified after the storm but were
shifted with respect to depth. Another potential
effect of the storm, which could also result in sig-
nificance of ANOVA interaction 2x3, is
homogenization of strongly stratified distribu-
tions into more nearly uniform ones. Reduction of
the temperature gradient (Fig. 1) reinforces this
possibility. The reverse process — an increase in
stratification — is possible as a result of biological
responses to the physical disturbance. Test 4 is a
simple way to examine this question, though it is
insufficient to detect some possible complex redis-
tributions. The results of this test were contrary to
expectation; only 2 taxa, Labidocera nauplii and
copepodites, had greater ranges of abundance in
the water column before the storm, while 13 taxa
had greater ranges after the storm. Included in the
latter group were Acartia and "other" nauplii,
both of which increased in overall abundance after
the storm, and all five juvenile copepodid stages of
Calanus. Thus, as far as the zooplankton is con-
cerned, poststorm stratification was generally
more marked than that prestorm. It may be of
significance, however, that the two taxa whose
prestorm abundances were more strongly
stratified than in the poststorm condition were
taxa with strong neustonic (nearsurface) affinities
(Barnett 1974; Appendix).
Inspection of the data (see Appendix) revealed
several other taxa which appeared to have dis-
tributional changes of the sorts described above,
though these were not significant by the criteria
used in the statistical tests. This means that other
sources of variability in abundance — notably,
horizontal patchiness on the scales of a few kilo-
meters, or vertical internal motions creating high
variability at a fixed depth from day to day as
water passed the sampling location — were more
important than were those patterns of change the
statistical tests were chosen to detect.
Finally, we can examine the overall similarities
in the zooplanktonic community of the upper 50 m
157
FISHERY BULLETIN: VOL. 83, NO. 2
(as abundances m^^), excluding those taxa which
significantly changed in total abundance in this
layer from day to night. The weighted-pair den-
drogram of Spearman's rank difference correla-
tion coefficients (Fig. 3A) shows an imperfect sep-
aration into profiles taken before and after the
storm, the first poststorm profile (#7) being more
like those before the storm. This is evidence
against the hypothesis that physical advection of
new populations caused all the poststorm differ-
ences, though it is also possible that advection
caused by the storm affected our site only after a
delay. The storm's apparent effect on the thermal
gradient (Fig. 1) was also delayed for some time.
Even with some of the migrating taxa excluded,
there is a partial separation in the dendrogram of
nocturnal from diurnal profiles.
o
UJ
a:
o
(J
ui
o
z
<
a:
1.0
.95
.9 0
.85
.80
.75
1.0
.9 5
,90
8 5
.8 0
.75
.7 0
.65
.60
.55
DDNDD DNN NN DD
BBBBA AAA BB AA
15 6 3 7 9 10 12 2 4 1113
N Doy or Night
A Before or After storrr
8 Profile number
A
DNDND NDNDD DM
8B8BB AAAAA AA
12 3 4 5 8 9 12 II 13 7 10
N Day or Night
B Before or After storm
6 Profile number
B.
FIGURE 3. — Dendrograms of faunal (A) and floral (B)
similarities of the upper 50 m of water off Dana Point, Calif
Faunal assemblages are based on 39 taxa, floral assemblages on
126 taxa (not just those listed in Appendix). "Floral" includes
protozoans. All coefficients are significant at P ■: 0.001.
B. Chlorophyll, Phytoplankton, and
Protozoa
Because of the mechanisms of feeding used to
separate small particles of food from water, there
are probably no strict herbivores among the zoo-
plankton we studied, i.e., no animals which ingest
living phytoplankton without also ingesting other
particulate organic matter Nevertheless, we used
the distribution of chlorophyll (see Appendix) as
the measure of the distribution of food for
particle-grazing species; in the euphotic zone of
the Southern California Bight, the concentration
of chlorophyll is closely correlated with that of
particulate organic carbon, with particulate ATP,
and (within any one season) with the chlorophyll
in particles >5 ^tm (Mullin and Brooks 1976;
Eppley et al. 1977; Mullin 1979).
We had adequate data to answer Questions 1-4
from Table 2 for chlorophyll ( = "taxon"). We used
the phytoplanktonic and protozoan abundances
from the physically integrated samples for all 13
profiles (see Methods) to perform Tests 1, 3, and 5
concerning the whole 50 m water column. We re-
stricted Questions 2 and 4 to the upper 40 m (since
these taxa were rare below this depth) and used
data from five diurnal and three nocturnal profiles
in answering these questions, since only those
profiles were suitable for counting (see Methods).
Only one of the nocturnal profiles was poststorm.
In order to obtain estimates of "within classifica-
tion" variability and still maintain a balanced de-
sign, we reduced the ANOVA to a two-way design,
retaining "before vs. after storm" and "depth" as
classifications. Thus, diurnal and nocturnal sam-
ples were considered replicates (there was no evi-
dence of diel migration in the phytoplanktonic
taxa). We again restricted the analysis to the
upper 40 m. Variances of log-transformed data for
these taxa were all homogeneous in the four pro-
file data set (profiles 5, 6, 9, and 10). Thus we
applied the ANOVA to a subset of those profiles
suitable for nonparametric tests.
The concentration of chlorophyll per m^ did not
change from day to night (Ho 1 accepted), nor did
the vertical distribution of chlorophyll within the
upper 50 m change from day to night (Ho 2 ac-
cepted). The median chlorophyll concentration
(m~^) was greater after the storm, but not sig-
nificantly so by Test 3. Vertical profiles of in vivo
fluorescence of chlorophyll and samples of phyto-
plankton from the fluorescence maximum layer
(cf. Kiefer and Lasker 1975; Cullen et al. 1982)
were taken from the second ship working concur-
rently at Dana Point. Comparison of the inte-
grated fluorescence profiles indicated that this
measure of chlorophyll increased significantly
after the storm (P 0.01 by a variant of Test 3).
Inspection of the data ( see Appendix ) indicated a
shoaling of the chlorophyll maximum layer after
the storm, and this was significant by a Mann-
Whitney U test for differences in depth of occur-
158
MULLIN ET AL.: VERTICAL STRUCTURE OF PLANKTON OFF CALIFORNIA
rence of the median value before vs. after the
storm. This tendency was also shown by isotherms
(see above). The range of concentrations of
chlorophyll in the water column tended to in-
crease, meaning that chlorophyll maxima were
accentuated after the storm, though hypothesis 4,
based on the median profiles, was not rejected
(0.01 < P < 0.025).
No phytoplanktonic or protozoan taxa we
examined migrated dielly into and out of the upper
50 m nor did any taxon migrate dielly within the
upper 40 m. The two-way ANOVA of four profiles
detected significant decreases in poststorm abun-
dances of the diatoms Nitzschia spp., Bacterias-
trum spp., Rh. alata, and Rh. fragilissima; all but
the last of these decreases were also significant by
nonparametric Test 3 applied to the full 13-
member set of integrated profiles. This latter test
also revealed a significant decrease in poststorm
abundance of another diatom, S. costatum. Only
the dinoflagellate, Prorocentrum, was more abun-
dant after the storm by the ANOVA test. When the
data set of 13 integrated profiles was examined by
nonparametric Test 3, significant increases were
also detected in the poststorm abundance of
Lohmanniella (a potential larval fish food) and
Ceratium spp. Neither Gymnodinium splendens
nor Cochlodinium catenatum (two potential food
items for larval anchovy) changed significantly in
abundance in samples taken at the depth of the
fluorescence maximum layer from the second ves-
sel. The large diatom category, Chaetoceros spp.,
did not change in total abundance, but the species
comprising this category changed at the time of
the storm; in particular, Ch. constrictus was the
dominant member of the genus after the storm,
but was not encountered in the prestorm samples.
From the ANOVA, no phytoplanktonic taxa had
poststorm vertical distributions different from
their prestorm ones, when the criterion of P "^ 0.01
was used for significance, and only Rh. alata and
Prorocentrum had significant changes as defined
by P < 0.05. Hence, as far as we could tell from the
four profiles which were usable in the ANOVA, the
storm had much less effect in changing the verti-
cal distributions of specific phytoplankters (and
protozoans) than it did for zooplankton. This con-
clusion is, however, suspect (see below).
Nonparametric Test 4, for which eight profiles
were usable, indicated that the poststorm range of
abundances in the upper 40 m was greater than
the prestorm range for five of the dinoflagellate
taxa, Mesodinium rubrum, and Lohmanniella,
while Nitzschia, Rh. fragilissima , and S. costatum
had significantly smaller poststorm ranges. These
eight profiles strongly suggested poststorm shoal-
ing of the vertical distributions of the potential
food species, C. catenatum, G. splendens, and
Laboea, but the data sets were too small to estab-
lish statistical significance at P ^ 0.01.
The general changes associated with the storm
were therefore decreases in the abundances and in
the degree of stratification of some diatoms, and
increases in abundances and degree of stratifica-
tion of some dinoflagellates and protozoans. How-
ever, significant changes in the pattern of stratifi-
cation with depth were more difficult to detect
because of the reduced data sets, except for the
shoaling of the distribution of chlorophyll.
The floral composition of the profiles permitted a
clear separation into prestorm and poststorm as-
semblages, with the exception of the last prestorm
profile, which was quite different from the others
(Fig. 3B). This result was different from the analy-
sis of zooplankton (Fig. 3A), where the first post-
storm profile was unexpectedly grouped with pre-
storm profiles. Both results, however, indicate that
the compositional changes associated with the
storm were gradual rather than abrupt. Unlike
the faunal assemblages, the floral grouping
showed no tendency to separate day from night.
The difference in correlation coefficients between
dendrograms A and B probably reflects the fact
that quite different numbers of taxa were counted,
and that samples were counted by different
techniques, rather than any fundamental distinc-
tion between phytoplanktonic and zooplanktonic
assemblages.
C Relations Between Zooplankton and
Phytoplanktonic Biomass
If positive correlations between the abundances
of particle-grazing zooplanktonic taxa and
chlorophyll existed before the storm, it is reason-
able to hypothesize that such correlations would
be weaker or nonexistent after the storm due to
turbulent disruption of associations.
We examined the following taxa of zooplankton
in this regard, sometimes combining categories
from the Appendix: Naupliar Acartia, naupliar
Calanus, naupliar "Paracalanus" , copepodid and
adult Acartia, CI-CIV Calanus, CV and female
Calanus (nocturnal only), copepodid and adult
"Paracalanus" , adult Metridia (nocturnal only),
adult Pleuromamma (nocturnal only), and the
appendicularians. We grouped data into four sets
of profiles: three diurnal, prestorm; three noc-
159
FISHERY BULLETIN: VOL. 83, NO. 2
turnal, prestorm; three diurnal, poststorm
(excluding the 6 April profile); and three noctur-
nal, poststorm. In order to give each profile w^ithin
a set equal weight and to restrict attention to
vertical relations, we arranged data from each
profile in order of increasing concentration of
chlorophyll; next ranked the samples in order of
increasing abundance of the taxon of interest;
then calculated the Kendall's tau coefficient as a
measure of correlation between that taxon and
chlorophyll within each profile; and finally calcu-
lated the coefficient of concordance between the
rearranged ranks of the taxon in the three profiles
of a set as a measure of agreement on a common
tendency (see Mullin and Brooks 1972). We then
defined a persistent relation between a taxon and
chlorophyll in one full set of profiles as requiring a
significant {P ^ 0.05) concordance between the
individual profiles of the set, tau coefficients of all
profiles of the same sign (positive or negative), and
at least one of the tau coefficients significant (P ^
0.05).
No persistently negative relations were found
between any taxon and chlorophyll in any set of
profiles. In the diurnal, prestorm set, naupliar
Acartia, naupliar Calanus, copepodid and adult
Acartia, and appendicularians were all positively
related to chlorophyll, and CI-CIV Calanus
tended in this direction. These relations all van-
ished at night by our criteria, though naupliar
Calanus tended to retain a positive association.
After the storm, the strength of the diurnal, posi-
tive relations of naupliar Acartia, copepodid and
adult Acartia, CI-CIV Calanus, and appendicula-
rians increased, and naupliar "Paracalanus" also
had a positive relation. At night after the storm,
all taxa except naupliar "Paracalanus" , CV and
adult Calanus, Metridia, and Pleuromamma had
positive relations with chlorophyll. Thus, contrary
to expectations, after the storm there were more
positive relations between these particle-grazing
taxa and the concentration of their food, measured
as chlorophyll.
We reached a similar conclusion for the ciliates,
Laboea and Lohmanniella; neither were persis-
tently related to the vertical distribution of
chlorophyll before the storm, but both were posi-
tively related after the storm by our criteria. Since
fewer profiles for these protozoans were counted,
we did not separate night from day in searching for
the correlations.
Such correlations can also show seasonal vari-
ability; for example, Fiedler (1983) found strongly
positive correlations between the vertical dis-
tributions of chlorophyll, Paracalanus, and
Penilia avirostris (a cladoceran) in October, but
strongly negative correlations between these zoo-
plankters and chlorophyll in May; Ctenocalanus
vanus showed a seasonal reversal of its relation to
chlorophyll in the opposite direction.
In spite of the increased correlation after the
storm between particle-grazers and their food,
there is some evidence that the poststorm grazing
pressure on phytoplankton was less than that pre-
storm. The ratio of chlorophyll to phaeopigments
in the water column is an indicator of the ratio of
living phytoplankton to the fecal material of graz-
ers, and hence is inversely related to the grazing
pressure per unit phytoplanktonic crop (Lorenzen
1967). The chlorophyll/phaeopigment ratio was
significantly greater (P < 0.05 by rank sum test)
after the storm, indicating a reduction in grazing
relative to the available crop.
We derived a second indicator of the effect of the
storm on relations between phytoplankton and
zooplankton from a study of egg production of the
copepod, Paracalanus parvus, and chlorophyll
and particulate nitrogen in the Southern Califor-
nia Bight (Checkley 1980b). Checkley found that
the nitrogen in phytoplankton was the best mea-
sure of fecundity-stimulating food, that about half
the chlorophyll retained on a fiberglass filter was
in particles >5 pim, and that the weight ratio of
nitrogen in phytoplankton to chlorophyll was 12.
From these relations, the egg production of
Paracalanus is food-limited where the concentra-
tion of total chlorophyll is below 1.3 /xg/1. By this
standard, only 18% of the upper 50 m contained
sufficient food for maximal egg production prior to
the storm, while 34% of the water column met this
criterion afterwards.
This conclusion is likely to be qualitatively cor-
rect unless the size distribution of phytoplankton
was altered markedly by the storm, or the breadth
of the copepods' diet with respect to nonphyto-
plankton was changed. Neither of these sources
of error is particularly likely, since the ratio of >5
/i,m to total chlorophyll agrees with earlier results
in the Bight (Mullin and Brooks 1976) and since
the range of the data from which Checkley de-
duced the importance of chlorophyll in regulating
egg production included all but one of the concen-
trations of chlorophyll we measured.
Further, the vertical distribution of adult and
copepodid "Paracalanus" was positively corre-
lated with that of chlorophyll after the storm and
at night (see above). If this finding applies to
female "Paracalanus" by themselves, a consider-
160
MULLIN ET AL.: VERTICAL STRUCTURE OF PLANKTON OFF CALIFORNIA
ably greater fraction of total reproduction oc-
curred at maximal (i.e., nonfood-limited) rates
after the storm.
A similar quantitative example of augmenta-
tion of zooplanktonic nutrition related to the
storm can be calculated for CIV-adult Calanus,
though the vertical distribution of these stages
was not well correlated with that of chlorophyll. In
June 1980, Cox et al. (1983) estimated the carbon
budget of Calanus at various stations and depths
in the Southern California Bight, and concluded
that gain in biomass of these copepods was possi-
ble where the concentration of chlorophyll ex-
ceeded 0.9 Mg/1- By this standard, the fraction of
the upper 50 m where some gi-owth was possible
(nighttime only, because of diel migration) was
36% before and 58% after the storm.
A third test of the significance of vertical dis-
tributions and the effect of the storm on them was
based on the plant pigments in the guts of the
large copepods caught at various times and
depths. The measurement of fluorescence of gut
contents can be used as a quantitative estimate of
the rate of ingestion of plant material if the break-
down of pigment, the gut passage time, and the
background fluorescence due to an animal's own
pigmentation are known (Mackas and Bohrer
1976). We chose to ask two simpler questions based
on changes in fluorescence: 1) Were the total gut
pigments (chlorophyll -I- phaeopigments) of
copepods caught at specific depths correlated with
the concentration of chlorophyll measured at the
same depths, before or after the storm or both? 2)
Did the amount of gut fluorescence of a tax on,
independent of specific depths, change coincident
with the storm? The first question addresses the
issue of whether the copepods can be shown to have
fuller guts at depths where phytoplanktonic food
(as measured by chlorophyll) is more concen-
trated. If copepods move frequently from the
depths at which they feed, such correlations would
be difficult to establish (cf. Dagg and Wjmian
1983). The second question is the more general one
of whether the copepods were better nourished
after the storm.
We tested data concerning female Acartia,
female and CV Calanus, female Metridia, and
female Pleuromamma in this regard, with 6-28
pre- or poststorm data points per taxon. Of these
taxa, only Acartia's abundance was significantly
positively associated with the vertical distribution
of chlorophyll (see above).
The gut pigment per Acartia showed no relation
to the ambient concentration of chlorophyll, how-
ever, while that of Pleuromamma was positively
correlated with chlorophyll. In no case was the
poststorm correlation (tau coefficient) between gut
fluorescence and chlorophyll stronger than that
prestorm. Hence, we could not show that for these
taxa the distribution of degree of satiety became
more strongly associated with the vertical dis-
tribution of chlorophyll after the storm, even
though the range of chlorophyll concentrations
available in the upper 50 m had increased.
Nor for any of these taxa was the poststorm
amount of gut fluorescence significantly greater
than that prestorm. Based on comparison between
field-caught female Acartia and Calanus, and
these same taxa fed to excess or starved in the
laboratory, we conclude that both these popula-
tions were well fed in general both before and after
the storm, and animals had plant food in their guts
at all depths sampled. Hence, we could not demon-
strate a change in nutritional status of the taxa as
a result of the storm, even though the overall con-
centration of chlorophyll increased. All these taxa
have been shown to feed on nauplii as well as
phytoplankton (e.g., Haq 1967; Lonsdale et al.
1979; Landry 1981), but we could not test whether
their nutrition from animal sources had improved
coincident with the increase in abundance of
nauplii following the storm.
D. Abundance and Vertical Distribution of
Food for Larval Fish
Because larval fish are visual predators, it is the
diurnal distributions of potential prey which are
particularly relevant. Different species select (or
are physically able to ingest) different prey, and of
course different types of prey differ in their catch-
ability, digestibility, and nutritive value. We will
consider the distributions of food for two prototyp-
ical larvae representing extremes in a continuum
of actual types. One is a small-mouthed larva
which we v^dll call "anchovy-like", based on Bemer
(1959), Lasker et al. (1970), O'Connell and
Raymond (1970), Arthur (1976), and Lasker and
Zweifel (1978). For these larvae, "large" prey con-
sists of all copepod nauplii and lamellibranch and
cyphonautes larvae (Appendix); "small" prey con-
sists of all ciliates and all nonthecate, large di-
noflagellates. Laboratory studies suggest the crit-
ical concentrations for both good survival and
rapid grov^rth are ^ 5 x 10^ large or s: 5 x 10^ small
prey 1~^ , or an equivalent combination.
The other prototypical larva has a larger mouth
and is more active; based on Arthur (1976), Hunter
161
FISHERY BULLETIN: VOL. 83, NO. 2
and Kimbrell (1980), Lipskaya (1982\ and De-
vonald (1983), this larva is "mackerel-like"
(though Scomber and Trachurus, especially the
latter, tend to spawn farther offshore than our
sampling location). This larva requires a much
lower concentration of "large" prey, 50 1 \ and a
large number of zooplanktonic taxa are potential
food: all copepod nauplii; lamellibranch and
cyphonautes larvae; Acartia, Labidocera, Met-
ridia, and Pleuromamma immature copepodites;
"Paracalanus" , Oithona, Euterpina, Corycaeus,
Oncaea, and Microsetella copepodites and adults;
euphausiid nauplii and calyptopes; CI, CII, and
CIII Calanus; "other copepods"; cladocerans; and
(see Lipskaya 1982) appendicularians. Nauplii
and lamellibranch and cyphonautes larvae are
considered small prey, the remainder being large.
This spectrum of prey is also appropriate for young
postlarval anchovy.
Figure 4 shows the prestorm and poststorm
diurnal vertical distributions of food for the two
prototypical larval types, in terms of the equiva-
lent "large prey" for each; the figure legend gives
the conversion factors used. In no instance was the
laboratory-determined critical concentration of
prey exceeded. We do not believe that this conclu-
sion is due to destruction of prey during preserva-
tion.
We tested hypotheses concerning the vertical
stratification and the effect of the storm on dis-
tributions of prey by two-way ANOVAs on log-
transformed abundances from the diurnal profiles
(3, 5, 7, and 9) similar to those used for phyto-
planktonic taxa (Section B above), since variances
were homogeneous by Barlett's test. We used our
data on the diurnal abundances of total larval fish
to examine correlations with the food of
"anchovy-like" larvae by means of the tau coeffi-
cient for these profiles.
It is apparent from Figure 4A that "small prey"
dominated the food supply for "anchovy-like" lar-
vae, even when expressed as its equivalence in
terms of large prey. Because this category had not
increased significantly after the storm, neither
had total prey for these larvae; however, large prey
were both more abundant and more strongly
stratified.
The food supply of "mackerel-type" larvae was
E
I-
CL
UJ
Q
EQUIVALENT LARGE PREY, lOV liter
1
EQUIVALENT LARGE PREY/ liter
20
\
30
I
40
I
50
I
B
30
I
40
I
Large prey
Small prey
50
_i
60
I
Large prey
Small prey
PRE -STORM
POST- STORM
Figure 4. — Median vertical, diurnal distributions of larval fish food, as "equivalent large prey", before and after the storm. Taxa
comprising categories of prey are li.sted in text. A. Prey of "anchovy-like" larvae. Graphed concentrations of small prey are 0.1 x actual
concentrations. B. Prey of "mackerel-like" larvae. Graphed concentrations of small prey are 0.2 x actual concentrations.
162
MULLIN ET AL.: VERTICAL STRUCTURE OF PLANKTON OFF CALIFORNIA
dominated by "large" rather than "small" prey.
That these types of zooplankters are less abundant
very near surface and below 30 m than at inter-
mediate depths is apparently not unusual in
spring ( Fiedler 1983:fig. 5). Both types of prey were
more abundant after the storm. Total food for both
types of larvae tended to be concentrated nearer
the surface in the poststorm condition.
Although the numbers of larval fish in our sam-
ples are too small, especially after the storm, to
provide a strong test of spatial correlation with
their food supplies, the tau coefficients of correla-
tion between total larval fish and their food by day
were positive in all cases, but somewhat less so
after the storm for the nonthecate dinoflagellates
and ciliates which dominated the food supply of
"anchovy-like" larvae. This was the case even
though the poststorm distributions of both larval
fish and food were concentrated nearer the surface
than were the prestorm distributions.
SUMMARY AND DISCUSSION
We concentrated during this study on the con-
sequences of the vertical distributions of plankton
for the production of zooplanktonic food for larval
fish, and on the differences in distributions of food
experienced by larval fish at one coastal location
before and after a small storm. Since advection
surely occurred, we do not intend to imply that the
same individual larvae experienced both sets of
conditions.
Conclusions we believe to be ecologically sig-
nificant and statistically verified are as follows:
1. The biotic environment was vertically struc-
tured.
a. Of the 28 zooplanktonic taxa for which the
ANOVA was appropriate, 22 had a consis-
tently uneven (i.e., stratified) pattern of dis-
tribution with depth in the upper 50 m. Of
the remaining six taxa, three had regular
temporal changes in vertical distribution.
Hence, only 3 of the 28 taxa were uniformly
distributed both vertically and dielly.
b. Chlorophyll was stratified in the upper 50
m, and 9 of the 18 phytoplanktonic-
protozoan taxa examined had stratified dis-
tributions in the upper 40 m; the stratified
taxa were notably dinoflagellates and the
oligotrich ciliates rather than the dia-
toms.
c. Both small prey and total prey for
"anchovy-type" larvae were vertically
stratified, but prey for "mackerel-type" lar-
vae was not.
d. Though the abundance of Acartia was cor-
related vertically with that of chlorophyll,
its gut fullness was not.
2. Several features were different after the storm.
a. Several zooplanktonic taxa — notably, vari-
ous nauplii — were more abundant, while
larval fish were less so. Ceratium, Prorocen-
trum, and Lohmannlella had increased,
while several diatoms had decreased. Evi-
dence suggested a poststorm increase in
chlorophyll, but contained ambiguities.
b. Several zooplanktonic taxa — Pleuro-
mamma at night, cyphonautes by day,
Calanus CII and CIII, larval fish — tended
to be concentrated in shallower depths after
the storm, as did chlorophyll, but data were
insufficient to show that the large-sized
phytoplanktonic taxa we studied responded
in this way. Food for both types of larval fish
was concentrated in shallower water after
the storm. The neustonic distribution of
Labidocera nauplii and copepodites was
less pronounced after the storm, but in gen-
eral the poststorm vertical stratification
was at least as great as that prestorm, even
though the temperature gradient was les-
sened. This general conclusion was also
true for phji^oplankton (except for some
diatoms which were less abundant after the
storm) and for the sum of forms represent-
ing "large food" for "anchovy-like" larvae
and "small food" for "mackerel-like" larvae.
3. Relations between predators and prey were dif-
ferent following the storm.
a. Several taxa maintained or established
abundant populations in those parts of the
water column where food was most plenti-
ful. However, this was not true for taxa with
pronounced diel vertical migrations. The
estimated poststorm reproduction of
"Paracalanus" was less limited by food than
was the prestorm reproduction, and
Calanus could obtain sufficient food for
growth in a greater fraction of the water
column after the storm; but we could not
demonstrate a poststorm increase in gut
fullness of large herbivores.
b. Larval fish, both those categorized as
"anchovy-like" and "mackerel-like", also
were exposed to augmented concentrations
of their respective "large" food items, both
immediately and perhaps as a result of en-
163
FISHERY BULLETIN: VOL. 83, NO. 2
hanced growth and reproduction of zoo-
plankton and reduced competition from
other larvae. However, the supply of food for
larvae was less than that thought neces-
sary for rapid growth and high survival,
and the spatial association between total
larvae and abundant, small food (di-
noflagellates and protozoans) was slightly
less strong after the storm; this category of
food was not significantly more abundant
after the storm.
Lacking information on the planktonic stocks
and their distribution, we might have hy-
pothesized that the decrease in abundance of lar-
val fish following the storm (Fig. 2) was due to
starvation because the storm-induced turbulence
homogenized the vertical distributions of food.
The results shown in Figure 4 make this
hypothesis untenable.
Even though we did not find concentrations of
food exceeding laboratory-determined thresholds
for growth, certainly the most important conclu-
sion with respect to the storm from the point of
view of a larval fish is that there was as much food
available after the storm and that copepod nauplii
(which laboratory studies have shown to be desir-
able prey) increased significantly. In view of this,
we predict that the larvae present after the storm
were growing faster (or starving more slowly),
were in better condition, and were more likely to
have food in their guts than those present before
the storm, even though the latter were the more
numerous. Also, since the available food increased
at several depths in the water column, we predict
that the occurrences of well-nourished anchovy
larvae (if any were present) should be shallower
after the storm and less strictly confined to one or
two depth strata.
A tendency for larvae to be less closely as-
sociated after the storm with layers of abundant
dinoflagellates and ciliates might negate this pre-
diction; the nature of the vertical relations should
now be examined using the more reliable distribu-
tions of larvae determined by a towed opening-
closing net. Another condition which would result
in failure of our prediction is if the larvae actually
rely for nutrition on micropatches of food, such as
organic aggregates and an associated assemblage
of phytoplankton and microzooplankton (e.g.,
Alldredge 1976; Silver et al. 1978). Devonald
(1983) has suggested this for larvae of jack mack-
erel, Trachurus symmetricus, farther offshore in
the Southern California Bight. If this is true, sam-
pling on the scale of hundreds of liters, as we did,
would not detect the redistribution of food on the
scale most important for larval survival and
growth; storm-induced turbulence could have dis-
rupted such micropatches, making the supply of
food less rather than more favorable. A large
amount of true microscale sampling, such as that
done by Owen (1981), would then be required to
predict correctly the effect of the storm on the
larvae.
ACKNOWLEDGMENTS
We thank R. Lasker, G. Moser, and R. Owen of
the National Marine Fisheries Service for collab-
oration in this project. J. Star and P. Peterson
assisted with sampling, as did D. Carlson, owner
and operator of the Fisherette. D. Cayan and R.
Seymour supplied some of the wind and wave data.
This long after the fact, we thank Neptune for the
storm. E. Venrick made helpful comments on the
manuscript (especially in its statistical aspects),
and D. Osborn typed it several times. Financial
support was from the Department of Energy, DE-
AT03-82-ER60031, and ship funds from the
Marine Life Research Group.
LITERATURE CITED
ALLDREDGE, A. L.
1976. Discarded appendicularian houses as sources of food,
surface habitats, and particulate organic matter in
planktonic environments. Limnol. Oceanogr. 21:14-23.
ARTHUR, D. K.
1976. Food and feeding of larvae of three fishes occurring
in the California Current, Sardinops sagax, Engraulis
mordax, and Trachurus aymmetricus. Fish. Bull., U.S.
74:517-530.
BARNETT, A.M.
1974. The feeding ecology of an omnivorous neritic
copepod, Lahidocera trispmosa Esterly. Ph.D. Thesis,
Univ. California — San Diego, La Jolla, 215 p.
BERNER, L., JR.
1959. The food of the larvae of the northern anchovy En-
graulis mordax. Bull. Inter-Am. Trop. Tuna Comm. 4:1-
22.
Brooks, e. r., and m. m. Mullin.
1983. Diel changes in the vertical distribution of biomass
and species in the Southern California Bight. CalCOFI
Rep. 24:210-215.
CHECKLEY, D. M., JR.
1980a. The egg production of a marine planktonic copepod
in relation to its food supply: Laboratory studies. Lim-
nol. Oceanogr. 25:430-446.
1980b. Food limitation of egg production by a marine,
planktonic copepod in the sea off Southern Califor-
nia. Limnol. Oceanogr. 25:991-998.
Cox, J. L., S. WILLASON, AND L. HARDING.
1983. Consequences of distributional heterogeneity of
164
MULLIN ET AL.: VERTICAL STRUCTURE OF PLANKTON OFF CALIFORNIA
Calanus pacificus grazing. Bull. Mar. Sci. 33:213-226.
CULLEN, J. J.. AND R. W. EPPLEY.
1981. Chlorophyll maximum layers of the Southern
California Bight and possible mechanisms of their forma-
tion and maintenance. Oceanol. Acta 4:23-32.
CULLEN, J. J., F. M. H. REID. AND E. STEWART.
1982. Phytoplankton in the surface and chlorophyll
maximum off Southern California in August, 1978. J.
Plank. Res. 4:665-694.
DAGG, M. J., AND K. D. WYMAN.
1983. Natural ingestion rates of the copepods Neocalanus
plumchrus and N. cristatus calculated from gut con-
tents. Mar. Ecol. Prog. Ser. 13:37-46.
DEVONALD, E K.
1983. Evaluation of the feeding success of jack mackerel
larvae off Southern California and some contributing fac-
tors. Ph.D. Thesis, Univ. California — San Diego, La
Jolla, 209 p.
DIXON, W. J., AND R J. MASSEY, JR.
1957. Introduction to statistical analysis. 2d ed.
McGraw-Hill, N.Y., 488 p.
DORMAN, C. E.
1982. Winds between San Diego and San Clemente Is-
land. J. Geophys. Res. 8:9636-9646.
ENRIGHT, J, T.
1977. Copepods in a hurry: Sustained high-speed upward
migration. Limnol. Oceanogr. 22:118-125.
ENRIGHT, J. T, AND H.-W. HONEGGER.
1977. Diurnal vertical migration: Adaptive significance
and timing Part 2. Test of the model: Details of tim-
ing. Limnol. Oceanogr. 22:873-886.
EPPLEY, R. W., W. G. HARRISON, S. W. CHISHOLM. AND E.
STEWART.
1977. Particulate organic matter in surface waters off
Southern California and its relationship to phyto-
plankton J. Mar. Res. 35:671-696.
ESTERLY, CO.
1912. The occurrence and vertical distribution of the
Copepoda of the San Diego Region with particular refer-
ence to nineteen species. Univ. Calif Publ. Zool. 9:253-
340.
Fiedler, R C.
1982. Zooplankton avoidance and reduced grazing re-
sponses to Gymnodinium splendens (Dinophy-
ceae). Limnol. Oceangr. 27:961-965.
1983. Fine-scale spatial patterns in coastal epiplankton off
Southern California. J. Plank. Res. 5:865-877.
Gruber, d., e. h. ahlstrom, and M. M. MULLIN.
1982. Distribution of ichthyoplankton in the Southern
California Bight. CalCOFI Rep. 23:172-179.
HAQ, S. M.
1967. Nutritional physiology of Metridia lucens and M.
longa from the Gulf of Maine. Limnol. Oceanogr. 12:40-
5L
Holm-Hansen, O., C. J. lorenzen, r. w. holmes, and J. D.
H. Strickland.
1965. Fluorometric determination of chlorophyll. J.
Cons. Perm. Int. Explor Mer 30:3-15.
Hunter, j. r.
1972. Swimming and feeding behavior of larval anchovy
Engraulis mordax. Fish. Bull., U.S. 70:821-838.
1976. Culture and growth of northern anchovy, Engraulis
mordax, larvae. Fish. Bull., U.S. 74:81-88.
Hunter, j. r., and C. A. Kimbrell.
1980. Early life history of Pacific mackerel. Scomber
japonicus. Fish. Bull., U.S. 78:89-101.
Huntley, m. e.
1982. Yellow water in La Jolla Bay, California, July 1980.
II. Suppression of zooplankton grazing. J. Exp. Mar. Biol.
Ecol. 63:81-91.
KIEFER, D. A., and R. LASKER.
1975. Two blooms of Gymnodinium splendens, an unar-
mored dinoflagellate. Fish. Bull., U.S. 73:675-678.
LANDRY, M. R.
1978. Population dynamics and production of a planktonic
marine copepod, Acartia clausii, in a small temperate
lagoon on San Juan Island, Washington. Int. Rev.
Gesamten Hydrobiol. 63:77-119.
1981. Switching between herbivory and carnivory by the
planktonic marine copepod Calanus pacificus. Mar. Biol.
(Berl.) 65:77-82.
LASKER, R.
1975. Field criteria for survival of anchovy larvae: The
relation between inshore chlorophyll maximum layers
and successful first feeding. Fish. Bull., U.S. 73:453-
462,
1981. Factors contributing to variable recruitment of the
northern anchovy (Engraulis mordax) in the California
Current: Contrasting years 1975 through 1978. Rapp.
P-V, Reun. Cons. Int. Explor. Mer 178:375-388.
LASKER, R,, H. M. FEDER, G. H. THEILACKER, AND R. C. MAY.
1970. Feeding, growth, and survival of Engraulis mordax
larvae reared in the laboratory. Mar Biol. (Berl.) 5:345-
353.
LASKER, R., J. PELAEZ, AND R. M. LAURS.
1981. The use of satellite infrared imagery for describing
ocean processes in relation to spawning of the northern
anchovy {Engraulis mordax). Remote Sensing Environ.
11:439-453.
LASKER, R., AND J. R. ZWEIFEL.
1978. Growth and survival of first-feeding northern an-
chovy larvae (Engraulis mordax) in patches containing
different proportions of large and small prey. In J. H.
Steele (editor). Spatial pattern in plankton communities,
p. 329-354. Plenum Press, N.Y.
LIPSKAYA, N. YA.
1982. [The feeding of larvae of the chub mackerel, Scomber
japonicus (Scombridae), from the southeastern
Pacific] Vopr Ikhtiol. 22:97-104.
LONSDALE, D. J., D. R. HEINLE, AND C. SIEGFRIED.
1979. Carnivorous feeding behavior of the adult calanoid
copepod Acartia tonsa Dana. J. Exp. Mar. Biol. Ecol.
36:235-248.
LORENZEN, C.J.
1967. Vertical distribution of chlorophyll and phaeopig-
ments: Baja California. Deep-Sea Res. 14:735-745.
MACKAS, D., AND R. BOHRER.
1976. Fluorescence analysis of zooplankton gut contents
and an investigation of diel feeding patterns. J. Exp.
Mar. Biol. Ecol. 25:77-85.
METHOT, R. D., JR., AND D. KRAMER.
1979. Growth of northern anchovy, Engraulis mordax, lar-
vae m the sea. Fish. Bull., U.S. 77:413-423.
MULLIN, M. M.
1979. Longshore variation in the distribution of plankton
in the Southern California Bight, CalCOFI Rep.
20:120-124.
MULLIN, M. M., AND E. R. BROOKS.
1970. The effect of concentration of food on body weight,
cumulative ingestion, and rate of growth of the marine
copepod Calanus helgolandicus . Limnol. Oceanogr.
15:748-755.
165
FISHERY BULLETIN: VOL. 83, NO. 2
1972. The vertical distribution of juvenile Calanus
(Copepoda) and phytoplankton within the upper 50m of
water off La Jolla, California. In A. Y. Takenouti
(editor). Biological oceanography of the northern North
Pacific Ocean, p. 347-354. Idemitsu Shoten, Tokyo.
1976. Some consequences of distributional heterogeneity
of phytoplankton and zooplankton. Limnol. Oceanogr.
21:784-796.
O'CONNELL, C. P.
1980. Percentage of starving northern anchovy, Engraulis
mordax, larvae in the sea as estimated by histological
methods. Fish Bull., U.S. 78:475-489.
O'CONNELL, C. P, AND L. P RAYMOND.
1970. The effect of food density on survival and growth of
early post yolk-sac larvae of the northern anchoyy ^En-
graulis mordax Girard) in the laboratory. J. Exp. Mar
Biol. Ecol. 5:187-197.
OWEN, R. W.
1981. Microscale plankton patchiness in the larval an-
chovy environment. Rapp. R-V. Reun. Cons. Int. Explor.
Mer 178:364-368.
PaffenhOfer, G.-A.
1976. Feeding, growth, and food conversion of the marine
planktonic copepod Calanus helgolandicus . Limnol.
Oceanogr. 21:39-50.
SILVER, M. W., A. L. SHANKS, AND J. D. TRENT.
1978. Marine snow: Microplankton habitat and source of
small-scale patchiness in pelagic populations. Science
(Wash., D.C.) 201:371-373.
TATE, M. W, AND R. C. CLELLAND.
1957. Nonparametric and shortcut statistics in the social,
biological, and medical sciences. Interstate Printers and
Publishers, Inc., Danville. 111., 171 p.
UYE, S.
1981. Fecundity studies of neritic-calanoid copepods Acar-
tia clnusi Giesbrecht and A. sfeucri Smirnov: A simple
empirical model of daily egg production. J. Exp. Man
Biol. Ecol. 50:255-271.
UYE, S., AND A. FLEMINGER.
1976. Effects of various environmental factors on egg de-
velopment of several species of Acartia in Southern
California. Mar. Biol. (Berl.) 38:253-262.
166
MULLIN ET AL.: VERTICAL STRUCTURE OF PLANKTON OFF CALIFORNIA
APPENDIX
Vertical Distribution of Taxa
APPENDIX TABLE 1. — Diurnal profiles before storm. * = variances heterogeneous; ANOVA not used.
Depth (m):
0
5
10
15
20
25
30
35
40
45
50
ZOOPLANKTON
■-median number per cuoic meter-
5,074 1,345 448
Naupliar Acartia
75
407
786
1,533
78
0
39
49
Naupliar Labidocera
1 1 ,688
325
75
77
70
67
34
0
0
0
0
"Naupliar Paracalanus'"'
2,397
3,004
2,000
1,529
1,761
2,941
8,679
3,333
1.418
1,023
1,478
"Naupliar Calanus
693
956
597
536
515
1,070
299
107
75
79
33
Naupliar Rhincaianus
0
0
0
77
7
252
163
71
7
4
0
"Other nauplii
1,653
1,832
3,283
4,138
7,647
2,809
5,000
2,679
3.060
1.732
1,569
Female Acartia
4
22
23
19
21
8
4
0
0
0
0
Male Acaitia
4
11
19
23
11
0
0
0
0
0
0
Copepodite Acartia
12
18
302
284
345
147
0
0
0
0
0
"Adult Labidocera
0
0
0
0
0
0
0
0
0
0
0
"Copepodite Labidocera
1,571
234
4
0
0
0
0
0
0
0
0
Adult and copepodite
"Paracalanus"'
3,117
2,711
2,239
1,456
1,029
840
3,051
4,783
3,694
2.598
1,814
"Appendiculanans
285
1,245
1,214
3,218
1,985
4.622
2,164
856
67
24
25
"Adult and copepodite Oithona
0
293
970
1,116
2,746
1,070
1,661
1,739
521
736
1,100
Adult and copepodite Euterpina
9
0
71
284
662
602
293
107
0
0
0
Euphausiid nauplii
0
0
11
0
4
0
3
11
16
4
13
'Euphausiid calypiopis
0
0
4
17
14
30
4
23
7
8
5
Euphausiid furcilia
0
0
4
0
4
20
7
31
8
12
14
Chaetognalhs
11
163
204
307
121
172
97
43
16
35
31
Female Calanus
0
0
0
0
0
0
0
0
0
0
0
Male Calanus
0
0
0
0
0
0
0
0
0
0
0
0 V Calanus
0
0
0
0
0
0
0
0
0
3
0
C IV Calanus
0
0
0
0
0
4
4
4
8
0
14
C III Calanus
0
0
0
4
0
3
8
14
15
4
5
C II Calanus
0
4
0
4
7
8
57
21
0
3
0
C 1 Calanus
0
8
4
0
13
13
57
18
4
0
0
"Adult Corycaeus
15
33
79
87
92
97
157
74
92
67
64
"Adult and copepodite Oncaea
83
73
38
230
70
168
2,463
2,536
1,679
1,299
1,225
Microsetella
0
4
4
843
1,513
1,271
305
286
65
173
196
Adull Melndia
0
0
0
0
0
0
0
0
0
0
0
"Adult Pleuromamma
0
0
0
0
0
0
0
0
0
0
0
"Copepodite Metndia
and Pleuromamma
0
0
0
0
0
0
0
12
22
91
163
"Adult Rhincaianus
0
0
0
0
0
0
0
0
0
0
0
Copepodite Rhincaianus
0
0
0
0
0
0
34
18
15
17
15
"Copepodite Eucalarius
0
0
0
0
0
0
0
25
0
0
0
Other copepods
0
0
15
0
0
0
75
11
7
0
3
Fish eggs
43
29
18
8
7
3
0
0
0
0
0
Fish larvae
0
0
30
74
59
57
23
7
C
0
0
Cladocerans {Evadne)
50
121
86
12
0
4
0
0
0
0
0
Polychaete larvae
0
22
104
92
56
104
78
5^
28
22 "
21
Lamellibranch larvae
0
0
0
0
C
0
0
0
0
104
0
Cyphonautes larvae
0
0
0
0
0
0
52
140
116
30
0
'CHI OROPHYi 1
— median
micrograms per liter —
*^ 1 IL_^^l tV^ 1 1 1 T k_ L_
0.33
0.36
0.44
0.63
097
1.03
2.06
0.77
0.49
0.32
0.28
PHYTOPLANKTON -r CILIATES
Nitzschia spp. S
rYlCwHiar"! rMimKi^r i-i^^r
inn ml ...
1,627
946
2,412
1,536
2,326
1 lUI 1 ii->c;i y^i
987
r \J\J INI
1,369
1,008
261
Bactenastrum spp. (chains)
56
86
84
78
78
95
66
54
16
Chaetoceros spp.
2,488
3,845
4,307
3,246
3,576
1,427
4.270
1.764
413
Rhizosolenia alata
112
116
90
86
80
35
18
4
2
Rhizosolenia fragillssima
98
120
156
120
268
53
6
0
8
Skeletonema costatum
78
56
18
96
76
24
3
88
40
Ceratium spp.
42
30
24
32
14
11
54
4
0
Gonyaulax polyedra Ipolygramma
26
14
16
20
12
15
14
0
0
Prcrocentrum sp. C
0
0
2
4
94
34
0
0
0
Piotoperidinium spp
26
30
26
20
18
7
22
2
4
Cochlodinium catenatum
50
56
290
714
1,272
4,065
1,182
148
68
Gymnodinium splendens
0
0
0
2
0
341
300
0
0
Torodinium robustum
30
26
20
10
0
16
12
0
0
Umbilicosphaera sibogae
50
52
42
34
44
0
18
4
0
'Emiliania huxleyi
1,213
1,821
1,822
1,298
1,883
1,928
927
2,489
1,152
Mesodinium rubrum
8
2
6
8
2
8
4
8
14
Laboea spp
30
146
110
74
82
104
124
72
36
Lohmaniella spp.
68
128
116
94
134
154
218
78
50
'Includes some Clausocalanus.
167
FISHERY BULLETIN: VOL. 83, NO. 2
APPENDIX TABLE 2.— Diurnal profiles after storm.
Depth (m):
10
15
20
25
30
35
40
45
50
ZOOPLANKTON
Naupliar Acartia
Naupliar Labidocera
Naupliar Paracalanus"^
Naupliar Calanus
Naupliar Rhincalanus
Other nauplll
Female Acartia
Male Acartia
Copepodlte Acartia
Adult Labidocera
Copepodlte Labidocera
Adult and copepodlte
"Paracalanus"'
Appendicularians
Adult and copepodlte Oithona
Adult and copepodlte Euterpina
Euphausiid nauplii
Euphausiid calyptopis
Euphausiid furcilia
Chaetognaths
Female Calanus
Male Calanus
C V Calanus
C IV Calanus
cm Calanus
C II Calanus
C I Calanus
Adult Corycaeus
Adull and copepodlte Oncaea
Microsetella
Adult Metndia
Adull Pleuromamma
Copepodlte Metndia
and Pleuromamma
Adult Rhincaianus
Copepodlte Rhincalanus
Copepodlte Eucalanus
Other copepods
Fish eggs
Fish larvae
Cladocerans {Evadne )
Polychaete larvae
Lamellibranch larvae
Cyphonautes larvae
CHLOROPHYLL
PHYTOPLANKTON -r CILIATES
Nitzscnia spp S
Bacteriastrum spp. (chains)
Chaetocoros spp
Rhizosolenia alaia
Rhizosolenia fragilissima
Skeletorema costatum
Ceratium sop
Gonyaula\ pclyedra Ipclygramma
Prorocentrum sp C
Protcperidinium spp
Cuchiodinium catenatum
Gymnodinium splendens
Torodinium robustum
Umbiliccsphaora sibogae
Emiliania huxleyi
Mesodinium ruorurn
Laboea spp
Lohmanielia spp.
1,834
8,333
10,525
21,954
1 1'cuiai i 1 lu
6,583
1,867
197
153
60
0
57
1.600
4.679
0
0
0
0
0
0
0
0
0
2.644
10,114
3,669
5,576
7,219
7,810
5,015
1.651
972
888
1,115
950
810
424
2,180
1.833
837
456
391
193
128
196
0
631
0
95
134
9
204
228
0
36
124
2,740
14,601
15,091
18,210
14,232
8,216
5,327
3,990
3,414
2,570
1,927
0
5,666
69
9,736
6,617
3,994
0
1.907
0
0
0
0
5,645
27
14
6,617
7
0
0
0
0
0
36
643
1.758
1,756
1,807
288
0
1,905
1,903
0
0
0
0
0
0
0
0
0
0
0
0
0
153
79
7
0
0
0
0
0
0
0
0
5.646
6,200
1,726
1,796
2,279
4,808
6,434
3. 090
1 371
660
435
3,053
3,165
3.551
5,785
8,364
5,651
1,745
754
122
79
44
21
696
391
983
814
^ei?
1.953
1.014
:'30
567
516
5
229
1,196
2,358
962
190
80
23
0
25
0
0
0
171
0
214
9
19
33
27
26
25
0
13
11
89
41
38
21
2C
15
9
14
0
0
12
15
23
36
27
28
IS
16
20
8
164
511
251
190
60
42
24
12
6
12
0
0
0
0
0
0
0
22
8
8
4
0
0
0
0
0
0
0
20
4
0
4
0
0
0
116
0
11
12
18
12
0
4
0
68
0
119
45
16
32
6
0
8
0
0
0
0
119
90
43
14
8
0
0
0
7
0
297
27
50
46
11
0
0
0
0
7
79
303
15
31
25
12
0
0
0
C
20
107
337
305
478
74
87
69
43
46
43
0
711
255
215
707
2,678
3.466
2.011
1,797
1,322
1,204
14
40
719
476
45
171
236
190
23
37
33
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1,047
0
0
0
0
0
0
0
0
0
81
153
176
135
115
0
0
0
0
0
0
0
0
97
80
0
0
0
0
0
30
31
57
8
99
80
6
0
0
0
0
23
16
0
7
97
80
0
0
0
0
15
0
17
6
6
10
0
6
14
18
19
89
0
0
0
0
C
0
0
0
11
15
95
19
0
0
0
0
0
0
164
273
101
102
16
0
0
0
0
0
0
0
100
294
193
375
256
181
101
52
33
19
0
0
0
0
0
54
195
138
0
0
0
0
193
20
36
15
58
0
3
0
0
0
0.74
1.08
2.91
median micrograms per liter ■
2.05 0.86 0.62
median number oer 100 ml ■
0.52
0.36
67
48
0
0
0
0
0
130
0
0
20
24
8
4
4
a
12
0
7,957
3.186
265
1,416
1,099
696
87
565
174
28
24
8
16
8
0
0
0
0
44
16
36
8
4
0
0
0
0
0
0
0
0
0
0
0
0
24
64
80
72
104
56
0
0
4
0
16
56
88
32
16
0
0
0
0
20
4
681
784
296
4
0
4
0
48
64
72
40
16
4
0
0
C
52
363
1,837
1,672
1,720
680
56
52
4
0
0
672
583
320
4
C
0
0
24
24
26
28
8
0
0
0
0
0
104
40
56
32
4
0
0
0
1,681
1,504
3,009
1,858
609
1,130
696
1,478
973
16
24
32
IS
8
0
0
0
0
52
464
326
134
204
116
32
20
4
143
520
580
568
616
152
36
16
6
0.31
0.21
' Includes some Clausocalanus .
168
MULLIN ET AL.: VERTICAL STRUCTURE OF PLANKTON OFF CALIFORNIA
APPENDIX TABLE 3.— Nocturnal profiles before storm.
Depth (m):
10
15
20
25
30
35
40
45
50
ZOOPLANKTON
Naupllar Acartia
Naupliar Labldocera
Naupllar "Paracalanus"^
Naupliar Calanus
Naupliar Rhincalanus
Other nauplii
Female Acartia
Male Acartia
Copepodite Acartia
Adult Labidocera
Copepodite Labidocera
Adult and copepodite
Paracalanus^^
Appendicularians
Adult and copepodite Oithona
Adult and copepodite Euterpina
Euphausiid nauplii
Euphausiid calyptopis
Euphausiid furcilia
Chaetognaths
Female Calanus
Male Calanus
0 V Calanus
C IV Calanus
cm Calanus
C II Calanus
C I Calanus
Adult Corycaeus
Adult and copepodite Oncaea
Microsetella
Adult Metndia
Adult Pleuromamma
Copepodite Metndia
and Pleuromamma
Adult Rhincalanus
Copepodite Rhincalanus
Copepodite Eucalanus
Other copepods
Fish eggs
Fish larvae
Cladocerans (Evadne)
Polychaete larvae
Lamellibranch larvae
Cyphonautes larvae
CHLOROPHYLL
PHYTOPLANKTON ^ CILIATES
Nitzschia spp. S
Bactenastrum spp. (chains)
Chaetoceros spp.
Rhizosolenia alata
Rhizosolenia fragilissima
Skeletonema costatum
Ceratium spp
Gonyaulax polyedra polygramma
Prorocentrum sp. C
Protopendinium spp.
Cochlodinium catenatum
Gymnodinium splendens
Torodinium robustum
Umbilicosphaera sibogae
Emiliania huxleyi
Mesodinium rubrum
Laboea spp
Lohmaniella spp.
352
315
4,286
5.874
1 iicuiai 1 1 lu
6,723
Miuci per ui
1,992
0
43
0
0
0
1.636
870
75
0
0
0
0
0
0
0
0
5.282
4,229
2,491
2,379
2,500
8,352
2,215
1,277
1,051
1,041
748
691
441
1.008
744
2,033
579
340
81
81
41
71
0
72
0
8
8
97
23
0
0
0
0
2,636
5,507
7,143
1 1 ,822
12,602
9.650
2,764
3,333
2,358
2,073
1,594
14
8
25
59
52
16
0
0
0
0
0
21
0
25
16
21
4
0
0
0
0
0
45
47
517
1,784
2.546
83
72
4
0
0
0
0
0
0
0
0
0
0
0
0
0
0
532
98
75
80
0
0
0
0
0
0
0
3.040
2.047
2.264
2,066
2,033
6.364
3,574
3,191
2,412
1.165
435
2,535
2,907
3,218
4,164
6,134
1.736
488
255
45
37
7
282
157
1,345
2,231
3.821
1.992
1,824
1.404
545
805
725
67
36
130
2.320
1,736
413
130
0
0
0
0
0
0
4
33
4
17
0
8
4
0
0
14
13
4
40
46
21
0
4
0
4
7
8
4
4
24
25
19
47
26
33
73
7
45
141
189
252
142
93
85
41
28
22
11
0
0
0
4
16
4
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
11
17
15
21
4
0
4
0
0
0
14
14
17
19
10
4
4
0
4
0
4
0
0
4
0
16
50
10
0
0
0
0
0
0
0
12
21
161
20
0
0
0
0
0
4
13
4
49
119
9
0
0
0
0
14
16
91
123
142
194
163
119
70
61
36
240
157
0
0
325
3,636
3,453
1,707
1,284
1,487
1,143
141
394
613
1.440
1,220
579
488
71
19
33
36
0
0
0
0
0
4
0
20
33
15
7
0
0
0
4
0
11
23
45
28
26
18
4
0
4
45
29
153
293
203
167
134
112
0
0
0
0
0
0
0
0
0
0
0
0
0
8
7
10
23
51
33
4
0
0
0
0
0
0
0
12
8
8
0
0
0
4
4
0
0
0
0
0
8
12
23
24
4
0
0
0
3
0
0
0
0
0
0
21
7
67
59
28
11
8
0
0
0
0
120
101
13
4
0
4
0
0
0
0
0
14
22
50
96
366
257
169
80
12
31
32
0
0
0
0
0
0
0
0
0
0
0
0
0
0
20
8
4
0
0
0
0
0
0.24
0.29
0.49
0.68
median micrograms per liter-
0.85 1.82 1.42
median number per 100 ml ■
0.97
0.51
1,036
2,181
791
372
1,593
162
841
241
217
36
90
44
78
14
168
108
50
18
5,974
1,855
3,628
2,008
1,814
3,585
2,035
1,428
435
88
122
96
72
34
28
6
2
4
108
160
114
70
68
11
8
2
4
56
74
70
8
10
18
96
52
116
18
24
38
32
18
28
4
2
0
10
2
54
26
18
2
0
0
0
2
0
58
76
50
6
0
0
0
14
16
12
22
23
32
10
0
0
46
96
456
1,092
1.869
2.064
522
68
0
0
0
2
12
241
21
0
0
0
28
30
12
12
7
0
0
0
2
16
0
16
86
0
30
2
2
0
858
1.518
1,498
706
1.372
2,173
3,009
1,580
957
2
34
6
4
0
11
4
6
4
102
74
134
122
217
125
44
24
14
210
84
152
174
118
123
30
20
12
0.32
0.26
includes some Clausocalanus
169
APPENDIX TABLE 4.— Nocturnal profiles after storm.
FISHERY BULLETIN: VOL. 83, NO. 2
Depth (m):
10
15
20
25
30
35
40
45
50
ZOOPLANKTON
Naupliar Acartia
Naupliar Labidocera
Naupliar "Paracalanus"^
Naupliar Calanus
Naupliar Rhincalanus
Other nauplii
Female Acartia
Male Acartia
Copepodite Acartia
Adult Labidocera
Copepodite Labidocera
Adult and copepodite
"Paracalanus'^
Appendicularians
Adult and copepodite Oitliona
Adult and copepodite Euterpina
Euphauslid nauplii
Euphausiid calyptopis
Euphausiid furcilia
Chaetognaths
Female Calanus
Male Calanus
C V Calanus
C IV Calanus
cm Calanus
C II Calanus
C I Calanus
Adult Corycaeus
Adult and copepodite Oncaea
Microsetella
Adult Metridia
Adult Pleuromamma
Copepodite Metridia
and Pleuromamma
Adult Rhincalanus
Copepodite Rhincalanus
Copepodite Eucalanus
Other copepods
Fish eggs
Fish larvae
Cladocerans (Evadne)
Polychaete larvae
Lamellibranch larvae
Cyphonautes larvae
CHLOROPHYLL
PHYTOPLANKTON + CILIATES
Nitzschia spp. S
Bacteriastrum spp. (chains)
Chaetoceros spp.
Rhizosolenia alata
Rhizosolenia fragilissima
Skeletonema costatum
Ceratium spp.
Gonyaulax polyedra Ipolygramma
Prorocentrum sp. C
Protoperidinium spp.
Cochlodinium catenatum
Gymnodinium splendens
Torodinium robustum
Umbilicosphaera sibogae
Emiliania huxleyi
Mesodinium rubrum
Laboea spp.
Lohmaniella spp.
median number per cubic meter
6,590
9,360
17.323
18,008
15,106
11.371
660
176
90
230
0
1,172
1.181
394
336
0
0
0
0
0
0
0
4,908
5,256
7,591
4.370
5,184
9,091
6,400
3,424
1,345
1,073
1,126
1,099
1.378
1,969
1,533
1,082
1,489
495
467
545
236
260
0
0
0
0
0
167
7
4
0
0
0
3.678
7,102
12.795
27,969
11,873
12,553
8,000
6,154
5.364
4.245
3,520
11
23
66
138
13
0
0
0
0
0
0
11
28
17
123
27
0
0
0 •
0
0
0
280
661
1,575
2,299
1,505
3,617
32
0
0
0
0
11
0
0
0
0
0
0
0
0
0
0
119
80
31
15
0
0
0
0
0
0
0
4,215
3,977
2,953
2,490
1.915
4,013
5,400
2,731
1.887
720
1.039
2,835
4,400
4,921
5,556
2,814
4,255
4,200
881
377
307
80
172
394
495
347
1,003
1,505
1,800
952
755
169
560
57
142
110
1.261
3,617
167
165
16
27
5
0
0
0
0
0
0
0
14
9
14
20
13
57
40
37
83
17
4
13
7
9
8
0
11
0
29
61
27
13
11
26
9
16
9
95
100
202
215
54
112
49
57
9
19
9
0
0
0
15
17
0
0
0
0
0
0
0
0
0
0
0
0
4
0
0
0
4
4
11
0
15
9
13
0
0
4
0
0
4
23
26
0
43
27
7
0
0
4
0
7
31
26
31
34
80
13
0
0
0
0
0
16
26
42
43
85
0
0
0
0
0
7
16
8
0
0
68
7
0
0
0
0
11
0
47
252
732
190
130
55
45
28
14
230
240
94
1,513
1,003
2,766
4.400
1.868
1,345
1,792
1,200
115
320
495
347
426
334
660
78
245
46
20
0
8
16
0
0
13
7
4
9
5
0
8
16
16
0
0
0
32
44
31
5
9
8
8
16
17
0
202
366
229
188
88
44
0
0
0
0
0
0
0
0
0
0
0
0
0
12
0
17
67
18
4
9
0
4
0
0
0
0
0
0
0
0
5
0
0
4
0
0
15
27
51
16
18
54
15
26
0
16
4
0
0
0
0
0
0
0
0
0
0
26
42
0
0
0
0
0
0
0
29
197
330
17
0
0
0
0
0
0
4
18
20
106
276
272
334
165
311
47
27
20
0
0
0
0
0
0
0
0
0
0
0
0
0
4
56
121
67
25
0
0
0
0
1.17
1.34
2.87
3.87
median micrograms per liter
4.15 3.11 1.01
median number per 100 ml ■
0.61
0.46
88
0
0
88
0
0
0
43
130
194
9
8
0
0
0
12
12
0
5,221
9.469
3,363
442
4,071
4,690
783
174
217
56
19
32
19
8
0
0
4
0
83
0
0
111
0
0
4
20
0
0
0
0
0
0
0
40
0
8
111
46
80
167
32
24
4
0
2
0
28
40
37
41
0
0
0
0
556
806
1,360
1,704
290
88
4
0
0
56
102
32
0
16
16
12
0
2
1,833
1,519
1.488
3.259
3,343
3,424
516
56
10
306
352
464
370
4,102
1,016
32
0
0
56
37
64
74
16
40
4
0
0
28
9
24
74
24
16
4
0
0
1,062
1,327
1,858
1,416
2,035
2,035
1.652
1.043
478
389
176
72
241
14
16
12
0
0
472
222
344
389
97
400
72
36
8
528
435
512
1,185
207
552
180
24
4
0.38
0.35
'Includes some Clausocalanus.
170
DIEL AND DEPTH VARIATIONS IN THE SEX-SPECIFIC ABUNDANCE,
SIZE COMPOSITION, AND FOOD HABITS OF
QUEENFISH, SERIPHUS POLITUS (SCIAENIDAE)
Edward E. DeMartini/ Larry G. Allen ,2 Robert K. Fountain,^
AND Dale Roberts*
ABSTRACT
Lampara seine-hauls were taken during day and night over 5-27 m bottom depths off the coast of
northern San Diego County, California, from September 1979 to March 1981. These samples were used
to characterize the temporal and spatial patterns of the abundances and size and sex compositions of
queenfish, Seriphus politus, in an unprotected, coastal environment. Stomach contents of sample
queenfish were examined to aid our interpretation of these patterns.
Adult queenfish of both sexes made diel, onshore, and offshore migrations, but immature fish
generally did not. Both immatures and adults occurred in epibenthic, resting schools in shallow areas
( -10 m or less depth, within -1.5 km of shore) during the day. At night, adult fish dispersed (to >3.5
km ) offshore. On average, a greater fraction of the adult males emigrated farther offshore at night than
adult females. Immature fish remained inshore of 16 m bottom depths (within -2.5 km of shore) at
night, with the majority staying inshore of -10 m depth. Regardless of maturity class, larger fish
occurred farther offshore at night.
Stomach contents data confirmed the primarily nocturnal feeding habits of both immature and adult
queenfish. Immatures fed primarily on meroplankton and other nearshore prey; however, adults
captured offshore had also eaten some nearshore prey. Thus, food habits explain much, but not all of the
diel migratory pattern. Immature queenfish may also remain nearshore at night because migration is
not worthwhile energetically and because of greater risk of predation offshore. Adults perhaps also
migrate offshore at dusk to spawn.
Numerous physical and biological factors influ-
ence the spatial and temporal distribution pat-
terns of fishes. In response to such factors, coastal
marine fishes often undergo diel shifts in spatial
distributions (reviewed by Woodhead 1966; Blax-
ter 1970). Examples of horizontal (Hobson 1965,
1973; Hobson and Chess 1976; Quinn et al. 1980;
Allen and DeMartini 1983) and vertical or water-
column (Parrish et al. 1964; Woodhead 1964;
Beamish 1966) diel migrations are recognized.
Diel horizontal migrations may vary with life
stage (e.g., see Hobson and Chess 1973). The type
of diel vertical movement also may vary with sea-
son and with age and spawning condition of fish
(Hickling 1933; Lucas 1936; Brawn 1960; Blaxter
and Parrish 1965; Beamish 1966). In other cases,
relatively static differences between the depth dis-
tributions of juvenile and adult life stages have
^Marine Science Institute, University of California, Santa
Barbara, Calif; present address: Marine Review Committee Re-
search Center, 531 Encinitas Boulevard, Suite 114, Encinitas,
CA 92024.
Marine Science Institute, University of California, Santa
Barbara, Calif.; present address: Department of Biology, Califor-
nia State University, Northridge, CA 91330.
Manuscript accepted March 1984.
FISHERY BULLETIN; VOL. 83, NO. 2, 1985.
been documented (reviewed by Helfman 1978).
Spatial segregation of adult males and females
has been commonly observed only in tropical reef
fishes (Moyer and Yogo 1982; Clavijo 1983; and
others).
This study describes the manner in which a
complex interplay of the factors listed above can
determine the temporal and spatial patterns of the
distribution of a temperate marine fish. Specifi-
cally, we report on diel shifts in the onshore,
offshore distribution of queenfish, Seriphus
politus, characterize the variation in these diel
shifts for immature, adult male, and adult female
fish, and relate these shifts to feeding, anti-
predator, and breeding functions previously de-
scribed.
The queenfish is a small, schooling sciaenid
whose center of geographic distribution lies in the
Southern California Bight, south of Point Concep-
tion (Miller and Lea 1972). The species contributes
significantly to the sport fish catch on piers in
southern California (Frey 1971) and provides for-
age for several game fishes (Young 1963; Feder et
al. 1974). Queenfish form inactive, epibenthic
schools nearshore (at — 10 m or less bottom depth)
171
FISHERY BULLETIN: VOL. 83, NO. 2
during the day (Hobson and Chess 1976; Allen and
DeMartini 1983). Queenfish are dispersed
throughout the water column and also occur
farther offshore (to 20-30 m depths) at night,
where they feed (Hobson and Chess 1976; Hobson
et al. 1981; Allen and DeMartini 1983) and perhaps
spawn (DeMartini and Fountain 1981).
This study represents part of an ongoing en-
vironmental impact assessment of the fishes of
coastal waters off San Onofre Nuclear Generating
Station near Oceanside, Calif., using the
queenfish as a target species. Recognition of poten-
tially complex patterns of spatial and temporal
distribution has general applicability for the de-
sign and interpretation of analogous monitoring
studies and for other assessments of nearshore fish
stocks (June 1972).
METHODS AND MATERIALS
Sampling Design
Catches made by lampara seines (a type of
semipursing, roundhaul net, Scofield 1951) were
used to characterize the distribution and abun-
dance of queenfish in terms of catch per unit effort
(CPUE), where a standard-area seine-haul was
defined as the unit of effort (Allen and DeMartini
1983). All queenfish present in each seine-haul
were counted aboard ship. Seines fished from sea
surface to seabed over bottom depths from 5 to 27
m. For diel comparisons, a total of 14 pairs of "day"
(1-6 h after sunrise) and "night" (1-6 h after sunset)
cruises were made during the period from Sep-
tember 1979 to March 1981, inclusive. On each
cruise, 1 or 2 seine-hauls were made within ran-
domly selected subareas within each of three
depth blocks (shallow, 5-10 m, 0.5-1.5 km offshore;
middepth, 11-16 m, 1.5-2.5 km offshore; deep, 18-27
m, 2.5-3.5 km offshore) at each of two longshore
locations, about 5 and 22 km upcoast of Oceanside,
Calif. Two replicate hauls were made at each
longshore location in the shallow depth block
(wherein catches were most variable) on day
cruises, and the two catch values averaged. For a
chart of the study area and further details of gear
and sampling designs, see Allen and DeMartini
(1983).
CPUE and Size-Composition Data
A maximum of two subsamples of —50 individu-
als each of queenfish of all sizes were randomly
selected from each seine-haul and placed on ice
172
aboard ship. In the laboratory, all fish in the sub-
samples were sexed macroscopically (DeMartini
and Fountain 1981) into immatures (of both sexes),
adult males, adult females, and sex indetermin-
able. (Fish of indeterminable sex comprised <5%
of total catch.) Fish were measured to the nearest
millimeter standard length (SL) and grouped into
5 mm length classes for analysis. For seine-hauls
in which the total number of queenfish caught
exceeded the total number measured, the numbers
of fish of each maturity and sex category caught
were estimated from the respective number mea-
sured, standardized to the total number of
queenfish caught. In these cases, the length fre-
quencies of the fishes in each sex category mea-
sured were then weighted by the estimated
number of that category present in the haul.
Queenfish length-frequency data were com-
pared between diel periods and depth blocks by
Kolmogorov-Smirnov Two-Sample test (Siegel
1956). A nonparametric 3-way ANOVA (Wilson
1956), available in the IMSL Library's^ statistical
package, was used to simultaneously evaluate the
effects of diel period, depth block, sampling date
(cruise), and their potential interactions on the
numerical CPUE of immature, adult male, and
adult female fish. In all ANOVA analyses, catches
made w.ithin the same depth block at the two long-
shore locations on a given cruise were considered
separate estimates, as differences between loca-
tions were sometimes evident.
Food Habits
Additional subsamples of one queenfish per 10
mm SL length class were randomly selected from
seine-hauls for analysis of food habits. Fish were
examined from a larger series of 11 day and 23
night cruises (that included 8 of the aforemen-
tioned 14 paired, day/night cruises) conducted
during September 1979-October 1980. These sub-
sampled fish were placed in lO^c Formalin'*
immediately following capture, after their abdom-
inal walls had been slit to accelerate preservation.
Stomachs were dissected and placed in 70% ethyl
alcohol after about 1 wk of fixation. Contents of
stomachs were scored for state of digestion on a
scale of 0 (undigested) to 10 (prey present but to-
tally indistinguishable). All prey were identified
to lowest taxonomic category, their numbers tal-
'IMSL Library, Sixth Floor, NBC Building, 7500 Bellaire
Blvd., Houston, TX 77036.
■* Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
DeMARTINl ET AL: DISTRIBUTION PATTERNS OF QUEENFISH
lied, and reconstructed wet weight biomass esti-
mated (to the nearest milligram, based on a key of
reference prey weights). Values were summed for
the aggregate of each taxon in each stomach. A
compound measure of numbers (N), weight (Wt),
and frequency occurrence (FO) of prey (IRI =
{(%N + 7r Wt)%FO}; Pinkasetal. 1971) was used
to characterize temporal and spatial variations in
the overall importance of various prey to the diet of
immature and adult male and female queenfish.
RESULTS
Catch per Unit of Effort
A large majority of the adults of both sexes, as
well as immature queenfish, occurred at shallow
depths (5-10 m) during daylight hours throughout
most of the year (Fig. 1). A plurality of immature
and adult fish of both sexes occurred at shallow
depths at night as well; however, the distribution
of numbers spread farther offshore at night, espe-
cially for adult fish (Fig. 1). The nocturnal offshore
distribution appears to have been especially
marked for adult males (Fig. IB). This diel shift in
the depth distribution of queenfish is charac-
terized by the diel-by-depth interaction term in
the ANOVA (Table 1). The (nearly) significant date
effect for adults (and insignificant date effect for
immatures) in the ANOVA (Table 1) reflects the
general offshore emigration of adult, but not im-
mature, queenfish during late fall and early
Table l. — Results of Wilson's Three- Way Non-
parametric ANOVA with equal replication (Wil-
son 1956) for the effects of diel period (day, night),
bottom depth (5-10, 11-16, 18-27 m), and date
(cruise ) on the lampara seine CPUE of immature,
adult male, and adult female queenfish. Data for
14 paired, day/night cruises made during the
period from September 1979 to March 1981, inclu-
sive. (* denotes significance at P s 0.05).
Maturity'
sex category
Factor
/
df
P
Immatures
Diel
27.5
1
<o.oor
Depth
52.0
2
<o.oor
Date
10.0
13
0.69
Diel X Depth
9.3
2
o.or
Diel X Date
7.8
13
086
Depth X Date
14.0
26
0.97
Dx DxD
11.3
26
0.99
Adult males
Diel
34.4
1
<o.oor
Depth
38.9
2
<-o.oor
Date
19.9
13
0 10
Diel X Depth
5.2
2
0.08
Diel X Date
5.6
13
096
Depth X Date
13.1
26
0.98
Dx Dx D
14.8
26
0.96
Adult females
Diel
50.6
1
' 0.001 •
Depth
16.1
2
<o.oor
Date
30.0
13
0.005-
Diel X Depth
14.0
2
0.001 •
Diel X Date
7.0
13
0.90
Depth X Date
11.4
26
0.99
Dx DxD
10.8
26
1.00
IMMATURE
C
FEMALE
DEEP
Figure l. — Bar histogram chart of arithmetic mean CPUE (catch per seine haul) during the day versus at night,
in the shallow (SHAL, 5-10 m), middepth (MID, 11-16 m), and deep (DEEP, 18-27 m) depth blocks, for immature,
adult male, and adult female queenfish. All data represent samples from 14 paired, day /night cruises made from
September 1979 to March 1981, inclusive.
173
FISHERY BULLETIN: VOL. 83, NO. 2
winter (also see Allen and DeMartini 1983). The
patterns illustrated by Figure 1 remained consis-
tent throughout most of the year, when queenfish
occurred nearshore (also see below).
Size Composition
bled the size distribution of the respective cate-
gory caught at night at 5-27 m depths (Fig. 4A, B,
C), even though the large numbers of fish mea-
sured (hence great power) yielded statistically
significant differences (Table 2). Clearly, queen-
fish present at 5-27 m depths at night occur at 5-10
The size composition of queenfish within sex and
maturity classes also generally differed between
diel periods within depth blocks (Fig. 2, Table 2).
Adult males, adult females, and immature fish of
both sexes were of generally larger body sizes in
day versus night samples within the shallow
depth block (Fig. 2, Table 2). At night, larger sized
queenfish of all categories occurred in samples
from middepths versus the shallow region (Fig. 3,
Table 2).
The diel differences in the size composition of
queenfish within depth blocks generally dis-
appeared when catches were pooled over depth
blocks throughout the year (Fig. 4). Specifically,
the length-frequency distribution of each sex
category in day-shallow samples closely resem-
TABLE 2. — Results of Kolmogorov-Smirnov Two Sample com-
parisons (Siegel 1956) of the length-frequency distributions of
sample queenfish of various sex and maturity classes between
diel periods and/or depth blocks. Based on all 14 D/N pairs of
cruise data for the period September 1979-March 1981. See
Figures 2-4 for data histograms.
Sign
ificance
Comparison
Dmax
Dcrit 0.05
evel
Day vs. night, shallow depths
Immatures
0 10
003
P ■
0,001
Adult males
028
0,05
P
0,001
Adult females
022
0,06
P
0,001
Shallow vs- mid-depths, at night
Immatures
0,26
006
P
0,001
Adult males
0.24
0,06
P
0,001
Adult females
0,12
0,09
0,01
P 0 001
Day-shallow vs. njght-ali depths
Immatures
0,03
0,03
P
0,05
Adult males
0.11
0,03
P
0,001
Adult females
0.14
0,04
P
0,001
IMMATURE QUEENFISH
SIZE FREQUENCIES
DEPTH=.5-10 M
DAY N=9394
NIGHT N=2247
UJ
o
cr
O
(J
o
u.
o
>-
o
UJ
o
UJ
a:
UJ
(J
X
z
10-
5-
0--
5-
10-
15-
10
20
30
40
rrrrp,
50
rrrrp-,
80
70
""I"
eo
90
'"I""
100
no
120 130 IdO
150
STANDARD LENGTH (MM)
Figure 2. — Relative (percenti length-frequency distributions of lAi immature, <Bi adult male, and (C) adult female
queenfish, caught during the day versus at night in the shallow depth block (see Figure 1 caption for details). Day/night
data are plotted above, below the horizontal axis in each panel.
174
DeMARTlNl ET AL: DISTRIBUTION PATTERNS OF QUEENFISH
ADULT MALE QUEENFISH
SIZE FREQUENCIES
DEPTH = 5-10 M DAY N = .323e NIGHT N»984
X
o
z
LiJ
UJ
cr
cr
Z)
u
o
o
o
>-
(J
3
o
LjJ
15-
10-
5-
0--
5-
10-
15-
20-
50
""1 1 1 1"
BO 70 80 90
'"I I I I I 1 1 1 1 1 1 1
100 110 120 130 140 150 160 170 160 190 200
ADULT FEMALE QUEENFISH
SIZE FREQUENCIES
DEPTH=5-10 M DAY N=3292 NIGHT N=S42
Ld
O
Ld
Q.
<
a
X
o
z
20-
15-
10-1
0--
10-
15-
60
c
'"1 1"
80 90
■"I ' I I I I I I I I ' I I
100 110 120 130 140 150 160 170 160 190 200 210 220
STANDARD LENGTH (MM)
175
FISHERY BULLETIN: VOL. 83, NO. 2
IMMATURE QUEENFISH
SIZE FREQUENCIES
NIGHT 5-lOM DEPTH N=2247 NIGHT 11-16M DEPTH N=725
n
a.
lit
a
I
o
liJ
O
z
UJ
a:
Z)
o
o
o
u.
o
>-
o
z
LJ
o
UJ
10-
5-
5-
10-
15-
30
40
' ' ' ' I I ■
50 80
70
80
90
"I I "
100 110
ADULT MALE QUEENFISH
SIZE FREQUENCIES
NIGHT 5-lOM DEPTH N=984 NIGHT 11-16M DEPTH N=1096
" 1 I ■
120 130
z
UJ
o
a:
a- §
a.
UJ
o
I
a
20-
15-
10-
5-
10-
15-
B
'I I T"' I"
80 70 80 90
100
'"1""
110
'I I'
MO 150
'"I""
180
^V
120 130 MO 150 180 170
STANDARD LENGTH (MM)
"■1 1 1 1 1""
180 190 200 210 220
176
DeMARTINI ET AL: DISTRIBUTION PATTERNS OF QUEENFISH
ADULT FEMALE QUEENFISH
SIZE FREQUENCIES
NIGHT 5-lOM DEPTH N=642 NIGHT 11-16M DEPTH N=350
LiJ
O
q:
O
(J
o
>-
o
UJ
o
ir
UJ
Q.
o
X
en
g
2
10-
0--
5-
10-
15-
c
5
1'"
0
60
70
r"
80
I'"
90
1""
100
""1 1
110 120
STANDARD
'"1 1 1""
130 140 150
LENGTH (MM)
160
— I —
170
180
190
""] !
200
Figure 3. — Relative length-frequency distributions of (A) immature, (B) adult male, and (C) adult female queenfish
caught during the night in the shallow versus middepth blocks (see Figure 1 caption for details). (Data for the deep depth
block were too few to evaluate independently. )
m depths nearshore during the day (also see Dis-
cussion and Conclusions).
In order to further aid our interpretation of the
function of the observed nocturnal offshore move-
ments, we subdivided our diel catch data into three
periods of year: 1) February-July (the onshore,
breeding season; see DeMartini and Fountain
1981); 2) August-October (the onshore, non-
breeding season); and 3) November-January
(the offshore, nonbreeding season). Analyses were
restricted to size-frequency data for queenfish
seined at shallow and middepths during the two
periods of onshore distribution, as scant data on
the size composition of adults were available for
the offshore season. During both breeding and
nonbreeding onshore periods, queenfish seined at
shallow depths were larger during the day versus
at night, and fish caught at night were consis-
tently larger in middepth versus shallow collec-
tions (Table 3). Thus the year-round patterns
illustrated by Figures 2 and 3 also basically
characterize both breeding and nonbreeding
periods of onshore distribution.
Food Habits
The food habits of immature, adult male, and
adult female queenfish were evaluated for day and
night collections made in the shallow- and mid-
depth blocks during the onshore, breeding and
onshore, nonbreeding periods of year (Stomachs of
fish from the deep depth block were not examined. )
The purpose of these comparisons was to help
interpret the relative importance of the feeding
and breeding functions of diel offshore movements.
We hypothesized that immature fish might remain
onshore at night to feed on meroplanktonic (noc-
turnally active) demersal crustaceans and other
prey more abundant at shallow depths. We further
expected that adults emigrated offshore to spawn
(DeMartini and Fountain 1981) and thereafter fed
on relatimely larger prey that were more preva-
lent farther offshore. In general, immature
queenfish fed on smaller prey than adult males,
and adult males, being smaller than adult
females, fed on generally smaller prey than
females (Table 4). Contrary to expectations, adult
177
FISHERY BULLETIN: VOL. 83, NO. 2
IMMATURE QUEENFISH
SIZE FREQUENCIES
DAY 5-lOM DEPTH N=9394 NIGHT 5-27M DEPTH N=3013
I
X
o
z
UJ
O
Z
UJ
q:
a:
o
o
o
u.
o
>-
o
z
llJ
z>
o
UJ
on
u.
UJ
o
UJ
Q.
i
10-
5-
0--
5-
10-
15-
I I I [ 1 1 1 1"! I I iiimiiiii»iniiiiMnn ii*! j I
0 10 20 30 40 50 80 70 80 90 100 110 120 130 140 150
ADULT MALE QUEENFISH
SIZE FREQUENCIES
DAY 5-lOM DEPTH N=3238 NIGHT 5-27M DEPTH N=3155
'I iijii mill n 1 1*1 II iiji ;iiiiiiii>pinniii[iniMiii[i ■iiliiii[iMi |ii |iiii [ III! imtiMi ji \t |llllllli« |
80 70 80 90 100 110 120 130 140 150 180 170 180 190 200 210 220
STANDARD LENGTH (MM)
178
DeMARTINI ET AL: DISTRIBUTION PATTERNS OF QUEENFISH
Ld
O
cr
o
o
o
o
>-
o
u
o
UJ
ij- 1-
^- <J
UJ
o
UJ
Q.
20-
15-
10-
5-
5-
10-
15-
ADULT FEMALE QUEENFISH
SIZE FREQUENCIES
DAY 5-lOM DEPTH N-3292 NIGHT 5-27M DEPTH N-1288
c
--
--
f
--
...
--■
--
--
...
--
--
--
.
--
--■
— 1 — 1 — 1 — 1
....
....
....
....
....
...,
....
•■■■•■■■■1 1 1 1
80 70 80 90 100 110 120 130 140 150 160 170 180 190 200 210 220
STANDARD LENGTH (MM)
Figure 4. — Relative length-frequency distributions of (A) immature, (B) adult male, and (C) adult female queenfish caught
during the day in the shallow depth block versus during the night in all depth blocks pooled (see Figure 1 caption for details).
Table 3. — Results of Kolmogorov-Smirnov Two Sample comparisons of the diel- and
depth-specific length-frequency distributions of queenfish caught during the onshore,
breeding versus onshore, nonbreeding periods of year. Qualitative results of compari-
sons are noted.
Breeding
Nonbreeding
D>N?
Dmax
P
D>N?
Dmax
P
Day vs. night, shallow depths
Immatures yes
Adult males yes
Adult females yes
0.37
0.06
0.28
<0.001
0.05
<0.001
yes
yes
yes
0.10
0.10
0.25
<0.001
0.05 >P> 0.01
<0.001
Mid > Shal?
Dmax
P
Mid > Shal?
Dmax
P
Shallow vs. mid-
Immatures
Adult males
Adult females
depths, at night
yes
yes
yes
0.19
0.32
0.15
<0.001
<0.001
0.01
yes
yes
no
0.33
0.12
0.14
<0.001
0.05
>0.1
queenfish of both sexes, as well as immatures, fed
to large extents on prey (Table 4) whose centers of
abundance were shallow (see Discussion and Con-
clusions). For immatures such major prey included
holoplankton {Labidocera trispinosa) and mero-
planktonic cumaceans (primarily Diastylopsis
tenuis) (Table 4). Diastylopsis tenuis and other
nearshore crustaceans also comprised nontrivial
fractions of the diet of adult queenfish d\iring the
periods of onshore depth distribution (Table 4).
Diastylopsis tenuis, a night-active meroplankter
characteristic of the shallow region (see below),
also occurred in the stomachs of fish collected at
shallow depths during the day and during the
night at middepths. Hence we feel justified to
characterize the queenfish diet using data for both
diel periods and depth blocks pooled in Table 4.
State of prey digestion, though, tended to be less at
179
FISHERY BULLETIN: VOL. 83, NO. 2
Table 4. — Prey taxa comprising ^1*^ of the diet (by IRI) of immature, adult male, and
adult female queenfish during the two periods of onshore distribution combined. Sample
fish collected during both day and night and at shallow (5-10 m) and middepths (11-16 m)
are pooled (see text). Diet characterized by number (N), reconstructed wet weight (Wt), and
frequency of occurrence (FO) of prey; overall contribution to diet evaluated by IRI (Pinkas et
al. 1971). Prey ranked by IRI within queenfish categories. A^ = number of fish examined
that had food in their stomachs. Mean (and range I of body lengths (SL, mm) of fish examined
were immatures — 70 (34-100), adult males— 127 (76-210), and adult females — 146 (102-
214).
%
Mean Wt/
Type of prey
IRI
%A/
%wt
%FO
prey (mg)
Immatures {n = 57)
Labidocera thspinosa
holoplanktonic
copepod
35.8
26.7
3.2
56.1
<0.2
Acartia tonsa
holoplanktonic
copepod
20.9
40.2
2,8
22.8
<0.1
Metamysidopsis elongata
meroplanktonic
mysid
15.6
5.9
7.9
52.6
1.7
Engraulis mordax
clupeold fish
9.0
1.1
11.6
33.3
13.7
Diastylopsis tenuis
meroplanktonic
cumacean
5.1
3.6
3.2
35.1
1.1
Ogyrides sp.
? meroplanktonic
caridean shrimp
2.4
<0.1
31.9
3.5
472
Atylis tridens
meroplanktonic
amphipod
2.1
2.0
2.6
21.1
1.7
Acanthomysis macropsis
meroplanktonic
mysid
1.3
0.6
2.2
21.1
4.7
Blephahpoda occidentalis
? meroplanktonic
megalops/juvs.
1.0
0.2
9.0
5.3
53.0
(anomuran)
All other prey
6.8
19.6
25.6
—
1.7
Adult males (n = 228)
Engraulis mordax
clupeoid fish
74.6
6.3
89.0
47.8
385
Diastylopsis tenuis
meroplanktonic
cumacean
7.1
18.4
0.9
224
1.3
Metamysidopsis elongata
meroplanktonic
mysid
6.4
10.0
08
36.4
2.1
Labidocera trispinosa
holoplanktonic
copepod
6.4
14.9
0.1
25.9
<0.2
All other prey
5.5
50.4
92
—
5.0
Adult females (n = 236)
Engraulis mordax
clupeoid fish
78.9
5.7
90.8
52.1
783
Metamysidopsis elongata
meroplanktonic
mysid
6.5
10.8
0.5
36.4
2.3
Diastylopsis tenuis
meroplanktonic
cumacean
3.7
10.8
0.3
21.2
1.2
Labidocera trispinosa
holoplanktonic
copepod
3.1
10.2
<0.1
19.4
<0.2
Acanthomysis sculpta
meroplanktonic
mysid
1.4
6.1
0.5
13.6
3.6
Caridean shrimp
? meroplanktonic
1.0
3.4
0.6
15.7
8.7
All other prey
5.4
53.0
7.3
—
6.9
night for both immature and adult queenfish
(Table 5), indicating that all sizes of fish fed
primarily at night.
DISCUSSION AND CONCLUSIONS
Functions of Nocturnal
Offshore Dispersal in Queenfish
Diel migrations of queenfish have been previ-
ously reported. Queenfish have been directly ob-
served emigrating offshore at dusk from inactive
daytime schools nearshore at Santa Catalina Is-
land, one of the Channel Islands offshore of the
southern California mainland (Hobson and Chess
1976; Hobson et al. 1981). Similar behavior has
been noted by Hobson^ in mainland waters off La
Jolla, near San Diego. Allen and DeMartini (1983)
have characterized the general pattern of noctur-
nal offshore dispersal of queenfish near San Diego.
Direct observation (Hobson and Chess 1976; Hob-
son et al. 1981) and examination of stomachs offish
collected during the day and at night (Hobson and
Chess 1976; Hobson et al. 1981; Allen and DeMar-
tini 1983; this study) confirm the primarily noc-
turnal feeding habits of queenfish. A spawning
function has also been implicated for the offshore
movements of adult queenfish at dusk (DeMartini
'Edmund S. Hobson, Southwest Fisheries Center Tiburon
Laboratory, National Marine Fisheries Service, NOAA, 3150
Paradise Drive, Tiburon, CA 94920, pers. commun. May 1978.
180
DeMARTINI ET AL: DISTRIBUTION PATTERNS OF QUEENFISH
Table 5. — Results of Spearman's
rank correlations (Siegel 1956) be-
tween index of state of digestion of
stomach contents and time of collec-
tion for immature, adult male, and
adult female queenfish. All samples
collected prior to midnight. Sample
fish collected during day, night, and at
shallow (5-10 m) and middepths
(1 1-16 m) are pooled over both onshore
periods of distribution (see text).
Digestion versus time
rho
N
Immatures
Adult males
Adult females
-0.35
-0.20
-0.22
57
228
236
0.007
0.003
;0.001
and Fountain 1981). During the February-July/
August spawning season, ripe females with
ovaries in hydrated (ready-to-spawn) condition
can be collected throughout the daylight period
beginning 1 h after sunrise, while females col-
lected as soon as 1 h after sunset are either ripen-
ing (but nonhydrated) or are recently spent (De-
Martini and Fountain 1981).
The diel distributional (CPUE) data of this
study (Fig. 1) clearly illustrate the differences in
diel migration made by immature, adult male, and
adult female queenfish. Size-composition data
(Figs. 2-4) further characterize the diel migrations
as related to size of fish, regardless of maturity
state or whether adults in the populations were
reproductively active.
Certain aspects of the diel CPUE data suggest a
breeding function for offshore dispersal at night,
since only the distribution of immatures remained
centered onshore at night. Also, a dispropor-
tionately greater number of adult males versus
females emigrated offshore at night (Fig. IB, C).
This is consistent with an offshore migration by
females for spawning that occurs on a less fre-
quent than daily basis, since individual female
queenfish ripen and spawn batches of eggs on av-
erage only once a week (DeMartini and Fountain
1981). The male-biased, daytime aggregations of
ready-to-spawn queenfish (DeMartini and Foun-
tain 1981) suggest that individual males spawn at
more frequent than weekly intervals. Also, pre-
flexion stages of queenfish larvae are most abun-
dant in midwaters over 12-45 m bottom depths
from 1.9 to 5.4 km offshore in the region of San
Onofre-Oceanside (Barnett et al.^), which strongly
suggests that most spawning occurs in outer near-
shore regions.
Other distributional data, however, indicate a
primarily feeding function for offshore dispersal
at night. The nighttime, offshore shift in the dis-
tribution of adults of both sexes, for example, oc-
curred during both the nonbreeding and breeding
seasons. In addition, relatively more of the larger
individuals among the immatures (as well as more
of the larger adults of both sexes) moved offshore
at night (Fig. 3) from the shallow region wherein
queenfish of all sizes co-occurred during the day
(Figs. 1, 4). The latter pattern persisted during
both breeding and nonbreeding periods of year
when distributions were generally inshore of 30 m
bottom depth. On balance, the size composition of
immature and adult female queenfish censused at
5-27 m depths at night resembled the composition
of those censused at 5-10 m depths during the day
(Fig. 4A, C), indicating that few very large imma-
tures or females move offshore of 27 m at night.
This moreover confirms that the queenfish seined
offshore at night had resided at 5-10 m depths
during the day and not in a region (e.g., shallower
or deeper) that we did not census. Analogous data
for adult males (Figs. 1, 4B) indicate that this may
not be true for the largest males. However, the
pattern of larger individuals farther offshore per-
sisted for males as well as immatures and females
during the nonbreeding period.
The diel food habit data also are largely consis-
tent with the hypothesis that queenfish disperse
offshore at night to feed, despite several dis-
crepancies. Certain prey are known to be much
more abundant at either extreme of the queenfish
depth distribution. The presence of shallow-living
"marker" species such as Diastylopsis tenuis (Ta-
ble 6) in the stomachs of queenfish collected
offshore of the respective prey distribution likely
reflects some feeding activity just prior to or dur-
ing the dusk offshore emigration. The presence of
some night-active meroplankton in stomachs of
fish collected during the day probably represents
the partial confounding of nighttime foraging by
circumdiel gut residence times. We consider it un-
likely that queenfish feed on prey such as D. tenuis
during the day, as the nocturnal activity patterns
of this and other species of demersal meroplankton
"Barnett, A. M., A. E. Jahn, P. D. Sertic, and W. Watson. Long
term average spatial patterns of ichthyoplankton off San Onofre
and their relationship to the position of the SONGS cooling
system. A study submitted to the Marine Review Committee of
the California Coastal Commission, July 22, 1980. Unpubl.
rep., 32 p. Marine Ecological Consultants of Southern Califor-
nia, 531 Encinitas Boulevard, Encinitas, CA 92024.
181
FISHERY BULLETIN: VOL. 83, NO. 2
Table 6. — Prey taxa comprising ^1% of the diet (by IRD of immature, adult male, and
adult female queenfish collected during the night from the mid-depth (11-16 m) block. Data
for the two periods of onshore distribution are pooled; for further details of diet characteriza-
tion see Table 4. Mean (and range) of body lengths (SL, mm) were immatures — 71 (42-86),
adult males — 126 (83-183), and adult females— 147 (103-207).
%
N^ean Wt/
Type of prey
IRI
%A/
%wt
%F0
prey (mg)
Immatures (n = 1 4)
Engraulis mordax
clupeoid fish
25.2
2.6
27,2
42,9
16.8
Metamysidopsis elongata
meroplanktonic
mysid
23.3
7.3
9,3
71,4
2.1
Acartia tonsa
holoplanktonic
copepod
16.4
55.0
3,2
14.3
<0.1
Labidocera trispinosa
holoplanktonic
copepod
15.0
16,2
1,6
42.9
<0.2
Ampelisca brevisimulata
? demersal
amphlpod
3.8
1,3
12,2
14.3
15.0
Diastylopsis tenuis
meroplanktonic
cumacean
3.5
3,3
2,9
28.6
1.4
Acanthomysis macropsis
meroplanktonic
mysid
3.1
1.3
4,2
28.6
5.2
Ampelisca cristata
? demersal
amphipod
2.8
1,6
18,2
7.1
18.0
Blepharipoda occidentalis
? meroplanktonic
juveniles
1.8
0,3
12.4
7.1
61.2
(anomuran)
Hemilamprops californica
meroplanktonic
amphipod
1.6
2,3
0.6
28.6
0.4
All other prey
3.5
8,8
8.2
—
1.6
Adult males (n = 125)
Engraulis mordax
clupeoid fish
82.4
11,0
95.5
53.6
463
Labidocera trispinosa
holoplanktonic
copepod
5.8
20,8
■0,1
19,2
<0.2
Metamysidopsis elongata
meroplanktonic
mysid
4.0
84
0.4
31,2
23
Diastylopsis tenuis
meroplanktonic
cumacean
3,2
12,2
0,3
17.6
1.3
All other prey
4.6
47,6
3,8
—
4.2
Adult females [n = 89)
Engraulis mordax
clupeoid fish
83.6
9 1
93,0
59.6
615
Metamysidopsis elongata
meroplanktonic
mysid
6,5
15,6
0,7
29.2
2.6
Diastylopsis tenuis
meroplanktonic
cumacean
2,5
11,6
0,2
15.7
1.2
Labidocera trispimsa
holoplanktonic
copepod
1,8
7,3
<0,1
18.0
<0.2
Hemilamprops californica
meroplanktonic
amphipod
1,0
8,1
<0,1
9.0
0.4
All other prey
4.6
48,3
6,0
—
7.5
are well recognized (Barnard and Given 1961;
Hobson and Chess 1976).
The significant amount of shallow-living prey
such as D. tenuis and Labidocera trispinosa pres-
ent in the stomachs of queenfish captured offshore
at night (Table 6) nonetheless clearly illustrates
that these fish had recently emigrated from depths
nearer to shore. Numerous data characterize D.
tenuis as largely restricted to within the 30 m
isobath (Barnard and Given 1961; Parr and
Diener'). Diastylopsis tenuis, in fact, declines >1
order of magnitude in abundance in benthic core
^Parr, T. D., and D. D. Diener San Onofre sand bottom
benthic studies, San Onofre Nuclear Generating Station
(SONGS) Units 2 and 3, pre-oi>eration monitoring results. Vol-
ume 2. A study submitted to the Marine Review Committee of
the California Coastal Commission, May 8, 1981. Unpubl. rep.,
109 p. Marine Ecological Consultants of Southern California,
531 Encinitas Boulevard, Encinitas, CA 92024.
samples between 8 and 15 m depths near San
Onofre (Parr and Diener footnote 7). Labidocera
trispinosa, a holoplanktonic copepod, also has
been described as much more abundant inshore of
12-15 m bottom depths, both off La Jolla (Barnett
1974) and off San Onofre-Oceanside (Barnett et
al.^). It seems less likely that nearshore forms
such as D. tenuis andL. trispinosa are more avail-
able as prey offshore at night, since they are
markedly less abundant offshore.
The presence of offshore prey in the stomachs of
adult queenfish collected offshore obviously re-
flects nocturnal foraging while in that region.
^Barnett, A. M., A. E. Jahn, P D. Sertic, and S. D. Watts. The
ecology of plankton off San Onofre Nuclear Generating Station,
Volume II. A study submitted to the Marine Review Committee
of the California Coastal Commission, April 30, 1981. Unpubl.
rep., 105 p. Marine Ecological Consultants of Southern
California, 531 Encinitas Boulevard, Encinitas, CA 92024.
182
DeMARTINI ET AL: DISTRIBUTION PATTERNS OF QUEENFISH
Neomysis kadiakensis, a mysid more abundant at
depths corresponding to those frequented by adult
queenfish at night (Clutter 1967; Bernstein and
Gleye^), was a nontrivial component of the diet of
adult queenfish that ranked third by weight in
both males and females (although <1% of the total
IRI for each sex). None of the immature queenfish
that we sampled, however, had eaten any A^.
kadiakensis, even its juvenile stages (which also
occur offshore, Bernstein and Gleye footnote 9).
Nearshore prey, such as L. trispinosa and the de-
mersal meroplankter, D. tenuis, were generally
more important by weight and frequency of occur-
rence, if not numbers, in the diet of immature
versus adult queenfish (Table 4). The tendency for
immatures to remain closer to shore than adults
and to feed on meroplankton (that are more abun-
dant in sheltered areas closer to shore) has been
noted for many species of nocturnal zooplank-
tivorous fishes on tropical coral reefs (Hobson and
Chess 1978).
Both immature and adult queenfish are concen-
trated nearshore during the day, probably in re-
sponse to pressure from diurnal predators (Hobson
1978; Allen and DeMartini 1983). Several species
of voracious carnivores including Pacific mack-
erel. Scomber japonicus; Pacific bonito, Sarda
chiliensis (Allen and DeMartini 1983); and
California halibut, Paralichthys californicus, of
piscivore-size (Plummer et al. 1983) are less abun-
dant nearshore in the San Onofre-Oceanside re-
gion. The California halibut is a known predator of
queenfish (Frey 1971; Plummer et al. 1983). The
kelp bass, Paralabrax clathratus, another species
known to prey on queenfish (Young 1963; E. De-
Martini^®), is most abundant in and near beds of
giant kelp, Macrocystis pyrifera, that occur at
10-15 m bottom depths in the region (Larson and
DeMartini 1984).
Overall, our data indicate that the nocturnal
offshore dispersal of adults and the less contagious
distribution of immatures nearshore at night are
primarily for feeding. Allen and DeMartini (1983)
reviewed and discussed the possible advantages of
dispersal for feeding in schooling, zooplank-
tivorous fishes. To these we add the possible
benefit (for adult queenfish) of foraging in regions
where M kadiakensis, a species of large mysid, is
more abundant. It is also likely that the rate at
which individual queenfish encounter planktonic
prey is enhanced by foraging in regions farther
offshore, where longshore currents are, on aver-
age, stronger (Reitzel").
The nighttime, nearshore distribution of small
immature queenfish also may be due to either or
both of the following factors. First, small queen-
fish are undoubtedly incapable of making as ex-
tensive diel migrations as adults because of body
size limitations. Hence the nearshore daytime dis-
tribution of immatures, probably set primarily by
the influence of diurnal predators offshore, might
limit the offshore movements of immatures at
night. Second, predation pressure from nocturnal
predators located farther offshore could restrict
immature queenfish to nearshore regions. Poten-
tial nocturnal predators of immature queenfish
include California halibut (Allen 1982) and
California scorpionfish, Scorpaena guttata (Hob-
son et al. 1981). The nocturnal habits of other po-
tential predators (Pacific mackerel. Pacific bonito,
and Pacific barracuda, Sphyraena argentea) of
small, immature queenfish are unknown. Large
(>70 mm SL, Fig. 3) immature queenfish move
offshore to some extent at night, which is also
consistent with offshore dispersal to feed on larger
prey, since size of prey is strongly related to
queenfish body size (Tables 4, 6). Offshore disper-
sal of large immatures is nonetheless consistent
with relaxed predation pressure, since susceptibil-
ity to predation must be inversely proportional to
body size.
Rigorous evaluation of offshore dispersal for
spawning would require censuses of the onshore,
offshore distribution of recent spawning products.
However, we are at present unable to routinely
distinguish queenfish eggs or yolk-sac larvae
<2.2-2.3 mm long (~4 d old or less) (Watson^'^).
In summary, we conclude that, as might be ex-
pected, the distributional (including migration)
patterns of queenfish have feeding, predator
avoidance, and perhaps other functions such as
breeding.
'Bernstein, B. B., and L. G. Gleye. The ecology of mysids in
the San Onofre region. A study submitted to the Marine Review
Committee of the California Coastal Commission, April 30,
1981. Unpubl. rep., 72 p. Marine Ecological Consultants of
Southern California, 531 Encinitas Boulevard, Encinitas, CA
92024.
'"E. DeMartini, Marine Science Institute, University of
California, Santa Barbara, CA 93106. Unpubl. data.
"J. Reitzel. 1979. Physical /chemical oceanography. In
Interim Report of the Marine Review Committee of the Califor-
nia Coastal Commission. Part II: Appendix of Technical Evi-
dence in Support of the General Summary, March 12, 1979, p.
6-23. Unpubl. rep. Marine Review Committee Research
Center, 531 Encinitas Boulevard, Suite 106, Encinitas, CA
92024.
'^W. Watson, Marine Ecological Consultants of Southern
California, Inc., 531 Encinitas Boulevard, Suite 110, Encinitas,
CA 92024, pers. commun. May 1983.
183
Comparison With
the Diel Migrations of Other Fishes
Numerous other temperate (see Hobson and
Chess 1976; Hobson et al. 1981; Allen and DeMar-
tini 1983) and tropical (reviewed in Helfman et al.
1982) fishes are known to make horizontal migra-
tions at dusk and dawn away from and back to
reefs and other shallow areas. Such migrations
have been characterized as a form of commuting
between daytime resting/sheltering and night-
time feeding areas (Hobson 1965, 1973). These be-
haviors are most widely recognized for tropical
coral reef-based fishes that forage on night-active
benthic invertebrates in surrounding sandflats
and seagrass beds or on nocturnal meroplankton
in the water column (Hobson 1965, 1973; Domm
and Domm 1973; Helfman et al. 1982; and others).
The diel migration of queenfish certainly suggests
feeding as a major, if not principal function. Both
predator avoidance and feeding are probably
major determinants of the nearshore distribution
of immature queenfish. Feeding is probably the
principal reason for the crepuscular onshore, off-
shore migrations of adults. Offshore movement for
spawning may be of secondary importance, but
data are inconclusive.
With the exception of the relatively short-range
(within-reef) migrations observed for some tropi-
cal wrasses (see Moyer and Yogo 1982 and others),
we are unaware of any study of the diel migratory
behavior of nearshore.temperate or tropical fishes
that has demonstrated a primary spawning func-
tion for the behavior We do not now believe that
spawning is a major reason for the nocturnal off-
shore movements of queenfish, although we still
feel that spawning is partly involved. We strongly
recommend that future studies of the diel migra-
tory patterns of temperate and tropical fishes be
watchful for possible spawning as well as feeding
activity.
ACKNOWLEDGMENTS
We thank Art Barnett for graciously allowing us
to cite some of his unpublished data and Jan Fox
for typing the manuscript. An anonymous re-
viewer helped us recognize the relative strengths
and weaknesses of our arguments. This paper is
the result of research funded by the Marine Re-
view Committee (MRC), Encinitas, Calif The
MRC does not necessarily accept the results, find-
ings, or conclusions stated herein.
FISHERY BULLETIN; VOL. 83, NO. 2
LITERATURE CITED
ALLEN, L. G., AND E. E. DEMARTINI.
1983. Temporal and spatial patterns of nearshore distribu-
tion and abundance of the pelagic fishes off San Onofre-
Oceanside, California. Fish. Bull., U.S. 81:569-586.
ALLEN, M. J.
1982. Functional structure of soft-bottom fish communities
of the southern California shelf. Ph.D. Thesis, Univ.
California, San Diego, 577 p.
BARNARD, J. L., AND R. R. GIVEN.
1961. Morphology and ecology of some sublittoral cuma-
cean Crustacea of Southern California. Pac. Nat. 2:153-
165.
BARNETT, A. M.
1974. The feeding ecology of an omnivorous neritic
copepod, Labidocera trispinosa Esterly. Ph.D. Thesis,
Univ. California, San Diego, 233 p.
BEAMISH, E W. H.
1966. Vertical migration by demersal fish in the northwest
Atlantic. J. Fish. Res. Board Can. 23:109-139.
BLAXTER, J. H. S.
1970. Light. In O. Kinne (editor). Marine ecology. Vol. 1,
Environmental factors, Part 1, p. 213-320. Wiley-Inter-
science, Lond.
BLAXTER, J. H. S., AND B. B. PARRISH.
1965. The importance of light in shoaling, avoidance of
nets and vertical migration by herring. J. Cons. 30:40-
57.
BRAWN, V. M.
1960. Seasonal and diurnal vertical distribution of herring
(Clupea harengus L.) in Passamaquoddy Bay, N.B. J.
Fish. Res. Board Can. 17:699-711.
CLAVIJO, E. J.
1983. Pair spawning and formation of a lek-like mating
system in the parrotfish Scarus vetula. Copeia
1983:253-256.
CLUTTER, R. I.
1967. Zonation of nearshore mysids. Ecology 48:200-208.
DEMARTINI, E. E., AND R. K. FOUNTAIN.
1981. Ovarian cycling frequency and batch fecundity in the
queenfish, Seriphus politus: Attributes representative of
serial spawning fishes. Fish. Bull., U.S. 79:547-560.
DOMM, S. B., AND A. J. DOMM.
1973. The sequence of appearance at dawn and disappear-
ance at dusk of some coral reef fishes. Pac. Sci. 27:128-
135.
FEDER, H. M., C. H. TURNER, AND C. LIMBAUGH.
1974. Observations on fishes associated with kelp beds in
southern California. Calif Dep. Fish Game, Fish Bull.
160, 144 p.
FREY, H. W. (editor).
1971. California's living marine resources and their utili-
zation. Calif Dep. Fish Game, Mar. Res. Agency, 148
P-
HELFMAN, G. S.
1978. Patterns of community structure in fishes: summary
and overview. Environ. Biol. Fish. 3:129-148.
HELFMAN, G. S., J. L. MEYER, AND W. N. MCFARLAND.
1982. The ontogeny of twilight migration patterns in
grunts (Pisces:Haemulidae). Anim. Behav 30:317-326.
HICKLING, C. F
1933. The natural history of the hake. Part IV. Age-
determination and the growth rate. Fish. Invest.,
Minist. Fish. Agric. Food (G.B.) Sen 2, 13 (2):1-120.
184
DeMARTlNI ET AL: DISTRIBUTION PATTERNS OF QUEENFISH
HOBSON, E. S.
1965. Diurnal-nocturnal activity of some inshore fishes in
the Gulf of California. Copeia 1965:291-302.
1973. Diel feeding migrations in tropical reef fishes. Hel-
gol. Wiss. Meeresunters. 24:361-370.
1978. Aggregating as a defense against predators in
aquatic and terrestrial environments. In E. S. Reese and
F. J. Lighter (editors), Contrasts in behavior, p. 219-
234. Wiley, N.Y.
HOBSON, E. S., AND J. R. CHESS.
1973. Feeding oriented movements of the atherinid fish
Pranesus pinguis at Majuro Atoll, Marshall Islands.
Fish. Bull., U.S. 71:777-786.
1976. Trophic interactions among fishes and zooplankters
near shore at Santa Catalina Island, California. Fish.
Bull., U.S. 74:567-598.
1978. Trophic relationships among fishes and plankton in
the lagoon at Enewetak Atoll, Marshall Islands. Fish.
Bull., U.S. 76:133-153.
HOBSON, E. S., W. N. MCFARLAND, AND J. R. CHESS.
1981. Crepuscular and nocturnal activities of Californian
nearshore fishes, with consideration of their scotopic vis-
ual pigments and the photic environment. Fish. Bull.,
U.S. 79:1-30.
JUNE, F C.
1972. Variations in size and length composition of Atlantic
menhaden groupings. Fish. Bull., U.S. 70:699-713.
LARSON, R. J., AND E. E. DEMARTINI.
1984. Abundance and vertical distribution of fishes in a
cobble-bottom kelp forest off San Onofre, California.
Fish. Bull., U.S. 82:37-53.
LUCAS, C. E.
1936. On the diurnal variation of size-groups of trawl-
caught herring. J. Cons. 11:53-59.
MILLER, D. J., AND R. N. LEA.
1972. Guide to the coastal marine fishes of California.
Calif Dep. Fish Game, Fish Bull. 157, 235 p.
MOVER, J. T, AND Y. YOGO.
1982. The lek-like mating system of Halichoeres
melanochir (Pisces:Labridae) at Miyake-jima, Japan. Z.
Tierpsychol. 60:209-226.
PARRISH, B. B., J. H. S. BLAXTER, AND W. B. HALL.
1964. Diurnal variations in size and composition of trawl
catches. Rapp. P-v Reun. Cons. Perm. int. Explor. Mer
155:27-34.
PINKAS, L., M. S. OLIPHANT, AND I. L. K. IVERSON.
1971. Food habits of albacore, bluefin tuna, and bonito in
California waters. Calif Dep. Fish Game, Fish Bull. 152,
105 p.
PLUMMER, K. M., E. E. DEMARTINI, AND D. A. ROBERTS.
1983. The feeding habits and distribution of juvenile-small
adult California halibut (Paralichthys callfornicus) in
coastal waters off northern San Diego County. CalCOFI
Rep. 24:194-201.
QUINN, T P, B. S. MILLER, AND R. C. WINGERT.
1980. Depth distribution and seasonal and diel movements
of ratfish, Hydrolagus colliei, in Puget Sound, Washing-
ton. Fish. Bull., U.S. 78:816-821.
SCOFIELD, W. L.
1951. Purse seines and other roundhaul nets in Califor-
nia. Calif Dep. Fish Game, Fish Bull. 81, 83 p.
SlEGEL, S.
1956. Nonparametric statistics for the behavioral
sciences. McGraw-Hill Book Co., 312 p.
WILSON, K. V.
1956. A distribution-free test of analysis of variance
hypotheses. Psychol. Bull. 53:96-101.
WOODHEAD, R M. J.
1964. Diurnal changes in trawl catches of fishes. Rapp.
P-v. Reun. Cons. int. Perm. Explor Mer 155:35-44.
1966. The behavior of fish in relation to light in the
sea. Oceanogr. Mar. Biol. Annu. Rev 4:337-403.
YOUNG, R H.
1963. The kelp bass iParalabrax clathratus ) and its fishery,
1947-1958. Calif Dep. Fish Game, Fish Bull. 122, 67
P-
185
REACTION OF DOLPHINS TO A SURVEY VESSEL:
EFFECTS ON CENSUS DATA
Roger P HEvmT^
ABSTRACT
A field experiment is described in which a helicopter was used to observe the efficiency of shipboard
line-transect sampling of dolphin populations in the eastern tropical Pacific Ocean. Nineteen dolphin
schools were tracked; 13 of these were detected by observers aboard the ship and 5 of these reacted to the
approach of the ship by altering the direction and/or the speed of their movement; however, only 1 school
reacted prior to shipboard detection. The results suggest that dolphin schools only occasionally react to
the approach of a survey vessel prior to their detection by shipboard observers and that the use of a
monotonically decreasing detection function is adequate to minimize bias. Aerial and shipboard
estimates of school size and species composition for six schools compared favorably.
The Marine Mammal Protection Act of 1972 pro-
hibits the harvest of marine mammals and
specifies that the Federal Government may issue
permits for their take only under special cir-
cumstances. One such circumstance involves the
incidental kill of dolphins associated with the yel-
lowfin tuna fishery in the eastern tropical Pacific
Ocean. Before issuing the permits, the govern-
ment must first certify the viability of the affected
dolphin populations. To meet this requirement,
scientists at the Southwest Fisheries Center define
stocks and monitor their population demography,
reproductive output, and abundance.
The vital statistics are derived primarily from
specimens obtained from the tuna fishery. How-
ever, to estimate abundance, surveys are con-
ducted using ships and aircraft independently of
the fishery. The surveys, using line-transect
methods (Burnham et al. 1980), have yielded esti-
mates of the density of dolphins in the eastern
tropical Pacific Ocean (Holt and Powers 1982). A
critical assumption in the application of the
method is that the animals do not move, in reac-
tion to the observer, prior to their detection. In
practice, a detection function, which is relatively
insensitive to nonrandom movement, is used to
describe the probability of observing a school of
dolphins given its position relative to the ob-
server's transect. A field experiment. was designed
with the following objective:
^Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, EO. Box 271, La Jolla, CA
92038.
Msinuscript accepted April 1984.
FISHERY BULLETIN: VOL. 83. NO. 2, 1985.
1) Test the assumption that the animals do not
alter their movement in reaction to the ap-
proach of a survey vessel prior to shipboard
detection.
During a survey the unit of observation is a
school of dolphins. In addition, species composition
and the number of individual animals in a school
(school size) are estimated. Surveys routinely col-
lect information to determine the precision of
these estimates by recording independent obser-
vations of several observers; however, determining
their accuracy is more difficult and attempted less
often (Holt and Powers 1982). Six schools Were
closely approached and observed from both an air-
craft and a ship with the following objective:
2) Compare shipboard and aerial estimates of
school size and species composition.
Although not an absolute determination of accu-
racy, the comparison yielded estimates from two
very different viewpoints (high-altitude plan view
versus low-altitude profile view).
A similar experiment was conducted using the
NOAA Ship Surveyor and a ship-supported
helicopter in 1977 (Au and Perryman 1982). They
observed the reaction of eight dolphin schools to
the approach of a ship; all eight schools swam
away from the projected trackline of the ship. Au
and Perryman also suggested that, in some cases,
avoidance began beyond the visual range of ship-
board observers. The present study was intended
to collect additional data under a wider variety of
conditions.
187
FISHERY BULLETIN: VOL. 83, NO. 2
METHODS
The experiment was designed to observe the
efficiency of shipboard survey operations by using
a helicopter to track dolphin schools before, dur-
ing, and after shipboard detection. This approach
was an enhancement of the design employed by Au
and Ferryman (1982) which focused only on the
behavior of the dolphins. A simulated survey op-
eration was included in the experiment for the
following reasons:
1) It was not reasonable to assume that move-
ment of a dolphin school and the probability
of detecting it are unrelated (i.e., it may be
easier to see a school in full flight than one at
rest). Therefore, associated data on move-
ment and shipboard detection were collected
for each school.
2) It was necessary to separate random move-
ment from directed movement toward or
away from the survey vessel. To do so unam-
biguously, the ship could not be directed to-
ward a school detected by the helicopter, but
rather had to continue searching along a
predetermined transect.
were tracked for about an hour's time until one of
three events occurred: 1) the school passed
abeam of the ship; 2) the school passed beyond the
visual range of shipboard observers; or 3) the aer-
ial observers lost sight of the school and had to
terminate the track prematurely; in all of the
latter cases the presence of the animals was
obscured by deteriorating sea state.
During a track, the helicopter was positioned
over the school at a minimum altitude of 1,200 ft
(370 m); the radar range and bearing to the
helicopter were determined from the approaching
survey vessel about every 4 min (an interval suffi-
cient to record the appropriate navigational data
and still provide continuity in the track). A tran-
sponder, mounted on the aircraft, facilitated accu-
rate radar measurements. In addition, OMEGA
navigation positions were recorded from dual sys-
tems aboard the helicopter and the ship. As the
track progressed, field notes were taken on visual
observations of school behavior and associated
birds and fish. The tracking altitude appeared to
SHIP TRANSECT
t
From the experience gained on the 1982 survey
(Holt 1983), we expected 80% of the sighting cues
to be within 3 nmi of the transect line and <5 nmi
ahead of the vessel. Furthermore, the Au and Fer-
ryman observations on eight schools suggested
that dolphins may react to a ship 6 nmi away. With
these considerations and prior experience in mind,
the following field procedure was employed.
The ship proceeded at 12 kn in a direction
selected so as to minimize glare from the sea sur-
face. Two observers maintained constant watch
through 25 power binoculars, mounted on the port
and starboard sides of the flying bridge (11m above
the water); search patterns extended from the bow
to the beam of the ship on each side. Records were
kept of searching effort and sighting details. With
the exception of selecting the transect direction,
these are the same methods employed during pre-
vious dolphin surveys (e.g.. Holt and Fowers 1982).
The helicopter searched a distance of 8 to 12 nmi
ahead of the ship and 2 nmi to either side of the
transect line, at right angles to the direction of the
ship's travel (Fig. 1). Search altitude was 1,200 ft
and speed was 60 kn. When a school was sighted by
the helicopter, shipboard radar tracking began.
The observers on the flying bridge were not aware
of a track in progress until its termination. Schools
I HELICOPTER PATH
j-2 nm.-J
'8-12
nm.
SHIP
Figure l. — Port and starboard search patterns (shaded areas)
and path of helicopter (sohd Hne) during transect (dashed line)
surveys for dolphins.
188
HEWITT DOLPHINS" REACTION TO A SURVEY VESSEL
be sufficient so as not to elicit a response from the
animals. The dolphins appeared to be swimming
calmly throughout the tracking; similar experi-
ence was reported by Au and Ferryman (1982). It
also placed the helicopter above the shipboard ob-
servers' vertical field of vision and therefore did
not prematurely cue them on a school. Two oil
drums were released and tracked at the beginning
of the cruise to test the procedure: The resolution
of radar measurements was 1-2° in bearing and 0.1
nmi in range; at 1,200 ft (370 m) altitude we were
able to maintain visual contact with aim object;
and the shipboard observers were not aware of the
helicopter until it was within 1 nmi of the ship,
where the noise signaled its presence. Shipboard
observers were questioned periodically through-
out the experiment as to their cognizance of the
helicopter; answers were always in the negative
except when the binoculars were purposefully di-
rected above the searching field. Observers were
aware that looking for the helicopter would com-
promise the experiment and did not do so.
At the finish of a track, the helicopter descended
to a lower altitude for additional photography and
to estimate school size and species composition.
The ship approached a limited number of schools
to enable close-range shipboard estimates of the
same school parameters. After school size and
species composition were determined, normal sur-
vey operation resumed, with the helicopter search-
ing ahead of the vessel and the shipboard observers
actively scanning and recording search effort.
Relative motion radar plots were maintained.
Apparent change in the relative direction of dol-
phin school movement was used as an indication of
avoidance; field notes of aerial observations of be-
havior supplemented this information. The
criteria defining reaction was a change of 30° or
more in the direction of relative motion that was
sustained over 2 or more subsequent fixes (Fig. 2).
The experimental design was opportunistic and
only specifically designed to compare between a
steam-powered survey vessel (NOAA Ship Sur-
veyor) and a diesel-powered survey vessel (NOAA
Ship David Starr Jordan). The experiment was
conducted within a 100 square nmi area to the
north and east of Clipperton Island (lat. 10°N,
long. 110°W) during March and April 1983.^ Ob-
servations were conducted with the Surveyor from
10 March through 17 March; the ship then ported
at Manzanillo, Mexico, to take on fuel and sub-
sequently met the David Starr Jordan, which had
just completed a marine mammal survey^ on 26
March at Clipperton Island. Observations were
conducted in the same area with the David Starr
Jordan until 7 April.
RESULTS
Avoidance
Tracks were started on a total of 26 dolphin
schools, 5 in front of the Surveyor and 21 in front of
^Cruise Report NOAA Ship Surveyor Cruise RP-12-SU-83
dated May 24, 1983, on file at the Southwest Fisheries Center,
National Marine Fisheries Service, NOAA, P.O. Box 271. La
Jolla, CA 92038.
^Cruise Report NOAA Ship David Starr Jordan Cruise DS-
83-01 dated May 6, 1983, on file at the Southwest Fisheries
Center, National Marine Fisheries Service, NOAA, RO. Box 271,
La Jolla, CA 92038.
300
270'
SCHOOL 8
Visual cue (birds) at 1306
Dolphins sighted at 1306
300
090° 270°
SCHOOL 23
Visual cue (birds) at 0926
Dolphins sighted at 0954
-090°
Figure 2. — Relative motion plots of dolphin school #8 and school #23. School #8 appeared to react to the approach of the ship; the
sighting cue was reported after the dolphins' initial reaction. School #23 did not appear to react to the survey vessel.
189
FISHERY BULLETIN: VOL. 83, NO. 2
the David Starr Jordan; a summary of the obser-
vations is listed in Table 1. Seven of the tracks were
terminated prematurely, and of the remaining 19,
6 schools passed undetected by shipboard observ-
ers. These 6 schools did not appear to adjust their
direction of movement in reaction to the survey
vessel.
Of the 13 schools sighted by ship, 1 school altered
its direction of movement in reaction to the ap-
proaching ship, prior to the detection of a sighting
cue by the shipboard observers, and 12 schools did
not appear to react before detection by the ship.
One of the 12 schools was composed of rough
toothed dolphins, Steno bredanensis, which are
not a target of abundance surveys. Thus, from the
results of this experiment, it is expected that 8%
( V12) of the target schools encountered on a survey
will have moved (in reaction to the observer) prior
to detection. This does not imply a corresponding
degree of survey bias. Nonrandom movement,
prior to detection, will alter the distribution of
sighting distances and the detection function fit
to the distribution; the survey will be biased to
the extent that the functional form is sensitive to
the data (see Discussion). Survey bias may also
exist as a result of schools that react to the ship
and are subsequently never seen by shipboard
observers; if these schools would have been ob-
served (the expectation is certain if they are on the
transect line, less certain if they are off the line),
then the bias is proportional to the fraction of
schools that escaped detection. As stated above, no
schools were observed to react to the ship and
avoid detection.
The data suggest that dolphin schools may alter
their direction of movement in reaction to the ap-
proach of a survey vessel. Thirty-eight percent
(V13) of the schools which were tracked by helicop-
TabLE L — Summary of dolphin school tracking data.
Interpolated
Number
Closest
Radial
radar position
Beaufort
of
point of
Reaction
sighting
at time of
School
sea
Indivi-
approach
distance
distance
Relative
Sighting
sighting
Vessel number
state
Species composition
duals
(nml)
(nml)
(nml)
bearing
cue
(range/bearing)
Surveyor 1
1
Sfeno bredanensis
100%
9
1.3
F'
2.5
317"
animals
1.8/335°
2
1
Stenella attenuata
S. longirostns
50%
50%
175
7.0
F'
F2
3
3
S. attenuata
100%
53
2.5
F'
F2
4
5
Unidentified dolphins
100%
100
2.0
F'
2.0
030
splashes
4 0/032°
5
5
Unidentified dolphins
100%
15
F3
Jordan 6
4
Unidentified dolphins
100%
22
F3
7
4
Unidentified dolphins
100%
35
F3
8
4
S. attenuata
S. longirostns
Unidentified dolphins
25%
5%
70%
300
1.5
2.5
1.5
024'
birds
1.6/030°
9
4
Unidentified dolphins
100%
25
F3
10
4
S. attenuata
S. longirostris
20%
80%
150
0.5
1.7
6.0
003°
birds
6.3/002°
11
4
S. attenuata
100%
25
5.0
F'
6.8"
023 =
birds
7.2/019°
12
4
S. attenuata
S. longirostris
1 5%
85%
65
7.0
F'
F2
13
4
S. attenuata
S. longirostris
65%
35%
175
1.3
2.2
6.8
356°
birds
6.2/357°
14
4
S. attenuata
S. longirostris
90%
10%
50
2.5
F'
6.8"
000°
birds
8.1/354°
15
4
Stenella spp
100%
150
F3
16
4
S. attenuata
100%
35
1.2
1.5
6.0
357°
birds
7.0/359°
17
3
Unidentified dolphins
100%
40
F3
18
3
S. coeruleoalba
100%
160
F3
19
3
S. attenuata
100%
45
3.0
F'
F2
20
0
S. attenuata
S. longirostns
15%
85%
260
1.7
F'
6.8"
355°
birds
6.7/353°
21
2
S. attenuata
S. longirostns
91%
9%
230
6.4
F'
F2
22
1
S. attenuata
S. longirostris
50%
50%
180
2.1
2.1
6.8"
340°
birds
6.7/336°
23
1
S. attenuata
S. longirostns
50%
50%
155
1.5
F'
6.8"
004°
birds
8.0/357°
24
1
S. coeruleoalba
100%
29
01
F'
1.8
020°
animals
1.8/018°
25
1
S. attenuata
S. longirostris
40%
60%
410
2.0
F'
4.0
015°
birds
50/010°
26
1
S. attenuata
100%
85
3.0
F'
F2
'School did not appear to react to the approach of the survey vessel.
'School passed undetected by shipboard observers
^Track prematurely tenninated.
"Cue observed on the horizon.
190
HEWITT DOLPHINS' REACTION TO A SURVEY VESSEL
ter and detected by shipboard observers appeared
to react to the ship. Spotted dolphins, Stenella
attenuata, and spinner dolphin, S. longirostris,
reacted at a distance of 0.5 to 2.5 nmi and were
able to maintain a separation of 0.5 to 2.0 nmi from
the ship; one school of striped dolphins, S.
coeruleoalba. was successfully tracked and these
animals stayed on a collision course with the ship
until they were only a few hundred meters away.
In all cases but one (school 8), the schools were
detected by shipboard observers at distances far
greater than the reaction distance.
None of the four dolphin schools successfully
tracked in front of the Surveyor appeared to react
to the approach of the ship. Five out of 15 schools
appeared to react to the approach of the David
Starr Jordan.
Estimates of School Size and
Species Composition
Six schools were approached at close range by
the David Starr Jordan so that shipboard observ-
ers could make estimates of school size and species
composition using the same techniques that were
used on previous abundance surveys. Estimates of
school size and species composition were made in-
dependently by four to six shipboard observers and
averaged, giving each an equal weight. These es-
timates compared favorably with estimates made
by a single aerial observer stationed in the heli-
copter (Table 2 ). Shipboard estimates of school size
ranged from 65 to 134% of the aerial estimates and
averaged 101% (mean difference = 1.167; Pr =
0.713, paired t test of mean difference = 0); ship-
board and aerial observers agreed on the species
composition for all six schools compared, although
there was some variation in the proportion as-
signed to each species.
DISCUSSION
The density estimator used in line-transect ap-
plications, formally derived by Burnham and An-
derson (1976), and used to estimate the density of
dolphin schools by Smith (1981) and Holt and Pow-
ers (1982), is:
D
Nf(0)
2L
where D is the estimated density of dolphin
schools in the survey area based on the number of
schools observed, A^, over transect length L. The
function fix) is a probability density function fit to
the observed perpendicular sighting distances and
estimating its value at zero distance, /"(Oi, is the
critical concern in the application of line-transect
methods (Burnham et al. 1980).
The frequency distribution of observed perpen-
dicular sighting distances reflects both the detec-
tion abilities of the observer and the reactions of
the observed (Burnham et al. 1980). Dolphin
schools are more difficult to see with distance from
the track line and avoidance, prior to detection,
may cause fewer schools to be seen close to the
track line and more schools to be seen further from
the track line. The school that did move away from
the transect line before shipboard detection (#8)
would have been sighted at 0.1 nmi off the transect
line if it had not altered the direction of its move-
ment. Instead it was detected at 1.0 nmi off the
transect line. If the sample size was larger, such
information could be used to dissect the frequency
distribution of perpendicular sighting distances
into that component which is the result of decreas-
ing visibility with distance from the transect line
and that component which is the result of dolphin
schools adjusting their natural spatial disposition
Table 2. — Comparison of shipboard and aerial estimates of dolphin school size and species composition.
Vessel estimate
Helicopter estimate
Number
Estimated number
Number
Estimated
School
of
of individuals
Species
proportions
of
number of
number
observers
(standard error)
(range)
observers
individuals
Species proportions
20
5
248 (24)
S attenuata
S longirostris
0 14(0 05-0.20)
0.86 (0 80-0.95)
1
260
S attenuata 0.15
S longirostns 0 85
22
4
241 (40)
S. attenuata
S. longirostris
0.96(0.90-1.00)
0.04 (0.00-0 10)
1
180
S attenuata 0.50
S longirostris 0.50
23
4
139(20)
S. attenuata
S. longirostris
Unidentified
0 62 (0 50-0.73)
0.35 (0.22-0 50)
0.03(0.00-0.12)
1
155
S attenuata 0.50
S. longirostris 0.50
24
6
36(6)
S. coeruleoalba
1 1.00(1.00-1.00)
1
29
S coeruleoalba 1.00
25
5
393(61)
S. attenuata
S. longirostris
Unidentified
0.55 (0.40-0.70)
0.39 (0.30-0.60)
0.06 (0.00-0.30)
1
410
S. attenuata 0.40
S. longirostris 0.60
26'
5
55(9)
S. attenuata
1.00(1.00-1.00)
1
85
S. attenuata 1 .00
'Not detected by shipboard observers while In survey mode; ship was directed to school by aerial observer.
191
FISHERY BULLETIN: VOL. 83, NO. 2
in response to the ship. There are, however, other
factors (such as glare and sea state) which are
seldom constant long enough to allow for accumu-
lation of a reasonably precise frequency distribu-
tion, such that the effects due to school movement
would not be overwhelmed by the effects due to
sighting conditions.
The results of this experiment suggest that 1)
dolphin schools occasionally react to the approach
of a survey vessel prior to their detection by ship-
board observers and 2) the expected rarity of the
event implies that a considerable amount of addi-
tional data would be required to quantify its effect.
Any directed movement prior to detection biases
the frequency distribution of perpendicular dis-
tances and may bias the function, fix), fit to these
data. In the absence of information regarding
movement, Burnhametal. (1980) suggested choos-
ing a function which is relatively insensitive to
data contaminated by movement, i.e., a function
that monotonically decreases with distance from
the transect line. Their simulations suggest that
in situations where "undetected movement is rela-
tively minor, then use of an estimator based on a
monotonically decreasing function will minimize
bias in D," (Burnham et al. 1980:130). The small
sample size of the present experiment was suffi-
cient to qualify undetected movement as relatively
minor but not sufficient to quantify its effect on
the distribution of perpendicular distances.
Although the work reported here was conducted
in the same geographic area (Clipperton Island,
lat. lO'N, long. 110 W) as the Au and Ferryman
(1982) observations, the two experiments are not
strictly comparable. Au and Ferryman used the
ship and helicopter to search for schools and col-
lected data on their reaction to the ship without
regard to the effect on survey operations; in four of
the eight schools they studied, the ship was turned
toward the school during tracking. They were in-
terested in describing the behavior of dolphin
schools and combining the description with a
search model to quantify survey bias. The present
experiment did not assume that the two processes
(reaction and detection) were independent and
was less ambitious because there was no intention
to generalize dolphin behavior Indeed, the results
presented here may only be relevant to this area
and for these sighting conditions. Both the reac-
tion distance and the sighting distance may be
affected by environmental conditions and may
vary between geographic areas with the degree of
animal naivete.
The comparisons of aerial and shipboard results
suggest that school-size estimates may be more
reliable than those of species composition. Al-
though neither observation platform can be con-
sidered to yield estimates without error, they do
provide unique vantage points with very different
views of the dolphin school. All shipboard observ-
ers, after exposure to observation conditions in the
helicopter, agreed that they could more confi-
dently estimate school size from the air than from
a vessel. The helicopter provides an opportunity to
observe the entire school over an extended period
of time, making it easier to estimate that portion
of the school which is submerged and not com-
pletely visible. Species proportions are more diffi-
cult to estimate and it is not clear which platform
is better; indeed, in the case of school 22, all four
shipboard observers reported similar proportions
which were quite different than that estimated
from the air One explanation may be that it is
more difficult to identify animals in plan view
than in profile view; alternately, the fluid charac-
ter of school structure may combine with the lim-
ited view of the school from a ship to preclude
accurate estimates of species proportions; a third
possibility is that both are inaccurate because of
species-specific behaviors which make the ani-
mals less visible from above and/or the side.
Estimates of the density of dolphin schools are
multiplied by the area of the survey, the average
school size and the species proportions to estimate
species abundances (Holt and Fowers 1982). Be-
cause they affect the abundance estimates di-
rectly, biases in the latter two parameters may be
more serious than the effect of school movement
prior to detection. As an example, consider the six
schools compared during this experiment: the av-
erage number of S. atten uata per school, estimated
by shipboard observers, was 2T^'( greater than that
estimated from the helicopter data, the shipboard
estimate of S. longirostris was 34% less than the
helicopter estimates, and the estimate of S. coeru-
leoalba was the same for both platforms (Table 3).
Although these differences should only be consid-
ered as variability between two estimates, they
illustrate the direct dependence of abundance es-
timates on accurate estimates of species propor-
tions. Avoidance affects density estimates less
dramatically; its affect on /'(O) may be somewhat
offset by using a function that is relatively insen-
sitive to predetection movement.
The application of line-transect methods re-
quires that along the transect line all schools are
seen with certainty. Any departures from the as-
sumption of perfect detection, either because of
192
HEWITT DOLPHINS' REACTION TO A SURVEY VESSEL
Table 3. — Average dolphin school composition.
Vessel Helicopter
Average school size
(number of individuals)
Average species proportions
S. attenuata
185.3
0.545
186.5
0.425
S. longirostris
S coeruleoalba
0.273
0.167
0.408
0.167
Unidentified dolptiin
Average school composition'
S. attenuata
0.015
102.5
79.3
S. longirostris
S. coeruleoalba
51.3
31.5
76.1
31 1
'Unidentified dolphins distributed proportionately among identified
dolphins following Holt and Pow/ers (1982).
generously gave their time and advice during the
design of the experiment; and the conscientious
and competent field observers included G. Fried-
richsen in the helicopter, A. Jackson, W. Irwin, and
M. Noel on the NOAA ship Surveyor, and J. Cotton,
J. Doxey, M. Henry, M. Graybill, R. Pitman, and
G. Yee lead by W. Parks on the NOAA Ship David
Starr Jordan. R. Holt, T. Jackson, W. Perrin, and
P Vergne reviewed the manuscript. The final draft
benefited from the comments of two anonymous
reviewers.
movement or visibility effects, will introduce a
negative bias in the density estimate that is pro-
portional to the decrease in apparent density
along the transect line (Smith 1979). The sample
size was insufficient to test this assumption rigor-
ously; only one school was observed on the transect
line (school 14) and it was detected well beyond any
of the reaction distances observed.
It is recommended that future fieldwork include
additional comparisons of estimates of school size
and species proportions. In addition, the assump-
tion of certain detection along the transect line
should be tested. Biases in school composition and
detection on the transect line affect the abundance
estimates directly and present a greater potential
for inaccuracy than the degree of directed move-
ment prior to detection observed during this
experiment.
ACKNOWLEDGMENTS
This work was accomplished with the help and
collaboration of several people: D. Au, D. Chap-
man, P Hammond, J. Laake, and W. Perryman
LITERATURE CITED
Au, D., AND W. L. PERRYMAN.
1982. Movement and speed of dolphin schools responding
to an approaching ship. Fish. Bull. U.S. 80:371-379.
BURNHAM, K. P., AND D. R. ANDERSON.
1976. Mathematical models for nonparametric inferences
from line transect data. Biometrics 32:325-336.
BURNHAM, K. P., D. R. ANDERSON, AND J. L. LAAKE.
1980. Estimation of density from line transect sampling of
biological populations. J. Wildl. Manage. Monogr. 72,
202 p.
HOLT, R. S.
1983. Report of eastern tropical Pacific research vessel
marine mammal survey, May 15- August 3, 1982. U.S.
Dep. Commer., NOAA Tech. Memo. NMFS-SWFC-29,
151 p.
HOLT, R. S., AND J. E. POWERS.
1982. Abundance estimation of dolphin stocks involved in
the eastern tropical Pacific yellowfin tuna fishery deter-
mined from aerial and ship surveys to 1979. U.S. Dep.
Commer., NOAA Tech. Memo. NMFS-SWFC-23, 95 p.
SMITH, G. E. J.
1979. Some aspects of line transect sampling when the
target population moves. Biometrics 35:323-329.
SMITH, T. D.
1981. Line transect techniques for estimating density of
porpoise schools. J. Wildl. Manage. 45:650-657.
193
FIN EROSION AMONG FISHES COLLECTED NEAR
A SOUTHERN CALIFORNIA MUNICIPAL WASTEWATER OUTFALL
(1971-82)*
Jeffrey N. Cross ^
ABSTRACT
In the Southern Cahfornia Bight, fin erosion is most frequently encountered among fishes collected
near municipal wastewater outfalls. This paper presents an analysis of the trends in the incidence of fin
erosion among fishes collected by otter trawls near Los Angeles from 1971 through 1982.
About 24% of the 122 species offish and 9% of the more than 170,000 individuals collected had the
disease. Flatfish (Pleuronectidae, Bothidae, and Cynoglossidae) and rockfish (Scorpaenidae) accounted
for 66% of the affected species and 99% of the affected individuals. Dover sole (Pleuronectidae:
Microstomus pacificus ) accounted for 89% of the affected individuals.
The incidence of fin erosion was highest close to the outfalls and declined with increasing distance.
The number of species with the disease declined from 1971 to 1982. The incidence of the disease also
declined in two of the three most affected species (Dover sole and rex sole, Glyptocephalus zachirus).
The contemporaneous decline in the number of species and the proportion of individuals with the
disease and the decline in surface sediment contaminant levels suggest that the magnitude of contami-
nation and the incidence of fin erosion are directly related.
The effect of fin erosion on the Dover sole population was examined. Dover sole recruit to the study
area when they are 40-50 mm SL; the incidence of fin erosion was negligible in new recruits but
increased rapidly with increasing fish size. No significant differences were detected in the length-
weight relationships or size-at-age data between Dover sole with and without the disease. Survival
rates of Dover sole with and without fin erosion were similar until age 3; thereafter, the survival rate of
diseased fish was significantly lower.
Fin erosion in the Southern California Bight is
most prevalent in fish collected near major munic-
ipal wastewater outfalls. Of the major outfalls, the
disease is most frequently encountered around the
Joint Water Pollution Control Project (JWPCP)
outfalls on the Palos Verdes shelf (Mearns and
Sherwood 1974, 1977; Sherwood and Mearns 1977).
About 20% of the 151 species offish collected in the
Southern California Bight between 1969 and 1976
were affected by the disease. Flatfish (Pleuronec-
tidae, Bothidae, and Cynoglossidae) and rockfish
(Scorpaenidae) accounted for 60% of the affected
species and 97% of the affected individuals
(Mearns and Sherwood 1977; Sherwood 1978).
Municipal wastewater discharge on the Palos
Verdes shelf began in the late 1930's. The mass
emission of suspended solids increased steadily
from about 17,000 metric tons (t) in the early
1940's to a peak of 167,000 t in 1971 (Wilson et al.
1980). Awareness of the problem of discharging
excessive amounts of solids and associated con-
'Contribution No. 196, Southern California Coastal Water Re-
search Project.
^Southern California Coastal Water Research Project, 646 W.
Pacific Coast Highway, Long Beach, CA 90806.
taminants by JWPCP in the early 1970's resulted
in the installation of new equipment and more
effective treatment procedures to reduce solid
emissions. By 1981, discharge of suspended solids
had declined to 84,000 t. The mass emission of
contaminants also declined from 1971 to 1981
(Schafer 1982). Otter trawling, as part of a regular
monitoring program of the animals on the Palos
Verdes shelf, began in 1971.
The purpose of this paper is to determine trends
in the incidence of fin erosion among fish collected
by otter trawls near the JWPCP outfalls from 1971
through 1982. The prevalence of the disease over
the size range of individuals collected and the ef-
fect of the disease on growth and survival are
examined for the most affected species.
METHODS
The data analyzed in this study were collected
by the Los Angeles County Sanitation District
(LACSD) during regular monitoring cruises on the
Palos Verdes shelf; station and transect identifica-
tions used herein are LACSD designations. Day-
time trawls were made at three depths (23, 61, and
Manuscript accepted April 1984.
FISHERY BULLETIN: VOL. 83, NO. 2, 1985.
195
FISHERY BULLETIN: VOL. 83, NO. 2
137 m) at each of seven transects (Fig. 1) with an
otter trawl towed along a depth isobath at 1.1 m/s
for 10 min. A 7.3 m (headrope length) trawl was
used from 1971 to 1974, when it was replaced by a
7.6 m net; a 1.25 cm mesh cod end liner was used in
both nets. From 1971 through 1978, two
samples — one between April and June and one
between October and December — were collected
annually at each depth; occasionally, additional
trawls were made and these were included in the
analyses. Quarterly trawling began in 1979 and
has continued to the present. Sampling was dis-
continued at transects T2, T3, and T6 in 1977.
Trawl catches were sorted by species and pro-
cessed on board ship. The standard length of each
individual was determined on a measuring board
(BSL = board standard length). External
abnormalities (e.g., fin erosion, parasites, tumors)
were recorded along with length.
Trends in the incidence of fin erosion per 10-min
trawl were determined from linear regressions of
the proportion ip) offish with the disease (trans-
formed to arcsin \ p) versus time [numbered in
consecutive months from 1971 through 1982 (i.e., 1,
2, 3, ..., 143, 144)]. Collections where only one
individual of the species of interest was caught
were dropped from the analysis because the result-
ing transformed datum (either 0 or 90) often had a
large effect on the residual sum of squares. Trends
in the total catch per 10-min trawl were deter-
mined from linear regressions of numbers
[transformed to logio (x -I- D] versus time. The null
hypothesis that the regression function (slope)
was equal to zero was tested with a ^-test. The null
hypothesis of equality of the regression functions
was tested by analysis of covariance (ANCOVA). If
the null hypothesis was not accepted, significant
differences were detected with a Newman-Keuls
multiple range test (Zar 1974). Calico rockfish,
Sebastes dalli, rex sole, Glyptocephalus zachirus,
and Dover sole. Microstomas pacificus, accounted
for 96.6% of the fish with fin erosion (Table 1) so the
trend analysis was performed on each species in-
dividually. Less than 1% of the fin eroded fish came
from the 23 m stations; these stations were then
dropped from the analyses.
The quarterly trawl data (1979-82) from tran-
sects T4 and T5 were examined for seasonal trends
in the total catch of Dover sole, the number with
fin erosion, and the proportion with fin erosion
with the following model:
Y,=fiT^,S,) + e^
where Y = observed abundance (or proportion) in
period t,T^ = trend factor of time series in period
t, S^ = seasonal factor of time series in period t,
f = function relating observed abundance (or pro-
portion) to the trend and seasonal components,
and e^ = irregular factor of time series in period t
(Bowerman and O'Connell 1979). Multiplicative
and additive models were fitted to the quarterly
trawl data after transformation [logio (x -I- 1) and
arcsin \ p ]. Multiplicative models gave the best fit
(lowest residual sum of squares) so only those re-
sults are presented. After determining the quar-
terly trends, the original transformed data were
"deseasonalize'd" by dividing each value by the
corresponding seasonal factor. Trends in the de-
X
.'b'^
<^
%
^o.
Figure l. — Location of sampling transects on the Palos Verdes shelf. Three depths (23, 61,
and 137 m) were sampled at each transect. Joint Water Pollution Control Project outfalls are
located between transects T4 and T5. Net current flow is northwest.
196
CROSS: FIN EROSION AMONG FISHES
Table l. — Taxonomic list of fish affected with fin erosion collected in 622 otter trawls on the Palos Verdes shelf
from 1971 through 1982.
Frequency of
occurrence (%)
Percent of
Number
in trawl
Percent with
all fish with
Common name
Scientific name
collected
collections
fin erosion
fin erosion
spotted cusk-eel
Chilara laylori
191
16.7
0.5
<0.1
blackbelly eelpout
Lycodopsis pacifica
2.629
20.6
<0.1
<0.1
shortspine thornyhead
Sebastolobus alascanus
312
4.3
1.9
<0.1
calico rockflsh
Sebastes dallii
9.153
23.6
9.9
5.8
shortbelly rockfish
Sebastes jordani
3,247
25.1
0.2
<0.1
stripetail rockfish
Sebastes saxicola
18,938
54.5
<0.1
<0.1
Vermillion rockfish
Sebastes miniatus
382
17.1
0.5
<0.1
pink rockfish
Sebastes eos
37
1.1
5.4
<0.1
greenstriped rockfish
Sebastes elongatus
263
13.8
2.3
<0.1
splitnose rockfish
Sebastes diploproa
6,973
24.0
<0.1
<0.1
sablefish
Anoplopoma fimbria
711
15.6
0.3
<0.1
shortspine combfish
Zaniolepis frenata
794
20.6
0.1
<0.1
longspine combfish
Zaniolepis latipinnis
891
20.7
0.4
<0.1
barred sand bass
Paralabrax nebulifer
40
4.0
2.5
-0.1
white croaker
Genyonemus lineatus
9,062
20.9
1.6
0.9
white seaperch
Phanerodon furcalus
848
12.1
0.2
<0.1
shiner perch
Cymatogaster aggregate
9,478
27.1
<0.1
<0.1
Pacific pompano
Peprilus simillimus
30
2.0
20.0
•'0.1
California tonguefish
Symphurus atricauda
1,091
25.4
1.7
0.1
Pacific sanddab
Citharichttiys sordidus
11,698
61.3
0.5
0.4
speckled sanddab
Citharichthys stigmaeus
15,491
39.6
<0.1
• 0.1
bigmouth sole
Hippoglossina stomala
148
14.6
2.1
<0.1
C-0 sole
Pleuronichthys coenosus
187
10.8
1.1
<0.1
curlfin sole
Pleuronichthys decurrens
3,774
40.4
2.4
0.6
hornyhead turbot
Pleuronichthys verticalis
458
25.0
1.1
0.1
English sole
Parophrys vetulus
1,256
44.7
0.9
<0.1
rex sole
Glyptocephalus zachirus
4,452
28.0
6.7
1.9
slender sole
Lyopsetta exilis
4,674
26.0
3.3
1.0
Dover sole
Microstomus pacificus
41.627
62.2
33.5
88.9
seasonalized data were determined by linear re-
gression.
The effects of fin erosion on the population of
Dover sole on the Palos Verdes shelf were
examined using the original data of Mearns and
Harris (1975)^ that consisted of length, weight,
sex, and age (from otoliths) of 328 Dover sole col-
lected in 1972 and 1973.
Size-frequency distributions between Dover sole
of the same age with and without fin erosion were
compared with a Kolmogorov-Smirnov two sample
test (Siegel 1957). A one-tailed test was used be-
cause the disease might be expected to reduce the
growth rate of affected individuals.
Weight-length relationships among male and
female Dover sole with and without fin erosion
were compared with the geometric mean regres-
sion
log w = log a + b (log /)
where w = weight, I = length, and a and b are
fitted constants (Ricker 1973). The regression co-
Mearns, A. J., and L. Harris. 1975. Age, length, and
weight relationships in southern California populations of Dover
sole. Tech. Memo. 219, 17 p. Southern California Coastal
Water Research Project, Long Beach.
efficients were compared statistically using the
method of Clarke (1980).
The survival rate of Dover sole with and without
fin erosion was compared. Using an age-length key
developed from the data, ages were assigned to all
Dover sole captured in LACSD monitoring trawls
on the Palos Verdes shelf from 1972 through 1975.
Survival rate (S) was calculated from age t (in
years) to age ^ -I- 1 from
S =
N
t + i
N.
where A^ = the number caught (Ricker 1975). Sur-
vival rates of fish with and without the disease
were compared with a ^-test after the data were
transformed to the reciprocal (l/x) to stabilize the
variance. A one-tailed test was used because the
disease might be expected to reduce the survival
rate of affected individuals.
RESULTS
From 1971 through 1982, LACSD made 622
monitoring trawls on the Palos Verdes shelf. Fin
erosion was reported for 15,680 individuals (9.2%
of all individuals collected) representing 29
species (23.8% of all species collected) (Table 1).
197
FISHERY BULLETIN: VOL. 83, NO. 2
Flatfish (Pleuronectidae, Bothidae, and Cynoglos-
sidae) and rockfish (Scorpaenidae) accounted for
65.5% of the affected species and 99.2% of the
affected individuals; Dover sole (Pleuronectidae)
accounted for 88.9% of the affected individuals.
The number of species affected by fin erosion
declined from a high of 18 in 1971 to a low of 3 in
1981 (Fig. 2); the decrease w^as highly significant
(r = -0.766, n = 12, 0.002 <P < 0.005). There
was no significant change in the number of species
collected over the same period (Fig. 2) (r = -0.291,
n = 12, 0.20 <P < 0.50).
80-1
TOTAL
" YEAR ^«
82
Figure 2. — Annual total number offish species collected and
number with fin erosion collected by otter trawl on the Palos
Verdes shelf from 1971 to 1982.
but the increase was not significant at TO (Table
2). ANCOVA detected a significant difference
among the regression coefficients of the 61 m sta-
tions (F = 5.02, 0.003 <P < 0.005) (Table 3).
The total number of calico rockfish collected in a
10-min trawl at 61 m decreased significantly at T4,
but did not change at TO, Tl, and T5 (Table 2). The
regression coefficients for these collections were
not significantly different (F = 1.02, P > 0.25).
REX SOLE
Seven percent of the rex sole, Glyptocephalus
zachirus, had fin erosion; as a species, they ac-
counted for 2% of all fish with the disease (Table 1).
More than 99% of the rex sole collected were
caught at 137 m. Less than 1% of the fish collected
at station TO-137 m had fin erosion. The incidence
of fin erosion among rex sole at the remaining
137 m stations declined significantly (Table 4).
ANCOVA did not detect a significant difference
among the regression coefficients for these collec-
tions (F = L05,P > 0.25).
The number of rex sole caught in a 10-min trawl
at the 137 m stations did not change over the study
period (Table 4), and the regression coefficients for
these collections were not significantly different
(F = 1.43, 0.10 <P< 0.25).
CALICO ROCKFISH
DOVER SOLE
Calico rockfish, Sebastes dallii, were rarely col-
lected before 1975. Beginning in 1975, they were
collected at all stations; the majority (72.4% ) were
collected at 61 m. Ten percent of the individuals
collected had fin erosion; as a species, they ac-
counted for 6% of all fish with the disease (Table 1).
The incidence of fin erosion among calico rockfish
increased at all 61 m stations from 1975 to 1982,
Dover sole. Microstomas pacificus, was by far
the most affected species. Thirty-four percent of
Dover sole collected had fin erosion; as a species,
they accounted for 89% of all fish with the disease
(Table 1). The incidence of fin erosion among Dover
sole declined significantly at all stations except
TO-137 m (Table 5). ANCOVA detected a signifi-
cant difference among the regression coefficients
Table 2. — Linear regressions of A) the proportion (p) of calico rockfish,
Sebastes dallii, in one 10-min trawl with fin erosion (transformed to arcsin
\ p) and B) the total number of calico rockfish caught in one 10-min trawl
[transformed to logio ^x + 1)\ against time (numbered in consecutive
months from 1971 through 1982). n = sample size; LI = lower limit of 95%
confidence interval of the regression coefficient ib); L2 = upper limit;
P = probability that b came from a sampling population with fi = 0.
Station
Y =a +bX
n
LI
L2
P
A) TO-61 m
Y =•
-0.384 + 0.010X
23
-0.020
0.040
0.20
P ■ 0.50
T1-61 m
Y =
-7.325 + 0.125X
26
0.021
0.229
P
= 0.02
T4-61 m
y =
-41.950 + 0.678X
19
0 178
1.178
0.01 '
P 0.02
T5-61 m
Y =
-20.150 + 0.410X
21
0.070
0.751
0.02 ■
; P • 0.05
B) TO-61 m
Y =
1.808 -0.0027X
25
-0.0150
0.0096
P
>0.50
T1-61 m
Y =
1.681 - 0.001 5X
27
-0.0115
0.0085
P
> 0.50
T4-61 m
Y =
1 888 - 0.0098X
26
-0.0194
-0.0002
0.02-
. P ■ 0.05
15-61 m
Y =
0.756 -^ 0.0021 X
26
-0.0076
0.0118
P
>0.50
198
CROSS: FIN EROSION AMONG FISHES
of these collections (F = 17.84, P < 0.0001)
(Table 6).
The total number of Dover sole collected in a
Table 3. — Results of Newman-Keuls multi-
ple range test for equality of regression coeffi-
cients (6) for the incidence of fin erosion
among calico rockfish. s = station; un-
derscored stations are not significantly dif-
ferent.
b:
s:
0.678
T4-61 m
0410
T5-61 m
0.125
T1-61 m
0010
TO-61 m
10-min trawl declined significantly at three of the
eight stations (Table 5). ANCOVA detected a sig-
nificant difference among the regression coeffi-
cients of these collections (F = 3.43,
0.001 < P < 0.003) (Table 6).
Size-Frequency Distributions
The size distributions of Dover sole with and
without fin erosion were examined (Fig. 3). Most
Dover sole recruit to the study area when they are
40-50 mm BSL (broad standard length). Fin ero-
TABLE 4. — Linear regressions of A) the proportion (p) of rex sole, Glyp-
tocephalus zachirus, in one 10-min trawl with fin erosion (transformed to arcsin
\ p) and B) the total number of rex sole caught in one 10-min trawl
[transformed to logio (J: -i- D] against time (numbered in consecutive months
from 1971 through 1982). See Table 2 for explanation of column headers.
Station
Y =a +bX
LI
L2
A) TO- 137 m
T1-137 m y = 10.217 - 0.085X
T4-137 m y = 18.259 - 0.151X
T5-137 m y = 10.733 - 0.087X
B) TO-137 m y = 1.828 - 0.0038X
T1-137m y = 1.326 - 0.0012X
T4-137 m y = 0.976 + 0.0023X
T5-137 m y = 1.182 - 0.0013X
[only 7 of 1,520 fish (0.5%) had fin erosion]
33
-0.132
-0.038
0.002 < P < 0.005
35
-0.239
-0.064
0.001 <P < 0.002
29
-0.151
-0.023
P = 0.01
33
-0.0081
0.0005
0.05 <P <0.10
33
-0.0053
0.0029
P >0.50
36
-0.0020
0.0066
0.20 < P < 0.50
32
-0.0064
0.0038
P > 0.50
Table 5. — Linear regressions of A) the proportion (p) the Dover sole, Micros-
tomas pacificus, in one 10-min trawl with fin erosion (transformed to arcsin \ p)
and B) the total number of Dover sole caught in one 10-min trawl [transformed
to logio (x -I- 1)] against time (numbered in consecutive months from 1971
through 1982). See Table 2 for explanation of column headers.
Station
y =a
+ bX
n
LI
L2
P
A) TO-61 m
y
= 0.861 -
0.0076X
29
-0.0148
-0.0004
0.02 < P < 0.05
TO-137 m
y
= 0.907 -
0.0047X
33
-0.0120
0.0026
P = 0.20
T1-61 m
y
= 29.526
- 0.240X
24
-0.308
-0.172
P <•: 0.001
T1-137m
y
= 28.048
- 0.201X
33
-0.274
-0.128
P <.. 0.001
T4-61 m
y
= 54.520
- 0.332X
29
-0.511
-0.154
P • 0.001
T4-137m
y
= 48.157
- 0.224X
36
-0.336
-0.112
P < 0.001
T5-61 m
y
= 54.732
- 0.374X
31
-0.482
-0.266
P < • 0.001
T5-137m
y
= 38.618
-0.214X
30
-0.300
-0.128
P < < 0.001
B) TO-61 m
y
= 1.601 -
0.0075X
37
-0.0128
-0.0022
0.005 < P < 0.01
TO-137 m
y
= 1.981 -
0.001 7X
34
-0.0066
0.0032
P > 0.50
T1-61 m
Y
= 1 .603 -
0.0077X
34
-0.0136
-00018
0.01 <P <0.02
Tl-137m
Y
= 2.432 -
0.0072X
34
-0.0115
-0.0029
0.001 < P < 0.002
T4-61 m
Y
= 0.688 +
0.0043X
40
-0.0010
0.0096
0.10 <P <0.20
T4-137m
Y
= 2.118 -
0.0007X
36
-0.0044
0.0030
P > 0.50
T5-61 m
y
= 1.354 -
0.001 8X
39
-0.0067
00031
0.20 < P < 0.50
T5-137m
y
= 2.592 -
0.0037X
31
-0.0082
0.0008
P =0.10
Table 6. — Results of Newman-Keuls multiple range test for equality of regression
coefficients (6) for A) the proportion of Dover sole. Microstomas pacificus, with fin
erosion and B) the total catch of Dover sole, s = station; underscored stations are not
significantly different.
A)
b:
s:
b:
s:
-0.374
T5-61 m
-0.332
T4-61 m
-0.240
T1-61 m
-0.224
T4-137m
-0.214
T5-137m
-0.201
T1-137m
-0.008
TO-61 m
-0.005
TO-137 m
B)
-0.0043
T4-61 m
-0.0007
T4-137m
-0.0017
TO-137 m
-0.0018
T5-61 m
-0.0037
T5-137m
-0.0072
T1-137m
-0.0075
TO-61 m
-0.0077
T1-61 m
199
FISHERY BULLETIN: VOL. 83, NO. 2
20 60 100 140 180 220 260 300
BSL (MM)
FIGURE 3. — Size distributions of Dover sole, Microstomas
pacificus, with fin erosion (dashed line) and without fin erosion
(solid line) by 20 mm size class (i.e., 20-39 mm, 40-59 mm, ...,
300-319 mm) for all collections (1971-82) combined. The number
of individuals is presented to the right. BSL = board standard
length.
sion was observed in 0.3% of the fish between 40
and 59 mm BSL, 3.8% of the fish between 60 and 79
mm BSL, and 17.7% of the fish between 80 and 99
mm BSL. The incidence of fin erosion peaked in
fish 120-139 mm BSL at stations close to the out-
falls, and in fish 140-179 mm BSL at more distant
stations. The proportion of fish with fin erosion in
a particular size class was greatest at stations
close to the outfalls and declined progressively
with increasing distance (Fig. 4).
Seasonal Trends
Time series analyses of the quarterly trawl data
(1979-82) for Dover sole at T4 and T5 showed con-
sistent seasonal peaks in the total catch and in the
number of individuals with fin erosion, but not in
the proportion of individuals with the disease (Fig.
20 60 100 140 180 220 260 300
BSL (mm)
FIGURE 4. — Percent of Dover sole, Microstomus pacificus, with
fin erosion in each 20 mm size class (i.e., 20-39 mm, 40-59 mm,
. . . , 280-299 mm) at 61 m and 137 m on the sampling transects.
Data for each station are 12-yr totals. BSL = board standard
length.
5). The seasonal indices of total catch and number
with fin erosion were highest in the second
(April-June) and third (July-September) quarters
at 61 m and in the third and fourth quarters at 137
m. The magnitude of the seasonal swing was
greater at 61 m.
Examination of the deseasonalized data re-
vealed that there was no change in the total catch
of Dover sole, the number of individuals with fin
erosion, or the proportion of individuals with fin
erosion at 61 m between 1979 and 1982 (Table 7).
At 137 m, there was a significant decline in the
number of Dover sole with fin erosion at T4 and T5,
and a significant decline in the total catch and
proportion of individuals with fin erosion at T4
(Table 7).
Size at Age
The Mearns and Harris (footnote 3) data were
examined for differences in the size-frequency dis-
tributions between Dover sole with and without
fin erosion at a particular age. There were no signi-
ficant differences for fish age 2 (x^ = 0, df = 2,
P > 0.90), age 3 (x^ = 1.27, df = 2, 0.50 <P <
0.70), age 4 (x^ = 1-71, df = 2, 0.30 < P < 0.50),
or age 5 (x^ = 2.12, df = 2, 0.30 <P < 0.50).
200
CROSS: FIN EROSION AMONG FISHES
NO. WITH FIN EROSION
160
TOTAL CATCH
PROP WITH FIN EROSION
Figure 5. — Quarterly seasonal trends in the total catch of Dover sole, Microstomas pacificus, the number of individuals with fin
erosion, and the proportion of individuals with fin erosion collected at 61 m and 137 m at T4 and T5 from 1979 through 1982. Quarter 1
= Jan.-Mar, 2 = Apr. -June, 3 = July-Sept., 4 = Oct.-Dec.
Table 7. — Linear regressions of the deseasonalized A) total catch of Dover
sole. Microstomas pacificus, in one 10-min trawl [transformed to logio ix + 1) ],
B) number of Dover sole with fin erosion [transformed to logio ix + D], and C)
proportion (p) of Dover sole with fin erosion (transformed to arcsin \p) re-
gressed against time (numbered in consecutive quarters from 1979 through
1982). See Table 2 for explanation of column headers.
Station
a +bt
LI
L2
A)
T4-61 m
y
= 1.176 + 0.014t
16
-0.057
0.085
P >0.50
T4-137 m
y
= 2.467 - 0.036f
16
-0.069
-0.003
0.02 <P < 0.05
T5-61 m
A
= 1.303 -0.007f
16
-0.082
0.068
P > 0.50
T5-137 m
y'
= 2.509 -0.04U
16
-0.115
0.033
0.05 < P < 0.10
B)
T4-61 m
y
= 0.370 + 0.043f
16
-0.028
0.114
0.20 <P < 0.50
T4-137 m
y
= 2.303 - 0.075f
16
-0.121
-0.029
0.002 < P < 0.005
T5-61 m
y
= 0.708 + 0.002f
16
-0.056
0.060
P >0.50
T5-137 m
y
= 2.082 - 0.067f
16
-0.121
-0.013
0.01 < P < 0.02
C)
T4-61 m
y
= 22.09 + 0.350f
16
-1.616
2.316
P > 0.50
T4-137 m
y
= 48.45 -1.470f
16
-2.819
-0.121
0.02 < P < 0.05
T5-61 m
y
= 29.32 - 0.267f
16
-2.055
1.521
P > 0.50
T5-137 m
y
= 40.87 - 0.982f
16
-2.635
0.671
0.20 < P < 0.50
Weight-Length Relationships
The Mearns and Harris data were examined for
differences in the weight-length relationships
among males and females with and without fin
erosion. There were no significant differences in
the regression coefficients between males with
and without the disease (T12 = 1.587, df = 38,
0.10 <P < 0.20) and between females with and
without the disease (Tja = 0.508, df = 56,
P > 0.50) (Table 8). There was a significant differ-
ence between males and females without the dis-
ease (T12 = 3.189, df= 64, 0.002 <P < 0.005), but
not between males and females with the disease
(T12 = 0.713, df = 37, 0.20 <P < 0.50).
Table 8. ^Results of the geometric mean regression of log
w = logo + b (log/), where u) = weight and / = length, for male
and female Dover sole with and without fin erosion. LI = lower
limit of 95'7f confidence interval of the regression coefficient (fe);
L2 = upper limit.
Fin erosion
log w = loga + b (log/)
LI
L2
Males without log w = -4.514 + 2.864 (log /) 2.663 3.065
Maleswith log iv = -4.994 + 3.114 (log/) 2.852 3.376
Females without log iv = -5.564 + 3.310 (log/) 3.116 3.504
Females with log iv = -5.379 + 3.234 (log/) 3.002 3.466
201
FISHERY BULLETIN: VOL. 83, NO. 2
Survival Rates
The survival rates of Dover sole with and with-
out fin erosion from Paios Verdes were not signifi-
cantly different from age 1 to age 2 {t ^ 1.267, df
= 4, 0.10 < P < 0.25) and from age 2 to age 3
{t - 0.741, df = 4,P = 0.25) (Fig. 6). The survival
rates were significantly lower for individuals with
fin erosion from age 3 to age 4 (^ = 2.826, df = 4,
0.01 <P < 0.025) and from age 4 to age 5
(t = 2.890, df= 4,0.01 <P < 0.025). No individu-
als with fin erosion older than age 5 were collected
(Fig. 6).
FIGURE 6. — Survival rate of Dover sole, Microstomas
pacificus, with fin erosion (solid line) and without fin erosion
(dashed line) from year t to year t + 1. Data presented as mean
and 1 SE (vertical line).
200
OUTFALLS
Figure 7. — Contour maps of total DDT (ppm dry weight) and
copper (ppm dry weight) concentrations in surface sediments
on the Palos Verdes shelf in 1975. Maps redrawn from Her-
shelmanet al. (1977).
DISCUSSION
Current and Sediment Characteristics
on the Palos Verdes Shelf
Near the outfalls, the net current movement 20
m from the bottom in 61 m of water is 5.5 cm/s
upcoast (northwest). Both net flow and major
current fluctuations are oriented in the upcoast
direction (Hendricks 1980). Sewage particles sus-
pended in freshwater are discharged from the out-
falls, rise in the water column, and are carried
generally upcoast as they settle back to the bot-
tom. Trace metal and chlorinated hydrocarbon
contaminants measured in surface sediments re-
veal the characteristic "footprint" of the settled
particles (Fig. 7) (Young and Heesen 1978; Young
et al. 1978). The concentrations of DDT (Table 9),
trace metals (Table 10), and organic material (Ta-
ble 11 ) in surface sediments are highest around the
outfalls and decline upcoast, and generally have
declined during the study period.
Table 9. — Total DDT concentration (ppm dry weight) of surface
sediments at the sampling transects from 1972 to 1981. Note that
the deeper samples were taken at 152 m while the trawls were
made at 137 m. Depth of sediments analyzed at bottom of the
table. (SCCWRP and LACSD, unpubl. data.)
Year
Station
1972
1973
1975
1977
1979
1980
1981
1982
TO- 30 m
0.9
0.3
TO-61 m
2.6
3.5
1.3
1.9
T0-152nn
2.6
3.7
1.6
T1-61 m
160
62
11
13
4
T1-152m
55
17
T4-30 m
31
1.1
T4-61 m
440
70
175
12
14
9
7.4
T4-152 m
220
133
72
T5-61 m
130
95
29
20
12
12
T5-152 m
80
95
124
Depth (cm)
0-2
0-5
0-5
0-2
0-2
0-2
0-2
0-2
Spatial Disease Patterns
Of the three depths sampled (23, 61, and 137 m),
<1% of the fish with fin erosion were collected at
23 m. This is probably a function of low sediment
contamination at the shallowest stations (Table 9).
Coastal sediments in southern California are
202
CROSS: FIN EROSION AMONG FISHES
Table lO. — Copper, cadmium, and chromium concentrations (ppm
dry weight) in surface sediments at the sampUng transects from 1975
to 1980. Note that the deeper samples were taken at 152 m while the
trawls were made at 137 m. Depth of sediments analyzed at bottom of
table. (SCCWRP, unpubl. data.)
Copper
Cadmium
Chromium
Station
1975
1978
1980
1975
1978
1980
1975
1978
1980
TO-61 m
48
42
1.7
1.3
137
119
TO- 152 m
66
66
3.3
2.6
170
174
T1-61 m
362
21
828
T1-152m
148
11
317
T4-61 m
937
427
352
61
28
31
1,480
1,042
972
T4-152m
555
408
66
24
968
862
T5-61 m
134
234
8.3
9.2
254
521
T5-152m
433
301
41
16
769
605
Depth (cm)
0-5
0-2
0-2
Table ll. — Mean organic content (percent)
of surface sediments at 61 m from 1972 to
1981 and correlation between organic content
and years, x = mean, SD = one standard
deviation, n = sample size, r = correlation
coefficient, P = probability that the calcu-
lated r came from a population with p = 0.
Transect
X
SD
n
r
P
TO
2.13
0.18
13
0.052
0.50
T1
6.83
1.45
17
-0.761
0.001
T4
11.21
1.39
17
-0.831
0.001
T5
7.83
1.62
17
-0.532
0.05
coarser and lower in volatile solids in shallow
water, and become finer and higher in volatile
solids with increasing depth. Contaminants are
generally attached to the finer particles and thus
increase in concentration with increasing depth
(Hershelman et al. 1982).
The incidence of fin erosion in Dover sole fol-
lowed the spatial pattern of sediment contaminant
distribution. The incidence was highest near the
outfalls (44.0% of all Dover sole collected at T4 and
37.3% at T5) and decreased with increasing dis-
tance upcoast (20.3% at Tl and 2.0% at TO). The
relationship between disease incidence and sedi-
ment contaminant levels suggests that fin erosion
is the result of contamination and that the inci-
dence of the disease is directly related to the mag-
nitude of contamination. Because preimpact data
do not exist, gradients of contamination and dis-
ease are assumed not to have existed before sew-
age discharge began. It is generally accepted that
the presence of fin erosion in the environment is
the result of contamination (Murchelano and Zis-
kowski 1976; Sindermann 1979). Controlled
laboratory experiments demonstrated that Dover
sole exposed to sediments from the Palos Verdes
shelf developed fin erosion (Sherwood 1976;
Mearns and Sherwood 1977).
Temporal Disease Patterns
The number of species affected by fin erosion
declined significantly from 1971 to 1982 and was
most rapid from 1971 to 1974 following the waste-
water treatment modifications made in the early
1970's. This pattern suggests that the decline was
related to reduced surface sediment contamina-
tion.
The incidence of fin erosion also declined in two
of the three most affected species (Dover and rex
soles). The declines were greater at Tl than at T4
or T5; the incidence of the disease at TO, the sta-
tion farthest from the outfalls, was always low.
There was a significant correlation between the
sediment concentration of DDT (Table 9) and the
proportion of Dover sole with fin erosion (deter-
mined by dividing the total number of Dover sole
with the disease by the total number of Dover sole
collected within a year) at T4-61 m (Spearman
r = 0.821, n = 1, 0.02 <P < 0.05).
s
The seasonal trends in the catch of Dover sole
and the number of Dover sole with fin erosion are
the result of recruitment and depth-related mi-
grations. Recruitment occurs at 61 and 137 m, but
more fish settle out at 137 m. The magnitude of the
seasonal swing appears greater at 61 m where few
Dover sole were captured in the first and fourth
quarters. Large numbers of Dover sole were col-
lected at 137 m in the fourth quarter but, by the
first quarter, the catches had declined substan-
tially. Dover sole apparently move off the shelf into
deeper water in the winter and back onto the shelf
in the summer. Hagerfnan (1952) reported an an-
nual depth-related migration of Dover sole into
deeper water in the winter related to reproduction
and a return migration into shallower water in the
summer related to feeding.
Examination of the deseasonalized data re-
vealed that fin erosion declined over the last 4 yr
203
FISHERY BULLETIN: VOL. 83, NO. 2
at the deeper (137 m) stations near the outfalls but
not at the depth of the outfalls (61 m). The total
catch of Dover sole also declined at 137 m but not at
61 m. The declines in Dover sole abundance in the
long-term (1971-82) and deseasonalized quarterly
(1979-82) data coincide with declines in surface
sediment contamination and therefore are some-
what surprising.
In southern California, Dover sole are an order
of magnitude more abundant around the outfalls
than in distant control areas. This probably is a
function of the distribution of their preferred prey
(polychaetes) which are more abundant around
the outfalls (Cross et al. in press). Pearcy and
Hancock (1978) found a positive correlation be-
tween the standing crop of Dover sole and the
standing crop of their preferred prey off Oregon. A
decrease in the quantity of sewage particles set-
tling at stations distant from the outfalls might
cause a reduction in the preferred prey popula-
tions accounting for the reduced abundance of
Dover sole. The decrease in organic content of sur-
face sediments at Tl, and the low value at TO,
which was within the ^5% confidence interval
(2.12-2.84% ) for reference areas in northern Santa
Monica Bay (Cross, unpubl. data), support this
hypothesis.
The trends in fin erosion among calico rockfish
were different from those of the two soles. The
general increase in disease incidence may result
from differential susceptibility.
Effect of Fin Erosion on
the Dover Sole Population
Although fin erosion has been reported in fishes
from a number of areas around the world [south-
ern California, Puget Sound, and the New York
Bight (Sherwood 1982); Japan (Nakai et al. 1973);
and northern Europe (Perkins et al. 1972)], no one
has yet shown that the disease is harmful to the
affected individuals (Murchelano and Ziskowski
1982).
Dover sole recruit to the study area between
February and May when they are 40-50 mm SL
(Allen and Mearns 1976; Sherwood 1980; Cross
unpubl. data). Fin erosion is negligible in new
recruits. By the time the fish are 80-100 mm BSL
[about 100 d after settlement, based on growth
curves presented in Sherwood (1980)], 18% have
the disease. The size distributions of Dover sole
with fin erosion are narrower than the size dis-
tributions offish without the disease (Fig. 3). Un-
derrepresentation in the lower tail of the size dis-
tribution of Dover sole with the disease occurs
because the fish do not contract fin erosion until
sometime after settlement. Underrepresentation
in the upper tail suggests increased mortality
among fish with the disease.
A size difference between Dover sole with and
without fin erosion was not detected in the data.
The x^ values increased with successive ages
suggesting a significant difference in the size-
frequency distributions may occur at an older age.
Dover sole older than 7 yr were rarely encountered
on the Palos Verdes shelf.
No significant differences were found in the
weight-length relationships between males with
and without the disease and between females with
and without the disease. The significant difference
observed between males and females without the
disease is characteristic of Dover sole (Hagerman
1952). The lack of significant difference between
males and females with fin erosion is difficult to
interpret at this time.
Fin erosion appears to have a detrimental effect
on the survival rate of Dover sole. Survival rates
for Dover sole with and without the disease were
similar up to 3 yr of age; thereafter, the survival
rate of diseased fish was significantly lower.
CONCLUSIONS
The data presented in this study suggest that
1) fin erosion is the result of exposure to contam-
inants discharged from the outfalls and 2) the
magnitude of disease incidence is directly related
to the magnitude of sediment contamination. Dis-
ease incidence and sediment contaminant con-
centrations decrease with increasing distance
from the outfalls. Disease incidence is negligible
in Dover sole recruits but increases rapidly with
increasing body size, and presumably contam-
inant exposure, after settlement. The number of
species affected by the disease, the disease inci-
dence in Dover sole, and the contaminant concen-
trations of surface sediments have declined over
time.
While the prevalence of fin erosion has declined,
the disease remains a problem. Fin erosion was
observed in 5.99c of the fishes collected at 61 m and
137 m at T4 and T5 in 1982 and appears to affect at
least one population causing increased mor-
talities.
Sindermann (1979) described fin erosion as
"Probably the best known but least understood
disease of fish from polluted waters... "(p. 719) and
concluded ". . .that generalized disease signs, such
204
CROSS: FIN EROSION AMONG FISHES
as fin rot . . . may be characteristic of fishes resident
in degraded habitats, where environmental
stresses of toxic chemicals, low dissolved oxygen,
and high microbial populations exist" (p. 722). The
etiology of the disease is unknown. "The multifac-
torial genesis of disease in marine species is be-
coming apparent, involving environmental stress,
facultative pathogens, resistance of hosts, and la-
tent infections" (Sindermann 1979:741).
ACKNOWLEDGMENTS
I would like to thank the Los Angeles County
Sanitation District for providing the monitoring
data and Alan Mearns and Leslie Harris for pro-
viding the age data on Dover sole. The comments
of an anonymous reviewer improved the quality of
the manuscript.
LITERATURE CITED
Allen, M. J., and a. J. Mearns.
1976. Life history of the Dover sole. In W. Bascom
I editor), Coastal water research project annual report
1976, p. 223-228. South. Calif. Coastal Water Res. Proj.,
El Segundo, Calif.
BOWERMAN, B. L., AND R. T. O'CONNELL.
1979. Time series and forecasting; an applied ap-
proach. Duxbury Press, North Scituate, Mass., 481 p.
CLARKE, M. R. B.
1980. The reduced major axis of a bivariate sam-
ple. Biometrika 67:441-446.
CROSS, J. N., J. RONEY, AND G. S. KLEPPEL.
In press. Fish food habits along a pollution gra-
dient. Calif. Fish Game.
HAGERMAN, F B.
1952. The biology of the Dover sole, Microstomas paciftcus
( Lockington). Calif. Dep. Fish Game, Fish Bull. 85, 48 p.
HENDRICKS, T. J.
1980. Currents in the Los Angeles area. In W. Bascom
(editor). Coastal water research project biennial report
1979-1980, p. 243-256. South. Calif. Coastal Water Res.
Proj., Long Beach, Calif
HERSHELMAN, G. P, T.-K. jAN, AND H. A. SCHAFER.
1977. Pollutants m sediments off PalosVerdes. /nW. Bas-
com (editor), Coastal water research project annual report
1977, p. 63-68. South. Calif. Coastal Water Res. Proj., El
Segundo, Calif.
HERSHELMAN, G. P, R SZALAY, AND C. WORD.
1982. Metals in surface sediments from Point Dume to
Point Hueneme. In W. Bascom (editor), Coastal water
research project biennial report 1981-1982, p. 259-
265. South. Calif. Coastal Water Res. Proj., Long Beach,
Calif.
^_Mearns, a. J., AND M. Sherwood.
•Q_JS74. Environmental aspects of fin erosion and tumors in
southern California Dover sole. Trans. Am. Fish. Soc.
103:799-810.
1977. Distribution of neoplasms and other diseases in
mafine fishes relative to the discharge of wastewater.
Ann. N.Y. Acad. Sci. 298:210-224.
MURCHELANO, R. A., AND J. ZlSKOWSKI.
I, 1976. Fin rot disease studies in the New York Bight. InM.
G. Gross (editor), Middle Atlantic continental shelf and
the New Y3rk Bight, p. 329-336. Am. Soc. Limnol.
Oceanogr., Spec. Symp. 2.
1982. Fin rot disease in the New York Bight (1973-
1977). In G. F. Mayer (editor). Ecological stress and the
New York Bight: Science and management, p. 347-
358. Estuarine Res. Found., Columbia, S.C.
Nakai, z., M. kosara, S. kudoh, a. NAGAI, F HAYASHIDA, T.
KUBOTA, M. OGURA, T MiZUSHIMA, AND I. UOTANI.
1973. Summary report on marine biological studies of
Suruga Bay accomplished by Tokai University, 1964-
72. J. Fac. Mar. Sci. Technol., Tokai Univ 7:63-117.
PEARCY, W. G., AND D. HANCOCK.
1978. Feeding habits of Dover sole, Microstomus pacificus;
rex sole, Glyptocephalus zachirus; slender sole, Lyopsetta
exilis; and Pacific sanddab, Citharichthys sordidus, in a
region of diverse sediments and bathymetry off Ore-
gon. Fish. Bull., U.S. 76:641-651.
PERKINS, E. J., J. R. S. GILCHRIST, AND O. J. ABBOT.
1972. Incidence of epidermal lesions in fish of the north-
east Irish Sea area, 1971. Nature (Lond.) 238:101-103.
RICKER, W. E.
1973. Linear regressions in fishery research. J. Fish. Res.
Board Can. 30:409-434.
1975. Computation and interpretation of biological statis-
tics offish populations. Fish. Res. Board Can., Bull. 191,
382 p.
SCHAFER, H.
1982. Characteristics of municipal wastewater. In W.
Bascom (editor), Coastal water research project biennial
report 1981-1982, p. 11-15. South. Calif. Coastal Water
Res. Proj., Long Beach, Calif.
Sherwood, m. J.
1976. Fin erosion disease induced in the laboratory, /n W.
Bascom (editor). Coastal water research project annual
report 1976, p. 149-153. South. Calif. Coastal Water Res.
Proj., El Segundo, Calif.
1978. The fin erosion syndrome. In W. Bascom (editor).
Coastal water research project annual report 1978, p.
203-221. South. Calif. Coastal Water Res. Proj., El
Segundo, Calif.
1980. Recruitment of nearshore demersal fishes. In W.
Bascom (editor). Coastal water research project biennial
report 1979-1980. South. Calif. Coastal Water Res. Proj.,
Long Beach, Calif.
1982. Fin erosion, liver condition, and trace contaminant
exposure in fishes from three coastal regions. In G. F.
Mayer (editor), Ecological stress and the New York Bight:
Science and management, p. 359-377. Estuarine Res.
Found., Columbia, S.C.
Sherwood, M. J., and a. J. mearns.
1977. Environmental significance of fin erosion in south-
em California demersal fishes. Ann. N.Y. Acad. Sci.
298:177-189.
SIEGEL, S.
1957. Nonparametric statistics for the behavioral
sciences. McGraw-Hill, N.Y, 312 p.
Sindermann, C. J.
1979. Pollution-associated diseases and abnormalities of
fish and shellfish: A review. Fish. Bull., U.S. 76:717-
749.
Wilson. K. C, a. J. mearns, and J. J. Grant.
1980. Changes in kelp forests at Palos Verdes. In W Bas-
com (editor), Coastal water research project biennial re-
205
FISHERY BULLETIN: VOL. 83, NO. 2
port, 1979-1980, p. 77-92. South. Calif. Coastal Water YOUNG, D. R., T.-K. JAN, AND T. C. HEESEN.
Res. Proj., Long Beach, Calif. 1978. Cycling of trace metal and chlorinated hydrocarbon
YOUNG, D. R., AND T. C. HEESEN. wastes in the southern California Bight. In M. L. Wiley
1978. DDT, PCB and chlorinated benzenes in the marine (editor), Estuarine interactions, p. 481-496. Acad. Press,
ecosystem off southern California. In R. L. Jolley, H. N.Y
Gorchev., and D. H. Hamilton, Jr (editors). Water chlori- ZAR, J. H.
nation: Environmental impact and health effects, Vol. 2, 1974. Biostatistical analysis. Prentice-Hall, Englewood
p. 267-290. Ann Arbor Sci. Publ., Ann Arbor, Mich. Cliffs, N.J., 620 p.
206
NOTICES
NOAA Technical Reports NMFS published during last 6 months of 1984.
Special Scientific Report — Fisheries
782. A five-year study of seasonal distribution and abundance of fishes and
decapod crustaceans in the Cooper River and Charleston Harbor, S.C,
prior to diversion. By E. L. Wenner, W. P Coon III, M. H. Shealy, Jr , and R
A. Sandifer. July 1984, iii + 16 p., 6 figs., 7 tables.
783. Biomass and density of macrobenthic invertebrates on the U.S. conti-
nental shelf off Martha's Vineyard, Mass., in relation to environmental
factors. By Don Maurer and Roland L. Wigley. July 1984, iv + 20 p., 6
figs., 4 tables.
NOAA Technical Reports NMFS
6. Ichthyoplankton survey of the estuarine and inshore waters of the
Florida Everglades, May 1971 to February 1972. By L. Alan Collins and
John H. Finucane. July 1984, iv + 75 p., 26 figs., and 18 tables.
7. The feeding ecology of some zooplankters that are important prey
items of larval fish. By Jefferson T. Turner July 1984, iii + 28 p., 2
figs., 1 table.
9. Sampling statistics in the Atlantic menhaden fishery. By Alexander
J. Chester August 1984, iii + 16 p., 6 figs., 12 tables.
10. Proceedings of the seventh U.S. -Japan meeting on aquaculture,
marine finfish culture, Tokyo, Japan, October 3-4, 1978. Carl J. Sinder-
mann (editor). August 1984, iii + 31 p., 6 papers.
11. Taxonomy of North American fish Eimeriidae. By Steve J. Upton,
David W. Reduker, William L. Current, and Donald W. Duszynski. Au-
gust 1984, iii + 18 p., 30 figs.
12. Soviet-American cooperative research on marine mammals. Volume 1
- Pinnipeds. Francis H. Fay and Gennadii A. Fedoseev (editors). Sep-
tember 1984, iii + 104 p., 12 papers.
13. Guidelines for reducing porpoise mortality in tuna purse sein-
ing. By James M. Coe, David B. Holts, and Richard W. Butler Sep-
tember 1984, iv + 16 p., 20 figs., 4 tables.
14. Synopsis of biological data on shortnose sturgeon, Acipenser breviros-
trum LeSueur 1818. By Michael J. Dadswell, Bruce D. Taubert, Thomas
S. Squiers, Donald Marchette, and Jack Buckley. October 1984, iv + 45
p., 43 figs., 24 tables.
15. Chaetognatha of the Caribbean Sea and adjacent areas. By Harding
B. Michel. October 1984, iv + 33 p., 41 figs., 5 tables.
16. Proceedings of the ninth and tenth U.S.-Japan meetings on aquacul-
ture. CarlJ.Sindermann (editor). November 1984, iii + 92 p., 11 papers.
17. Identification and estimation of size from the beaks of 18 species of
cephalopods from the Pacific Ocean. By Gary A. Wolff. November 1984,
iv -I- 50 p., 55 figs., 3 tables.
18. A temporal and spatial study of invertebrate communities associated
with hard-bottom habitats in the South Atlantic Bight. By E. L. Wenner,
R Hinde, D. M. Knott, and R. F Van Dolah. November 1984, iii + 104 p., 6
figs., 8 tables.
Some NOAA publications are available by purchase from the Superintendent of Documents,
U.S. Government Printing Office, Washington, DC 20402.
g
INFORMATION FOR CONTRIBUTORS TO THE FISHERY BULLETIN
Manuscripts submitted to the Fishery Bulletin will reach print faster if they conform to the following instructions.
These are not absolute requirements, of course, but desiderata.
CONTENT OF MANUSCRIPT
The title page should give only the title of the paper,
the author's name, his affiliation, and mailing address,
including ZIP code.
The abstract should not exceed one double-spaced
page.
In the text, Fishery Bulletin style, for the most part,
follows that of the U.S. Government Printing Office
Style Manual. Fish names follow the style of the Amer-
ican Fisheries Society Special Publication No. 12, A
List of Common and Scientific Names of Fishes from the
United States and Canada, Fourth Edition, 1980.
Text footnotes should be typed separately from the
text.
Figures and tables, with their legends and headings,
should be self-explanatory, not requiring reference to
the text. Their placement should be indicated in the
right-hand margin of the manuscript.
Preferably figures should be reduced by photography
to 5% inches (for single-column figures, allowing for
50% reduction in printing), or to 12 inches (four double-
column figures). The maximum height, for either width,
is 14 inches. Photographs should be printed on high
quality or glossy paper.
Do not send original drawings to the Scientific Editor;
if they, rather than the photographic reductions, are
needed by the printer, the Scientific Publications Office
will request them.
Each table should start on a separate page. Consis-
tency in headings and format is desirable. Vertical
rules should be avoided, as they make the tables more
expensive to print. Footnotes in tables should be num-
bered sequentially in arabic numerals. To avoid confu-
sion with powers, they should be placed to the left of
numerals.
Acknowledgments, if included, are placed at the
end of the text.
Literature is cited in the text as: Lynn and Reid
(1968) or (Lynn and Reid 1968). All papers referred to
in the text should be listed alphabetically by the senior
author's surname under the heading "Literature Cited."
Only the author's surname and initials are required in
the literature cited. The accuracy of the literature
cited is the responsibility of the author. Abbreviations
of names of periodicals and serials should conform to
Serial Sources for the BIOSIS Data Base. (Chemical
Abstracts also uses this system, which was developed
by the American Standards Association.)
Common abbreviations and symbols, such as
mm, m, g, ml, mg, °C (for Celsius), %, "L , and so forth,
should be used. Abbreviate units of measure only when
used with numerals. Periods are only rarely used with
abbreviations.
We prefer that measurements be given in met-
ric units; other equivalent units may be given in
parentheses.
FORM OF THE MANUSCRIPT
The original of the manuscript should be typed,
double-spaced, on white bond paper. Please triple space
above headings. We would rather receive good dupli-
cated copies of manuscripts than carbon copies. The
sequence of the material should be
TITLE PAGE
ABSTRACT
TEXT
LITERATURE CITED
TEXT FOOTNOTES
APPENDIX
TABLES (Each table should be numbered with an
arabic numeral and heading provided)
LIST OF FIGURES (Entire figure legends)
FIGURES (Each figure should be numbered with
an arabic numeral; legends are desired)
ADDITIONAL INFORMATION
Send the ribbon copy and two duplicated or carbon
copies of the manuscript to:
Dr. William J. Richards, Scientific Editor
Fishery Bulletin
Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service, NOAA
75 Virginia Beach Drive
Miami, FL 33149-1099
Fifty separates will be supplied to an author free of
charge and 50 supplied to his organization. No covers
will be supplied.
• GPO 693-007
/ V \
Fishery Bulletin
"^^ates o^ ^
DEC 10 1985
Vol. 83, No. 3
Woods Hole, Mass.
July 1985
GERRODETTE, TIM, DANIEL GOODMAN, and JAY BARLOW. Confidence limits
for population projections when vital rates vary randomly 207
STEVENSON, DAVID K., and FRAN PIERCE. Life history characteristics of Pan-
daliis montagui and Dichelopandalics leptocertis in Penobscot Bay, Maine 219
HUNTER, JOHN, and RAGAN NICHOLL. Visual threshold for schooling in northern
anchovy, Engraulis mordax 235
LOVE, MILTON S., WILLIAM WESTPHAL, and ROBSON A. COLLINS. Distribu-
tional patterns of fishes captured aboard commercial passenger fishing vessels along
the northern Channel Islands, California 243
HAYNES, EVAN B. Morphological development, identification, and biology of larvae
of Pandalidae, Hippolytidae, and Crangonidae (Crustacea, Decapoda) of the northern
North Pacific Ocean 253
JONES, CYNTHIA. Within-season differences in growth of larval Atlantic herring,
Clupea harengtcs harengus 289
GUILLEMOT, PATRICK J., RALPH J. LARSON, and WILLIAM H. LENARZ.
Seasonal cycles of fat and gonad volume in fish species of northern California rockfish
(Scorpaenidae: Sebastes) 299
FLIERL, G. R., and J. S. WROBLEWSKI. The possible influence of warm core Gulf
Stream rings upon shelf water larval fish distribution 313
CONOVER, DAVID 0. Field and laboratory assessment of patterns in fecundity of
a multiple spawning fish: the Atlantic silverside Menidia menidia 331
LESTER, R. J. G., A. BARNES, and G. HABIB. Parasites of skipjack tuna, Katsu-
womts pelamis: fishery implications 343
WURSIG, BERND, ELEANOR M. DORSEY, MARK A. FRAKER, ROGER S.
PAYNE, and W. JOHN RICHARDSON. Behavior of bowhead whales, Balaena
mysticetiLs, summering in the Beaufort Sea: a description 357
ANKENBRANDT, LISA. Food habits of bait-caught skipjack tuna, Katsuwonus
pelamis, from the southwestern Atlantic Ocean , .r". 1 . . 379
MEDVED, ROBERT J., CHARLES E. STILLWELL, and JOHN J. CASEY. Stomach
contents of young sandbar sharks, Carcharhinus plumbeus, in Chincoteague Bay,
Virginia 395
ROSENBLUM, SHELLY E., and THOMAS M. NIESEN. The spawning cycle of
soft-shell clam. My a arenaria, in San Francisco Bay 403
McFARLAND, W. N., E. B. BROTHERS, J. C. OGDEN, M. J. SHULMAN, E. L.
BERMINGHAM, and N. M. KOTCHIAN-PRENTISS. Recruitment patterns in
young French grunts, Haemulon Jlavolineatum (Family Haemulidae), at St. Croix,
Virgin Islands 413
{Contimied on back cover)
Seattle, Washington
U.S. DEPARTMENT OF COMMERCE
Malcolm Baldrige, Secretary
NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION
John V. Byrne, Administrator
NATIONAL MARINE FISHERIES SERVICE
William G. Gordon, Assistant Administrator
Fishery Bulletin
The Fishery Bulletin carries original research reports and technical notes on investigations in fishery science^ engineering, and economics.
The Bulletin of the United States Fish Commission was begun in 1881; it became the Bulletin of the Bureau of Fisheries in 1904 and
the Fishery Bulletin of the Fish and Wildlife Service in 1941. Separates were issued as documents through volume 46; the last document
was Na 1103. Beginning with volume 47 in 1931 and continuing through volume 62 in 1963, each separate appeared as a numbered bulletin.
A new system began in 1963 with volume 63 in which papers are bound together in a single issue of the bulletin instead of being issued
individually. Beginning with volume 70, number 1, January 1972, the Fishery Bulletin became a periodical, issued quarterly. In this form,
it is available by subscription from the Superintendent of Documents, U.S. Government Printing Office, Washington, DC 20402. It is also
available free in limited numbers to libraries, research institutions, State and Federal agencies, and in exchange for other scientific
publications.
SCIENTIFIC EDITOR, Fishery Bulletin
Dr. William J. Richards
Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service, NOAA
Miami, FL 33149-1099
Editorial Committee
Dr. Bruce B. Collette
National Marine Fisheries Service
Dr. Edward D. Houde
Chesapeake Biological Laboratory
Dr. Merton C. Ingham
National Marine Fisheries Service
Dr. Reuben Lasker
National Marine Fisheries Service
Dr. Donald C. Malins
National Marine Fisheries Service
Dr. Jerome J. Pella
National Marine Fisheries Service
Dr. Jay C. Quast
National Marine Fisheries Service
Dr. Carl J. Sindermann
National Marine Fisheries Service
Mary S. Fizkuyama, Managing Editor
The Fishery Bulletin (ISSN 0090-0656) is published quarterly by the Scientific Publications Office, National Marine Fisheries Service,
NOAA, 7600 Sand Point Way NE, BIN C15700, Seattle, WA 98115. Second class postage is paid in Seattle, Wash., and additional offices.
POSTMASTER send address changes for subscriptions to Superintendent of Documents, U.S. Government Printing Office, Washing^ton,
DC 20402.
Although the contents have not been copyrighted and may be reprinted entirely, reference to source is appreciated.
The Secretary of Commerce has determined that the publication of this periodical is necessary in the transaction of the public business
required by law of this Department Use of funds for printing of this periodical has been approved by the Director of the Office of Manage-
ment and Budget through 1 April 1986.
Fishery Bulletin
CONTENTS
Vol. 83, No. 3
July 1985
GERRODETTE, TIM, DANIEL GOODMAN, and JAY BARLOW. Confidence limits
for population projections when vital rates vary randomly 207
STEVENSON, DAVID K., and FRAN PIERCE. Life history characteristics of Pan-
daliis montagui and Dichelopandalus leptocertis in Penobscot Bay, Maine 219
HUNTER, JOHN, and RAG AN NICHOLL. Visual threshold for schooling in northern
anchovy, Engraulis mordax 235
LOVE, MILTON S., WILLIAM WESTPHAL, and ROBSON A. COLLINS. Distribu-
tional patterns of fishes captured aboard commercial passenger fishing vessels along
the northern Channel Islands, California 243
HAYNES, EVAN B. Morphological development, identification, and biology of larvae
of Pandalidae, Hippolytidae, and Crangonidae (Crustacea, Decapoda) of the northern
North Pacific Ocean 253
JONES, CYNTHIA. Within-season differences in growth of larval Atlantic herring,
Clupea harengus harengtts 289
GUILLEMOT, PATRICK J., RALPH J. LARSON, and WILLIAM H. LENARZ.
Seasonal cycles of fat and gonad volume in fish species of northern California rockfish
(Scorpaenidae: Sebastes) 299
FLIERL, G. R., and J. S. WROBLEWSKI. The possible influence of warm core Gulf
Stream rings upon shelf water larval fish distribution 313
CONOVER, DAVID 0. Field and laboratory assessment of patterns in fecundity of
a multiple spawning fish: the Atlantic silverside Menidia menidia 331
LESTER, R. J. G., A. BARNES, and G. HABIB. Parasites of skipjack tuna, Katsu-
wonus pelamis: fishery implications 343
WURSIG, BERND, ELEANOR M. DORSEY, MARK A. FRAKER, ROGER S.
PAYNE, and W. JOHN RICHARDSON. Behavior of bowhead whales, Balaena
mysticetus, summering in the Beaufort Sea: a description 357
ANKENBRANDT, LISA. Food habits of bait-caught skipjack tuna, Katsuwomis
pelamis, from the southwestern Atlantic Ocean 379
MEDVED, ROBERT J., CHARLES E. STILLWELL, and JOHN J. CASEY. Stomach
contents of young sandbar sharks, Carcharhinus plumbeus, in Chincoteague Bay,
Virginia 395
ROSENBLUM, SHELLY E., and THOMAS M. NIESEN. The spawning cycle of
soft-shell clam, Mya arenaria, in San Francisco Bay 403
McFARLAND, W. N., E. B. BROTHERS, J. C. OGDEN, M. J. SHULMAN, E. L.
BERMINGHAM, and N. M. KOTCHIAN-PRENTISS. Recruitment patterns in
young French grunts, Haemulon flavolineatum (Family Haemulidae), at St. Croix,
Virgin Islands 413
(Continued on next page)
Seattle, Washington
1985
Fbr sale by the Superintendent of Documents, U.S. Government Printing Office, Wtshington
DC 20402-Subscription price per year $21.00 domestic and $26.25 foreign. Cost «r sii^j|I^QQ^g ^QJQ MSSS.
issue: $6.50 domestic and $8.15 foreign. •' "
fUiarins bislaglcaS U<!)iir3tofy
LIBRARY
DEC 10 1985
Contents— Continued
GASKIN, DAVID E., and ALAN P. WATSON. The harbor porpoise, Phocoena pho-
coena, in Fish Harbour, New Brunswick, Canada: occupancy, distribution, and
movements 427
Notes
GROSSMAN, GARY D., MICHAEL J. HARRIS, and JOSEPH E. HIGHTOWER.
The relationship between tilefish, Lopholatilvs chamaeleonticeps, abundance and
sediment composition off Georgia 443
MATARESE, ANN C, and BEVERLY M. VINTER. The development and occur-
rence of larvae of the longfin Irish lord, Hemilepidotus zapiis (Cottidae) 447
POLOVINA, JEFFREY J., and MARK D. OW. An approach to estimating an eco-
system box model 457
SEDBERRY, GEORGE R. Food and feeding of the tomtate, Haemulon aurolineatum
(Pisces, Haemulidae), in the South Atlantic Bight 461
HINES, ANSON H, KENRIC E. OSGOOD, and JOSEPH J. MIKLAS. Semilunar
reproductive cycles in Fundulns heteroclitus (Pisces: Cyprinodontidae) in an area
without lunar tidal cycles 467
HUI, CLIFFORD A. Undersea topography and the comparative distributions of two
pelagic cetaceans 472
BOEHLERT, GEORGE W., and MARY M. YOKLAVICH. Larval and juvenile growth
of sablefish, Anoplopoma fimbria, as determined from otolith increments 475
The National Marine Fisheries Service (NMFS) does not approve, recommend or en-
dorse any proprietary product or proprietary material mentioned in this publication.
No reference shall be made to NMFS, or to this publication furnished by NMFS, in
any advertising or sales promotion which would indicate or imply that NMFS approves,
recommends or endorses any proprietary product or proprietary material mentioned
herein, or which has as its purpose an intent to cause directly or indirectly the adver-
tised product to be used or purchased because of this NMFS publication.
CONFIDENCE LIMITS FOR POPULATION PROJECTIONS
WHEN VITAL RATES VARY RANDOMLY
Tim Gerrodette/ Daniel Goodman,^ aito Jay Barlow^
ABSTRACT
Due to unpredictable future environmental changes, population growth is more realistically viewed as a
stochastic than a deterministic process. Environmental variablity is modeled by allowing the population's
survival and fecundity rates to be correlated random variables. The expected future population vector and
its variance-covariance matrix are computed. The projected total future population size is approximately log-
normally distributed, but confidence limits for future population size can be more accurately computed from
the distribution of the realized factor of increase. Numerical examples illustrate how the calculation of con-
fidence limits for future population size and of the probability that the population will increase in size can be
applied to the management of living resources.
The predicted size of an age-structured population
can be projected if its initial size, age distribution,
and vital rates are known (e.g., Leslie 1945; Keyfitz
1968). Such population projections are commonly
used in fisheries and wildlife management when age-
specific fecundity and mortality rates are available.
However, there is uncertainty in such projections.
First, we rarely know vital rates exactly; rather, we
have estimates of the true rates, and these estimates
are subject to sampling and other types of errors.
Second, the true rates themselves are not constant
with time. Environmental conditions are always
changing, and the vital rates would be expected to
change in response. To an extent, the changes of con-
ditions may themselves be forecast and incorporated
into a population model. Some changes, however, are
unpredictable, and these changes give rise to fluctua-
tions in the vital rates which make our estimates of
population size for some future time less certain.
Nevertheless, it may still be possible to make proba-
bilistic predictions about future population size given
some statistical knowledge about the fluctuating
vital rates.
In this paper we limit ourselves to consideration of
the second of these problems, projecting age-
structured populations when mortality and fecundity
'Scripps Institution of Oceanography, University of California at
San Diego, La Jolla, CA 92093; present address: Southwest
Fisheries Center Honolulu Laboratory, National Marine Fisheries
Service, NOAA, P.O. Box 3830, Honolulu, HI 96812.
^Scripps Institution of Oceanography, University of California at
San Diego, La Jolla, CA 92093; present address: Department of
Biology, Montana State University, Bozeman, MT 59717.
^Scripps Institution of Oceanography, University of California at
San Diego, La Jolla, CA 92093; present address: Southwest
Fisheries Center, La Jolla Laboratory, National Marine Fisheries
Service, NOAA, P.O. Box 271, La JoUa, CA 92038.
Manuscript accepted May 1984.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
rates vary randomly with time. Recently this topic
has been of interest and controversy in a more
theoretical context (Boyce 1977; Cohen 1979a, b;
Daley 1979; Tuljapurkar and Orzack 1980; Tuljapur-
kar 1982; Slade and Levenson 1982). In spite of
earlier results to the contrary (Boyce 1977), analyses
(Sykes 1969; Cohen 1977), and simulations (Slade
and Levenson 1982) have shown that when vital
rates fluctuate randomly with no serial correlation,
the expectation of population size at a future time
will be exactly equal to the population size projected
using the mean vital rates in a deterministic projec-
tion. For application in fisheries and wildlife manage-
ment, the problem is that the distribution of future
population sizes will often be strongly skewed. This
skew means that the mean and variance of future
population size, even if known, are not sufficient to
characterize the distribution and, in particular, not
sufficient to compute confidence hmits for total
population size. In this paper we examine two trans-
formations of this skewed distribution which approx-
imate a normal distribution, and evaluate the ac-
curacy of confidence limits computed from these
transformations.
As pointed out by several of the authors cited
above and earlier by Lewontin and Cohen (1969) for
a non-age-structured population, stochastic effects
can cause the modal or most likely population trajec-
tory to decline to extinction, even though the ex-
pected or mean population size is growing at a
geometric rate. Clearly, if we are to use population
projections in fisheries and wildlife management, we
should be concerned about the effects of natural
variability on the results of our projections. In
response to this concern, we have written two com-
207
FISHERY BULLETIN: VOL. 83, NO. 3
puter programs for stochastic population projections
which can serve as research and management tools.
Here we illustrate the utility of these programs with
numerical examples, compare our results with recent
theoretical analyses, and discuss the implications of
these results to the management of living resources.
METHODS
Sykes (1969) presented three models for incor-
porating stochasticity into population projections. He
concluded that the observed variability in human
demographic projections was best described by his
third model, in which the elements of the Leslie
matrix (the effective fecundity rates and the survival
rates) are random variables, each with a specified
mean and variance, and with specified covariances
between them. The model does not allow for serial
covariance in vital rates between successive time
periods.
Let Ut be a population vector of co age classes at
time t. The stochastic projection model is
n,^i = {A + A,)n„ t = 0,1,2, .. .
where i4 is a constant projection matrix of mean vital
rates and A, is a matrix of random deviations whose
elements have a specified covariance structure
{Cov(A,,Aj)} but which are uncorrelated in time. Let
N, = ^ Ufj be the total population size at time t. It
is convenient to normalize the projected population
to the initial population size and consider the distri-
bution of the ratio N,INq. The mean and variance of
this ratio are given by
EiN./N,) = EiN,)INo
and
Yar (NtlNo) = VsLriN,)/Nl
= 11 Gov {nt„ntj)/Nl
1=1 j=i
From Sykes (1969, equations 19 and 20), the mean
and variance of the population vector are given by
E(n,) = {E{n,,)} = A'no
and
Var(7i,) = {Cov(%,n(^)}
t-i
k=0 Vo=l fl=l
Cov(A,„, A,„)
[Gov (nfc„,n^p) -i- Ein,,JE{n,,p)] [ A '
't-l-k
where A ' is the transpose of A and where the curly
brackets indicate that the expression inside them is
the tth element of the vector or the ijth element of
the matrix considered.
Tuljapurkar and Orzack (1980) predict that for
large t, Nf/N^ will be lognormally distributed. The
mean and variance of the normally distributed
variable log {Nf/No) are calculated from the mean
and variance of the lognormally distributed variable
NtIN, by
E[\og(N,/No)] = \og[EiN,/No)] -
par[log(iV,/iVo)]
}
and
Var
[log(^,/^o)] = log|'^^^^^l!
(Aitchison and Brown 1957). We have found in simu-
lations that the distribution of the realized factor of
increase (Nf/NQf" is approximately normal. Based
on the assumption that the realized factor of increase
is normally distributed, the mean and variance of
(Nt/NQf" are computed from the mean variance of
Nf/NQ by methods given in Appendices 1 and 2.
Using the formulae of Sykes (1969), the mean and
variance of each age class in the future population
can be computed analytically. Confidence intervals
for the total population size and for the realized fac-
tor of increase, and an estimate of the probability
that the future population will be larger than the
starting population, are computed based on the
assumption that either log (NflNo) or (A/^(/iVo)^" is nor-
mally distributed.
We can also simulate the growth of an age-struc-
tured population under fluctuating environmental
conditions. At each time period, a new set of fecun-
dity and survival rates, the elements of the Leslie
matrix, are chosen and used to project the popula-
tion. Each fecundity and survival rate is a normally
distributed random variable with specified mean,
variance, and covariance with every other fecundity
and survival rate. The projection, starting from the
208
GERRODEITE ET AL.: CONFIDENCE LIMITS FOR POPULATION PROJECTIONS
same initial population vector, may be replicated a
given number of times. From these replicated projec-
tions, the mean, variance, and covariances of the
population vector are computed, together with
statistics on a variety of other demographic para-
meters. The distributions of the final population size
and the realized factor of increase are tabulated.
The computer programs to accomplish these
stochastic projections are called, respectively, SPP
(Stochastic Population Projection) and SLT (Sto-
chastic Life Table simulation). Program listings and
guides to the use of both programs are given in Ger-
dynamics of the population are given in Table 2
(taken from Goodman 1981: table 1) and confer a
population growth rate of about 8% per year. The
initial age vector in this case was chosen to be the
stable age distribution with a total of 100,000
females. Values for the standard deviations in vital
rates in Table 2 were selected by choosing reason-
able values for their coefficients of variation. Corre-
lations in vital rates were assumed to be 0.9 between
fecundities at different ages, 0.9 between survival
rates at different ages, and 0.5 between all fecun-
dities and survival rates.
Table 1.— initial population vector, mean vital rates, and covariance matrix of vital rates for a
three age-class population projection. In the covariance matrix, F refers to fecundity rate, P to
survival rate, and numbers to age classes.
Age
class
Initial
population
size
Mean
fecundity
rate
Mean
Covariance matrix
rate
F1
F2
F3
PI
P2
P3
1
100
0.1
0.7
F^
0.0010
0.0020
0.0020
0.0005
0.0005
0.0
2
80
1.0
0.9
F2
0.0050
0.0045
0.0010
0.0010
0.0
3
50
230
0.4
0.0
F3
p^
P2
P3
0.0050
0.0010
0.0050
0.0010
0.0045
0.0050
0.0
0.0
0.0
0.0
rodette et al. (1983). Although lengthy, these pro-
grams are suitable for use on many microcompu-
ters.
Numerical Examples
Two numerical examples are presented to verify
various analytic results and to illustrate the use of
programs SPP and SLT in a management context.
The first example is a simple artificial life table
with three age classes. The mean vital rates and the
covariance matrix for the vital rates are given in
Table 1. This example was used to compare the
predicted mean and variance in projected population
size based on Sykes' (1969) formulae with the actual
mean and variance from the simulation. The example
was also used to test the assumption that ultimate
population sizes will be lognormally distributed, and
in particular whether accurate confidence limits for
the tails of the distribution can be made based on this
assumption.
The second example is based on a real population.
A northern fur seal, Callorhinus ursimis, population
is projected using vital rates consistent with a phase
of rapid growth which occurred earlier in this cen-
tury. The mean vital rates which govern the
Table 2.— initial population vector, means, and standard
deviations (S.D.) of vital rates for a fur seal population projec-
tion used as a numerical example in the text. Mean rates are
taken from Goodman (1981: table 1). Each age class repre-
sents 1 yr, and only the female portion of the population is
tabulated. The initial population vector is in the stable age
distribution with a total of 100,000 females.
Initial
Mean
Mean
Age
population
fecundity
survival
class
size
rate
S.D.
rate
S.D.
1
17,618
0.0000
0.0000
0.8786
0.0439
2
14,312
0.0000
0.0000
0.8786
0.0439
3
11,627
0.0050
0.0003
0.8837
0.0442
4
9,500
0.0151
0.0008
0.8888
0.0444
5
7,807
0.2631
0.0132
0.9039
0.0090
6
6,525
0.3693
0.0185
0.9191
0.0092
7
5,545
0.4250
0.0213
0.9342
0.0093
8
4,789
0.4604
0.0230
0.9443
0.0094
9
4,182
0.4756
0.0238
0.9494
0.0095
10
3,671
0.4705
0.0235
0.9443
0.0094
11
3,205
0.4655
0.0233
0.9292
0.0093
12
2,753
0.4554
0.0228
0.9039
0.0090
13
2,301
0.4402
0.0220
0.8786
0.0088
14
1,869
0.4250
0.0213
0.8484
0.0085
15
1,466
0.4048
0.0202
0.8029
0.0080
16
1,089
0.3794
0.0190
0.7524
0.0075
17
757
0.3542
0.0177
0.6918
0.0069
18
484
0.3187
0.0159
0.6262
0.0063
19
280
0.2833
0.0142
0.5454
0.0055
20
141
0.2479
0.0124
0.4494
0.0045
21
59
0.2024
0.0101
0.3282
0.0033
22
18
0.1467
0.0073
0.1009
0.0010
23
2
0.0657
0.0033
0.0000
0.0000
Total
100,000
209
FISHERY BULLETIN: VOL. 83, NO. 3
RESULTS
Example 1.
The results of the stochastic projection by program
SPP are presented in Table 3. The second column
shows the expected (mean) population vector for
each time step. The mean population vector is obtain-
ed by projecting w^ith the mean vital rates. The co-
variance matrix for the population vector gives, on
the diagonal, the variances of each age class and,
above the diagonal, the covariances between age
classes.
The calculations using Sykes' formulae concur with
the results of the Monte Carlo simulation of a sto-
chastic population projection, taking the entries of
the life table as time-varying random variables (pro-
gram SLT). In Tables 4 and 5 the results of the simu-
lation are presented. The means and covariances of
the vital rates actually achieved on this particular
run of program SLT are shown in Table 4 and are
close to the specified rates given in Table 1. By com-
paring the results in Table 5 with those of time step 6
in Table 3, we see that the results of the simulation
(SLT) and the analytic solution (SPP) agree closely.
The distribution of the ratio of the final population
size to the initial population size is shown as a histo-
gram in Figure 1 A. The curve is skewed to the right,
Table 3.— Results of the stochastic projection of the population, given in Table 1, through 6 time steps
(program SPP). The columns labeled "95% C.L." give the lower and upper 95% confidence limits for total
population size and for the realized factor of increase relative to the initial population. The last column
gives the probability P that the final population size will be greater than the initial population size.
Expected
Time population
step vector
Covariance matrix
Total population
Lower 95% C.L.
Mean Upper 95% C.L.
Factor of increase
Lower 95% C.L.
Mean Upper 95% C.L.
100
80
50
110
142.5
18.0
14.4
70
50.0
36.0
72
32.0
110
261.5
48.4
73.5
77
131.0
46.1
63
65.3
113
365.3
94.4
154.1
77
189.7
68.7
69
136.4
116
485.5
158.2
219.9
79
244.9
99.0
69
184.2
119
559.6
230.8
287.1
81
307.5
141.7
71
231.0
121
736.2
309.8
366.2
83
367.0
189.7
73
283.5
230
252
250
259
264
271
277
215
289
197
307
193
335
187
356
184
378
182
400
1.096
1.041
1.039
1.033
1.031
1.029
0.934
1.258
0.925
1.156
0.934
1.134
0.950
1.116
0.957
1.105
0.961
1.096
0.8764
0.7545
0.7856
0.7808
0.7910
0.7990
Table 4.— Means, variances, and covariances of vital rates achieved
during a Monte Carlo projection of the population given in Table 1 (pro-
gram SLT). Values were computed on the basis of 30,000 vectors of
vital rates. F refers to fecundity rate, P to survival rate, and numbers
to age classes. Values in this table should be compared with the
"target" values in Table 1.
Covariance matrix
Mean
F^
F2
F3
PI
P2
F2
1.00027
F3
0.39998
PI
0.69992
P2
0.89744
P3
0.00000
0.00505
0.00453
0.00502
0.00100
0.00099
0.00501
0.00092
0.00091
0.00414
0.00435
P3
F1 0.10016 0.00101 0.00202 0.00201 0.00049 0.00045 0.0000
0.0000
0.0000
0.0000
0.0000
0.0000
210
GERRODETTE ET AL.: CONFIDENCE LIMITS FOR POPULATION PROJECTIONS
Table 5.— Results of the Monte Carlo simulation of the 6 time-
step projection of the population whose age structure and vital
rates are given in Table 1 (program SLT). Sample size for the
simulation was 5,000 trials. Results in this table should be com-
pared with the "predicted" values in the last row of Table 3.
Here P is the proportion of final population sizes greater than
the initial population size.
Mean
Mean
Mean
popula-
total
factor
Time
tion
popula-
of
step
vector
Covariance matrix
tion
mcrease
P
121
741.3 314.7 369.8
6
83
73
371.7 187.6
281.5
277
1.029
0.7954
as anticipated. Both the logarithmic transformation
(Fig. IB) and the root transformation (Fig. IC)
appear to normalize the distribution. When the
cumulative frequency distributions are plotted on
normal probability scales (dots in Fig. 1), however,
the root transformation appears superior to the
logarithmic. The dots in Figure IC are nearly linear,
indicating that the distribution is close to normal.
In Table 6 the accuracy of the 95% confidence
limits for the total population size computed by the
logarithmic and root transformations is compared
for projections of 2, 5, and 10 time steps, using the
same numerical example. Program SLT calculates
the proportion of final populations which fall above
and below the computed upper and lower confidence
limits. We expect that 2.5% of the cases should fall
above the upper limit and 2.5% below the lower limit
if the 95% confidence interval has been correctly
estimated. Table 6 shows that both the logarithmic
and the root transformations do a fair job of esti-
mating the 95% confidence limits. The root transfor-
mation, however, appears more accurate in this
example, as well as in other examples we have tried,
when the number of time steps is small. When the
number of time steps is large (50-100), both transfor-
mations produce normally distributed variables.
Since the root transformation gave the most accu-
rate results for short projections, we used this trans-
formation in program SPP to compute a confidence
interval on total population size. More details of the
Figure 1 .- Distributions of future total population size under
variable conditions. Histograms show the percentage frequency,
and dots the cumulative percentage frequency plotted on a normal
probability scale, for 5,000 stochastic projections of the population
given in Table 1 for six time steps. A. Distribution of NqINq, the
final population size divided by the initial. B. Distribution of logg
>-
o
z
HI
a
LU
CC
U-
LU
<
LU
o
CC
LU
20
10
I I rii I I I I I I I I I i~i I I I
0.5 1.0 1.5 2.0 2.5
Ne/No
99.9
99.0
90.0
50.0
10.0
- 1.0
- 0.1
20 -
10
B
I I r
-0.5
20 -
10
Jl •■
WNo).
crease.
C. Distribution of (NqINq)^'^, the realized factor of in-
(Ng/No)
1/6
99.9
99.0
90.0
50.0
- 10.0
- 1.0
0.1
-1 — I — I — I — I — I — I — I — I — I I r
0.0 0.5 1.0
LOGeCNg/No)
99.9
99.0
90.0
50.0
10.0
- 1.0
- 0.1
■i — I rii I — I — I — r~i — I — I I I ii r
0.9 1.0 1.1 1.2
>
o
2
LU
Zi
O
Hi
CO
Li.
LU
o
<
LU
o
CC
m
CL
LU
>
3
ID
o
211
FISHERY BULLETIN: VOL. 83, NO. 3
Table 6. — Accuracy of the 95% confidence limits (C.L.) on popula-
tion size estimated by the logarithmic and root transformations of
the distribution of total population size. For each transformation,
the estimated lower and upper confidence limits are shown for pro-
jections of the population given in Table 1 for 2, 5, and 10 time steps.
The columns labeled "Proportion beyond C.L." give the actual pro-
portion of 10,000 stochastic projections using program SLT which
fall below the estimated lower limit and above the estimated upper
limit for each transformation. Each set of projections was replicated
3 times. The root transformation estimates the 95% confidence in-
terval on population size more accurately, especially for short pro-
jections.
Transformation
No. of
time steps
to
projection
Logar
thmic
Root
Estimated
95% C.L.
Proportion
beyond
C.L.
Estimated
95% C.L.
Proportion
beyond
C.L.
2
Lower
Upper
199
309
0.0311
0.0317
0.0295
0.0160
0.0181
0.0199
197
307
0.0256
0.0255
0.0231
0.0204
0.0214
0.0228
5
Lower
Upper
187
380
0.0290
0.0285
0.0318
0.0227
0.0219
0.0215
184
378
0.0251
0.0242
0.0260
0.0245
0.0235
0.0235
10
Lower
Upper
178
489
0.0266
0.0280
0.0286
0.0226
0.0211
0.0217
175
486
0.0238
0.0252
0.0257
0.0234
0.0221
0.0226
example projection are shown in the columns on the
right side of Table 3. The mean and the 95% con-
fidence interval for the total population size and for
the realized factor of increase are given for each time
step. As the population vector approaches the stable
age distribution, the ratio between successive mean
total population sizes approaches the asymptotic
value 1.0240. The mean realized factor of increase
shown in Table 3, which is computed relative to the
initial population, does not converge on this asymp-
totic value; nor can the mean realized factor of in-
crease be computed from the ratio of the mean final
population size to the initial population size. Instead,
the mean and variance of the realized factor of in-
crease are computed by methods described above.
The probability that the total population size will
have increased over its initial value is also shown for
each time step in the last column of Table 3. In this
particular example, since we did not begin with the
stable age distribution, this probability decreases at
first and then increases. As a further check, program
SLT computes the proportion of cases in which the
final population was greater than the initial popula-
tion, and this answer (0.7954, Table 5) is close to the
probability computed analytically by program SPP
assuming that the realized factor of increase is nor-
mally distributed (0.7990, Table 3). Given a popula-
tion whose age structure and dynamics conform to
the values given in Table 1, therefore, we can make
the statement that there is an 80% chance that the
population will be larger 6 time steps from now and a
20% chance that it will be smaller.
Example 2.
The results of the stochastic projection of the
northern fur seal population by program SPP are
given in Table 7 and Figure 2. Table 7 shows that
after 5 yr, the expected (mean) number of 9-yr-olds,
for example, is 6,188 with a standard deviation of
333. The expected total population size is 147,982
with a standard deviation of 8,832. The mean and
standard deviation of the realized factor of increase
are 1.0812 and 0.0129, respectively; from these
values we compute the 99% confidence interval on
population size to be from 126,410 to 171,930. Note
212
GERRODETTE ET AL.: CONFIDENCE LIMITS FOR POPULATION PROJECTIONS
Table 7.— Results of the 5-yr stochastic pro-
jection of the northern fur seal population, bas-
ed on the age structure and vital rates given in
Table 2. Probability that the final population
> initial population = 0.999 -t-.
Expected
Age
population
Standard
class
size
deviation
1
26,071
1,672
2
21,179
1,619
3
17,205
1,519
4
14,058
1,402
5
11,553
1,280
6
9,655
972
7
8,205
720
8
7,087
516
9
6,188
333
10
5,432
121
11
4,743
106
12
4,075
92
13
3,406
76
14
2,767
62
15
2,170
49
16
1,611
36
17
1,121
25
18
717
16
19
415
9
20
209
5
21
87
2
22
26
1
23
2
0.05
Total
147,982
Total
Factor of
population
increase
Low/er99% C.L.
126,410
1.0480
Expected value (mean)
147,982
1.0812
Upper 99% C.L.
171,930
1.1145
that, as will generally be the case, the confidence in-
terval for total population size is not symmetric
about the mean value.
In the last line of Table 7, the probability of an in-
creased population is shown to be very close to 1.0.
In other words, it is virtually certain that the popula-
tion will have increased in size after 5 yr. Figure 2
presents the results for total population size graph-
ically. The 95% and 99% confidence limits computed
by program SPP are shown for each time step. The
confidence limits grow nearly geometrically.
DISCUSSION
Fishery and wildlife management often involves
predictions of population size, and, owing to im-
perfect knowledge of the world, these predictions are
uncertain. Accordingly, a practical analysis attaches
estimates of confidence intervals for any given
prediction. The programs described in this paper
carry out the computation of confidence intervals for
projections of age- structured populations, if we can
specify the statistics of the variation in the age-
specific vital rates. Realistically, we do not expect
there to be be many examples where the statistics of
the variation in vital rates are genuinely known with
substantial precision, for these rates are difficult to
measure in natural populations. Nevertheless, in an
imperfect world, management decisions must be
made with imperfect data. A considerable compo-
nent of the uncertainty in a population prediction will
be owing to the phenomena treated in this paper.
Thus, even the use of very rough guesses at the sta-
tistics of the variation in the age-specific vital rates,
in order to estimate confidence intervals in a popula-
tion projection, is preferable to neglecting this
source of variation entirely. At the very least, incor-
poration of speculative estimates in this applied con-
text will allow the exploration of "what if " questions
in a fashion that can indicate priorities for future
data gathering.
In many fish and aquatic invertebrate species,
there is an enormous variation in the success of year
classes. In such cases the population dynamics may
be dominated by the overwhelming abundance of one
180 |- 95% Confidence limits
99% Confidence limits
■g 160
0 12 3 4 5
YEARS IN FUTURE
Figure 2. -Confidence limits for future total female population size
for the northern fur seal, based on the schedule of vital rates in
Table 2. The solid line plots the mean population trajectory.
213
FISHERY BULLETIN: VOL. 83, NO. 3
or two cohorts. The environmental factors which
lead to such huge variations in recruitment are as yet
imperfectly understood for most species. In order to
predict future population sizes, the year-to-year
variation could be incorporated into the variances of
the effective fecundity terms in the first row of the
Leslie matrix. This will lead to enormous (but
realistic) confidence limits for predicted future
population sizes of such stocks. A more fruitful use of
the results of this paper, however, would be to
separate recruitment uncertainty from survival
uncertainty and to calculate a confidence interval on
future population size given recruitment success for
a particular cohort. Among harvested species such a
conditional forecast could be used to incorporate
environmental variation into management recom-
mendations.
In keeping with the fact that applied management
may often depend on very elementary quantities, we
also calculate a particularly important special
statistic of the distribution of projections- the prob-
ability that the population will increase under the
specified conditions. In the first example, the prob-
ability of an increased population was found to be
about 0.8. In the second example, the fur seal popula-
tion projection, there is a higher probability that the
population will increase. Starting with the female
population of 100,000, the calculations indicate 99%
certainty that the population will have increased to
between 126,410 and 171,930 in 5 yr.
Our simulations of stochastic population growth
differ from previous efforts by Boyce (1977) and
Slade and Levenson (1982) by allowing all vital rates
to vary simultaneously, rather than only one at a
time, and by permitting correlations among the vital
rates to be specified. In the stochastic growth models
of Cohen (1977, 1979a) and Tuljapurkar and Orzack
(1980), at each time step the population finds itself in
one of several possible environments. Within each
environment vital rates are fixed. By contrast, here
we model a single variable environment whose condi-
tions, as reflected in the population's vital rates at
any point in time, are never precisely duplicated. The
results of Example 1 verify the results for the mean
and variance of future population vectors and show
that the mean and variance for total ultimate popula-
tion size can be computed from Sykes' formulae. Our
results confirm the conclusions of Cohen (1977), Tul-
japurkar and Orzack (1980), and Slade and Levenson
(1982) that the expected mean value of a stochastic
population projection with no serial correlation in
vital rates is equivalent to the value projected deter-
ministically from mean vital rates. Cohen (1979a, b)
and Tuljapurkar (1982) address the more general
question of serial correlation in vital rates.
All of the work cited above has been concerned
v^dth the state of the population at a time in the
future much greater than will generally be useful in
management. In this paper we have examined the
stochastic behavior of the population at a shorter
time in the future. Example 1 has verified that the
distribution of ultimate population sizes from
stochastic population projections is approximately
lognormal (Tuljapurkar and Orzack 1980). From the
perspective of fitting the tails of this distribution for
a small number of time steps t, however, it appears
better to assume that the 1/tth power of the distribu-
tion is normally distributed. In either case the distri-
bution of ultimate population sizes is skewed (with
long tails at the higher values), and the skew
becomes more pronounced as t increases. An impor-
tant property of such a distribution is that the most
likely or modal population value will always be
smaller than the mean. How much smaller depends
on the number of time steps t, and on the variances
and covariances among the survival and fecundity
rates.
An interesting theoretical and practical problem is
to find a descriptor of population growth under
stochastic conditions which characterizes the skewed
distribution of ultimate population size. Cohen
(1979a) has proposed two measures of long-run popu-
lation growth: A, the ensemble average of realized
factors of increase; and pi, the factor of increase need-
ed to realize the ensemble average of final population
sizes. The first is a measure based on growth rates,
while the second is based on population sizes (Cohen
1979b). The average realized factor of increase calcu-
lated here is analogous to A. If the Leslie matrix of
mean vital rates is known, pi is easily calculated as
the dominant eigenvalue of that matrix. The prob-
lem, as we have seen, is that under stochastic condi-
tions the mean of the population sizes is not very in-
formative and may, in fact, be misleading. Tul-
japurkar (1982) has proposed a growth measure a
which leads to the approximate median population
size. The two measures proposed here -namely, E
[(iV^/A^o)'"] a.ndE[\og{N,/N(f)]-are close approxima-
tions to the rate of growth leading to the modal
population size. As such, they may loosely be said to
describe the most probable trajectory of the popula-
tion under stochastic conditions.
ACKNOWLEDGMENTS
The work was supported by a National Research
Council Fellowship to the first author and by NOAA
214
GERRODETTE ET AL.: CONFIDENCE LIMITS FOR POPULATION PROJECTIONS
Contract 80-ABC-00207 to the second. We thank
Douglas Chapman for his helpful comments. Typing
assistance was provided by Lorraine Prescott and
her staff at the Southwest Fisheries Center.
LITERATURE CITED
AlTCHISON, J., AND J. A. C. BROWN.
1957. The lognormal distribution with special reference to its
uses in economics. Cambridge Univ. Press, Cambridge,
176 p.
BOYCE, M. S.
1977. Population growth with stochastic fluctuations in the
life table. Theor. Pop. Biol. 12:366-373.
Cohen, J. E.
1977. Ergodicity of age structure in populations with Marko-
vian vital rates, III: Finite-state moments and growth rate;
an illustration. Adv. Appl. Prob. 9:462-475.
1979a. Long-run growth rates of discrete multiplicative
processes in Markovian environments. J. Math. Anal. Appl.
69:243-251.
1979b. Comparative statics and stochastic dynamics of age-
structured populations. Theor. Pop. Biol. 16:159-171.
Daley, D. J.
1979. Bias in estimating the Malthusian parameters for
Leslie matrices. Theor. Pop. Biol. 15:257-263.
Gerrodette, T., D. Goodman, and J. Barlow.
1983. Two computer programs to project populations with
time-varying vital rates. Natl. Mar. Fish. Serv. Tech. Memo.
N{)AA-TM-NMFS-SWFC-28, 56 p. (Copies are available
through NTIS or from the Southwest Fisheries Center,
National Marine Fisheries Service, NOAA, P.O. Box 271, La
JoUa, CA 92038.)
Goodman, D.
1981. Life history analysis of large animals. In C. W. F'owler
and T. D. Smith (editors). Dynamics of large mammal popula-
tions, p. 415-436. Wiley, N.Y.
Keyfitz, N.
1968. Introduction to the mathematics of population. Addi-
son-Wesley, Reading, Mass., 450 p.
Leslie, P. H.
1945. On the use of matrices in certain population mathema-
tics. Biometrika 33:183-212.
Lewontin, R. C, and D. Cohen.
1969. On population growth in a randomly varying environ-
ment. Proc. Natl. Acad. Sci. (U.S.) 62:1056-1060.
Slade, N. a., and H. Levenson.
1982. Estimating population growth rates from stochastic
Leslie matrices. Theor. Pop. Biol. 22:299-308.
Sykes, Z. M.
1969. Some stochastic versions of the matrix model for popu-
lation dynamics. J. Am. Stat. Assn. 64:111-130.
Tuljapurkar, S. D.
1982. Population dynamics in variable environments. II.
Correlated environments, sensitivity analysis and dynamics.
Theor. Pop. Biol. 21:114-140.
Tuljapurkar, S. D., and S. H. Orzack.
1980. Population dynamics in variable environments. I. Long-
run growth rates and extinction. Theor. Pop. Biol. 18:314-
342.
215
FISHERY BULLETIN: VOL. 83, NO. 3
APPENDIX 1.
Calculation of the mean and variance of the realized factor
of increase, assuming it is normally distributed.
Let A, the realized factor of increase, be defined as the ^th root of the ratio of the
population size at time t to the initial population size:
nJ
or
Let ^ be the mean and v the variance of A. The mean and variance of A' are given by
formulae in the Methods section. The problem is to find the mean and variance of A.
Let F (/^,v) be a function which gives the ^th moment of A:
F(m,v) = E(A').
Similarly let G{^a,v) be a function which gives the variance of A' in terms of the ^th
and 2tth moments of A:
G(m,v) = F(A2')- [F(A')]2.
Now assume that A is normally distributed. Appendix 2 gives a recursive algorithm
which allows any moment of a normally distributed variate to be calculated. From
the tth and 2tth moments of A, the functions F and G can be computed from the
equations above. Generally, F and G will be tth and 2tth order polynomials in fu and
V. Then, with F and G known, we have a system of two equations
F(m,v) - Eil^) = 0
G(m,v) - Var (A' ) = 0
in two unknowns. Given initial estimates of ^ and u, a two-variable version of
Newton's method, or any similar iterative technique, can be used to converge on a
simultaneous solution.
216
GERRODETTE ET AL.: CONFIDENCE LIMITS FOR POPULATION PROJECTIONS
APPENDIX 2.
A recursive algorithm for computing the higher order
moments of the normal distribution.
The moment generating function for the normal distribution is
2
where ^ is the mean and v is the variance of the normal variate x. The nth moment of x is found by
evaluating, at ^ = 0, the nth derivative ofM^{t) with respect to t. The wth differentiation with respect to t
leads to the series
(m + vO"M^(0 + ... + A(m+ vt)" v'^ M^{t) + 5(m + vty-^v^^^M^it) + ...,
which, evaluated oXt = 0, gives
where A and B are coefficients and a and ft are exponents such that a + 2/3 = w. The next [(n + l)th] dif-
ferentiation of the middle terms gives
A(m + vtf^^ v^M,{t) + Aa{yL + vty-^ v^^^ MJt)
+ B{yL + vt)"-^ v^*^ M,{t) + B{q - 2)(m + vt)'-^ v^^^ M^(t)
= ... + (Aa + 5)(m + vty-^ v'^^^ M,{t) + ...
which, evaluated at ^ = 0, gives
... + (Aa + 5V"^ v^^l + ... .
Thus the coefficient of each term of the series of the {n + l)th moment can be computed from the two
terms in the series of the nth moment "before" and "after" it. The exponents of ^ and v follow the regular
pattern shown.
217
LIFE HISTORY CHARACTERISTICS OF
PANDALUS MONTAGUI AND DICHELOPANDALUS LEPTOCERUS
IN PENOBSCOT BAY, MAINE
David K. Stevenson^ and Fran Pierce^
ABSTRACT
A number of life history characteristics of two species of pandalid shrimp from Penobscot Bay, ME, were
inferred from length-frequency and relative abundance data collected on five occasions during a bottom
trawl survey in 1980-81. Pandalus montagui is a sequential hermaphrodite. Sex transition occurs
throughout the year, but most transitional individuals were observed in late March. Most individuals change
sex shortly before or after reaching age 2, but some do so either a year earlier or a year later. Ovigerous
females were observed from late November through January; eggs are apparently produced during the sec-
ond, third, and fourth years. Fifteen percent of the 0 age-group caught in the fall of 1980 were females
which may never have functioned as males. Growth was rapid in the spring and summer and negligible in
the late fall and winter. Females which changed sex at age 1 were larger than females which changed sex a
year later. Dichelc/pandalus leptocerus is not hermaphroditic. Ovigerous females were collected primarily in
late November and early December. Some females produce eggs during their first and second years, but
most do so only during their second year. None of the females caught during this study appeared to be older
than age 2; a few large males remained in the population during their third year of life. Females of both
species were larger than males of the same age-group, a distinction which was attributed to differences in
growth rate and, for P. montagui, was associated with earlier sex transition. Larger shrimp of both species
migrated down the Bay into deeper water as the winter progressed.
The Pandalidae are a family of boreal, subarctic
shrimp composed of 2 genera and about 20 species.
Four species {Pandalus borealis, P. montagui, P.
propinquus, and Dichelapandalus leptocerus) are
common in offshore waters of the Gulf of Maine
(Wigley 1960). Of these, P. borealis is the largest,
reaching a maximum total length of 17-18 cm (7 in),
and has been the object of a directed winter fishery
in coastal waters of the Gulf of Maine since the late
1930s (Scattergood 1952) and in coastal and offshore
waters since 1958^. This species is also exploited
commercially on the west coast of North America, in
the Canadian Maritime Provinces, on the west coast
of Greenland, in the Norwegian and North Seas, and
in the northwest Pacific (Balsiger 1981).
Pandalus montagui and D. lefptocerus are smaller
species (maximum length 10 cm or 4 in), which are
harvested incidentally with P. borealis in the Gulf of
'Zoology Department, University of Maine, Orono, ME 04469
and Maine Department of Marine Resources, West Boothbay Har-
bor, ME 04575.
^Maine Department of Marine Resources, West Boothbay Har-
bor, ME 04575.
^Stickney, A. P. 1980. A characterization of the northern
shrimp fishery of Maine. In C. J. Walton (editor). Fisheries
management and development. Vol. Ill, Element D: Character-
ization of the shellfisheries, p. 244-293. Completion report to the
State Planning Office, Oct. 1, 1978-Sept. 30, 1979, Maine Depart-
ment of Marine Resources, Augusta.
Maine, but have little or no market value because of
their size. Pandalus montagui is also harvested as an
incidental species in the Gulf of St. Lawrence
(Balsiger 1981), and for many years was the object of
several localized commercial beam trawl fisheries in
the southern North Sea and in Morecambe Bay,
northwest England, until declining stock sizes led to
the demise of the fisheries in the Thames estuary
(described by Mistakidis 1957) and Morecambe Bay
in the 1950s and 1960s. Warren (1973) described a
fishery for P. montagui in the Wash on the east coast
of England which was still active in the early 1970s.
Pandalus propinquus is also smaller than P. borealis
and is generally restricted to deeper water (165-330
m in New England waters according to Wigley
1960); consequently it is rarely taken in Gulf of
Maine commercial catches.
Pandalus montagui is differentiated taxonomically
into two subspecies: P. montagui tridens in the
North Pacific and P. montagui montagui in the
North Atlantic from the Arctic south to the British
Isles and Cape Cod (Simpson et al. 1970) or Rhode
Island (Rathbun 1929). According to Simpson et al.
P. montagui montagui is found in estuaries, coastal
waters, and offshore in depths of 5 to over 700 m,
but is more common in shallow waters (20-90 m); at
depths > 90 m it is gradually replaced by P. borealis.
Manuscript accepted August 1984.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
219'^^
Squires (1968) reported that P. borealis occurred
together with P. montagui in depths < 200 m in the
Gulf of St. Lawrence and southwest of Newfound-
land, but at depths between 200 and 300 m with a
smooth detritus bottom and temperatures of 4°-6°C,
only P. borealis were caught; in colder temperatures
(-1° to 3° C) in this same depth range, P. montagui
were more abundant. Pandalus montagui was
described as a more eurythermal and eurybathic
species than P. borealis. Of all the pandalids in the
northwest Atlantic, P. montagui is the only one
which inhabits colder Arctic waters < 1.5°C (Squires
1966). The Atlantic subspecies of P. montagui has
been the subject of several biological studies
(Mistakidis 1957; Allen 1963; Couture and Trudel
1969a, b).
Dichel&pandahis leptoceru^ is distributed in the
northwest Atlantic from Newfoundland to North
Carolina (Rathbun 1929). It has not been reported
from the northeast Atlantic and is rare in the north-
ern Pacific (Squires 1966). During a November 1956
bottom trawl survey in New England waters, D. lep-
tocerus was much more widely distributed than P.
montagui or P. borealis (Wigley 1960). Dichelopan-
dalus leptoceru^ was also found over a broad depth
range (33-340 m), but was common between 35 and
145 m and at temperatures (in November) of
5°-20°C, whereas P. montagui occurred primarily
between 70 and 135 m and at temperatures of
6°-10°C. Dichelopandalu^ leptocerus was also col-
lected in areas where bottom sediments contained
low, medium, and high quantities of organic matter,
whereas P. montagui appeared to be associated with
sediments with relatively low organic content. Thus,
in several ways, D. leptocerus appears to have less
restricted habitat requirements than P. montagui (or
P. borealis). No detailed biological studies of D. lep-
tocerus have been published.
The Maine Department of Marine Resources con-
ducted an exploratory bottom trawl survey to deter-
mine the abundance and distribution of pandalid
shrimp populations in Penobscot Bay (Figure. 1) dur-
ing 1980-81. During the course of this survey,
biological data were collected from about 10,000
shrimp. The objective of this paper is to describe im-
portant life history characteristics of P. montagui
and D. leptocerus in Penobscot Bay (the Bay); these
include breeding seasons, female sizes and ages at
maturity, sex transition, growth, longevity, and
migratory behavior. Aspects of the life cycle and
reproductive biology of each species were examined
as functions of time of year, depth, and location
within the Bay.
FISHERY BULLETIN: VOL. 83, NO. 3
METHODS
The survey was conducted over the course of a
12-mo period from late November 1980 to early
October 1981. Samples were collected during five
distinct periods of time at 19 different stations
located from Cape Jellison in the northern end of
Penobscot Bay to Mark Island, a distance of about 37
km (23 mi) (Fig. 1). Stations were established at
depths ranging from 12 m (40 ft) to 84 m (280 ft) and
were located in areas of trawlable bottom. Since a
primary objective of the survey was to stimulate
commercial shrimp fishing, no attempt was made to
randomly select station locations, depths, or sam-
pling times. Attempts were made, however, to
return to each station as often as possible so as to
determine the seasonal variation in the relative
abundance of different sexes, reproductive stages,
and size groups of each species at individual locations
over the course of the year. Adjacent, well-defined,
length groups were assumed to represent successive
age-groups.
A total of 45 successful tows (i.e., tows that were
not aborted because of bottom obstructions, damage
to the trawl, or gear malfunction) were made during
the entire survey. Of these, 37 tows which could be
assigned to a specific area, depth range, and sam-
pling period were selected for data analysis. Area 1
was defined as the upper Bay, area 2 as west of
Islesboro, area 3 as south of Islesboro, and area 4 as
east of Islesboro; depth ranges were defined as
shallow (12-25 m), moderate (25-50 m), and deep
(50-85 m) (Table 1). The distributions of sampling ef-
fort between stations by sampling period, area, and
depth range are shown in Table 2. No data were
Table 1.— Definitions of coded sampling periods, areas, and
depth ranges, 1980-81 Penobscot Bay shrimp survey.
Sampling
periods
1
2
3
4
5
Areas
1
2
3
4
Depth
ranges
1
2
3
20 November-2 December 1980
21-29 January 1981
24-31 March 1981
16 July-18 September 1981
5-6 October 1981
Upper Bay: stations 2, 3, 4, 6, 18
West of Islesboro: stations 1, 5, 9, 10, 14
South of Islesboro: stations 7, 8. 12, 15, 16, 17,
19
East of Islesboro: stations 11. 13
12-15 m (shallow)
25-50 m (moderate)
50-85 m (deep)
220
STEVENSON and PIERCE: PANDALUS MONTAGUI AND DICHELOPANDALUS LEPTOCERVS
Figure l.-Map of Penobscot Bay. ME, showing bottom trawl stations visited during 1980-81 survey.
221
FISHERY BULLETIN: VOL. 83, NO. 3
Table 2. — Distribution of sampling effort (number
of tows per station) by sampling period, area, and
depth range, 1980-81 Penobscot Bay shrimp
survey.'
Sampling
period
Area
Depth
Station
1
2
3
4
5
1
2
3
4
1
2
3
1
2
1
6
9
9
3
1
2
2
4
1
1
5
1
1
6
1
1
7
1
1
1
3
3
8
1
1
9
1
2
1
1
10
1
3
5
5
11
1
1
2
1
1
12
1
1
13
1
1
1
15
1
1
16
1
1
1
3
3
17
1
1
18
2
2
2
19
1
1
Totals
9
10
9
6
3
6
17
11
3
6
17
14
'See Table 1 for definitions of coded sampling
periods, areas, and depth ranges.
available from stations 2 and 14. Trawling opera-
tions were limited to the area between Northport
and Islesboro in the summer of 1981, since the only
vessel available at that time was not equipped to
work elsewhere in the Bay.
The trawl used was a semiballoon shrimp try-net
with a 7.6 m (25 ft) headrope and 9.5 m (31 ft) foot-
rope with no rollers; mesh size was 38 mm (IV2 in) in
the body and 31 mm (IV4 in) in the cod end. The
trawl was also equipped with a 12.5 mm (V2 in) liner.
The net was rigged on 1.2 m (4 ft) legs with ark
floats on the headrope and 2/0 chain on the footrope.
The trawl doors were hardwood, 76 x 41 cm (30 x
16 in), with iron bracings and a wide shoe. The net
was fished on a single trawl wire attached to a 30.5
m (100 ft) wire net bridle. All tows lasted 30 min and
were made at speeds varying from 1.5 to 2.5 kn.
Loran bearings were recorded at the beginning and
end of each tow, and depth was recorded either as a
single reading or at the beginning and end of each
tow. Location and depth could not be determined in
the summer since the vessel used then did not have
sonar or navigational equipment. Although three dif-
ferent vessels were used during the course of the
survey, the gear was identical and was fished the
same way during the entire survey.
If catches were small (under 1 kg), the entire catch
was generally brought to the laboratory and frozen
for later analysis; otherwise, the catch was sub-
sampled aboard the vessel. In some cases, large
samples were further subsampled in the laboratory
after they were thawed. Inasmuch as was possible,
all samples and subsamples were randomly selected.
Samples (or subsamples) of 200-900 g were sorted
(after removing extraneous "trash") by species ac-
cording to morphological characteristics described
by Rathbun (1929). Biological data were compiled for
a total of 7,259 D. leptocerus and 2,475 P. montagui;
numbers of P. borealis were inadequate for data
analysis. Each individual shrimp was sexed (male,
female, or transitional) using external morphological
characteristics for the genus Pandalics originally
described by Wollebaek (1908), Berkeley (1930),
Jagersten (1936), and Leloup (1936) and summarized
by Mistakidis (1957). The females were further
grouped as ovigerous or non-ovigerous depending on
whether or not the eggs had "dropped" and were
being carried on the pleopods; the non-ovigerous
females were further subdivided into two groups -
those which had never carried eggs before and those
which had - based on the presence or absence of ster-
nal spines. This characteristic of non-ovigerous
females was originally described by McCrary (1971)
for three pandalid species (Pandalus borealis, P.
goniurus, and P. hypsinotus) in Alaska. Stage I
females were defined as those which had not carried
eggs before and Stage II females as those which had;
there was no way to distinguish between females
which had carried eggs only once before and those
which had carried eggs more than once. Carapace
lengths were measured between the eye socket and
posterior dorsal edge of the carapace and recorded to
the nearest 0.1 mm.
For each species, the numbers and lengths of
shrimp in each biological category (sex, with or
without eggs. Stage I or II) were compiled by sam-
pling period, geographic area, and depth range.
Length frequencies were expressed as numbers of
shrimp per 0.5 mm dorsal carapace length. Since
nearly all of the samples collected in areas 1-3 were
also collected in specific depth ranges (i.e., all 6
samples from area 1 were from shallow water, 16/17
samples from area 2 were from moderate depths,
and all samples from area 3 were from deep water),
length frequencies were presented for appropriate
area/depth combinations. Length-frequency data for
P. montagui collected in October 1981 were not
presented since so few individuals were captured.
RESULTS AND DISCUSSION
Breeding Seasons and
Female Sizes (Ages) at Maturity'*
Nearly all the ovigerous female D. leptocerus were
222
STEVENSON and PIERCE: PANDALUS MONTAGUI AND DICHELOPANDALUS LEPTOCERUS
caught in November-December 1980 (Table 3),
although a few remained in January and March. It
was therefore apparent that most eggs hatched dur-
ing a relatively short period of time in late December
and early January. Although only the larger size
group was carrying eggs (Fig. 2D), the presence of a
were reported for the same populations as late
February through April with peak activity in April.
According to Couture and Trudel (1969b), ovigerous
females were observed in Grand-Rivifere, Quebec,
beginning in July and accounted for the greatest
percentage of the population in October (no samples
Table 3.— Percent total number of male and female Dichelopandalus leptocerus
collected at all locations and depths in Penobscot Bay during five sampling
periods in 1980-81. (Females are categorized by reproductive stage.)
11/20-12/2
1/21-1/29
3/24-3/31
7/16-9/18
10/5-10/6
Sex/Stage
1980
1981
1981
1981
1981
Total
Total males
49.7
65.3
59.4
47.6
53.0
53.2
Females/Stage 1
32.0
33.5
37.8
50.2
45.3
38.8
Females/Stage II
1.4
0.3
1.5
2.2
1.5
1.5
Total
non-ovigerous
females
33.4
33.7
39.3
52.4
46.8
40.2
Ovigerous females
16.8
1.0
1.3
0.0
0.2
6.6
Total females
50.3
34.7
40.6
52.4
47.0
46.8
Total no.
individuals
2,694
729
1,151
1,107
1,577
7,259
few Stage II non-ovigerous females in roughly the
same size range (Fig. 2C) indicated that some
females produced eggs a year earlier as well. It could
not be determined from the samples collected during
this study whether the younger females spawned
earlier or later than the older group. The fact that so
few Stage II females were captured in the Bay at any
time of year indicated that most of the spawning
population was made up of first time spawners.
Ovigerous females were collected at all depths and in
all areas (Tables 4, 5), but made up a greater percent-
age of the catch at moderate depths in area 2.
Nearly all of the ovigerous female P. montagui
were collected in November-December and late
January (Table 6); the fact that 50% of the females in
late January were still ovigerous suggests that eggs
hatched over a more prolonged period then was true
for D. leptocerus, possibly from November at least
through February. Females belonging to two North
Sea P. montagui populations were reported to carry
eggs primarily between November and February
(Mistakidis 1957; Allen 1963), although ovigerous
females were observed from mid-October to April in
the Thames estuary by Mistakidis. Hatching times
*Since no internal sexual characteristics (such as oocyte develop-
ment) were examined in this study, the breeding season was defined
as the period of time when ovigerous females were observed and
sizes (ages) at maturity as the sizes (ages) when females produce
eggs. No comparable information for males (i.e., mating times or
sizes (ages) at maturity) was available. As used in this paper, the
breeding season was, strictly speaking, the period of time between
spawning and hatching when eggs were incubated.
Table 4.— Percent total number of male and female Dichelo-
pandalus leptocerus collected at all depths and times of year
in four areas in Penobscot Bay during 1980-81. (Females are
categorized by reproductive stage.)
Sex/Stage
Area 1
Area 2
Area 3
Area 4
Total
Total males
54.4
49.3
57.4
70.6
53.0
Females/Stage 1
Females/Stage II
Total
42.2
1.0
39.7
1.8
36.7
1.1
26.1
1.1
38.9
1.4
non-ovigerous
females
43.2
41.5
37.8
27.2
40.3
Ovigerous
females
2.4
9.2
4.8
2.2
6.6
Total females
45.6
50.7
42.6
29.4
47.0
Total no.
individuals
1,047
3,626
2,419
92
7,184
Table 5.— Percent total number of male and female Dichelo-
pandalus leptocerus collected in all areas and times of year
by depth range in Penobscot Bay during 1980-81. (Females
are categorized by reproductive stage.)
Sex/Stage
Shallow
(12-25 m)
Moderate
(25-50 m)
Deep
(50-85 m)
Total
Total males
54.4
47.7
80.3
53.3
Females/Stage 1
Females/Stage II
Total
41.5
1.1
40.4
2.0
32.4
0.9
37.6
1.4
non-ovigerous
females
42.6
42.4
33.3
39.0
Ovigerous
females
3.0
9.9
6.4
7.7
Total females
45.6
52.3
39.7
46.7
Total no.
individuals
812
3,015
2,299
6,126
223
FISHERY BULLETIN: VOL. 83, NO. 3
120-
100
80-
60-
40-
2 0-
180-
N0V20
-DEC 2
1980
160-
Males
N = l 33 1
140-
120-
h
100-
— 1
8 0-
H
^
60-
, —
,
40-
U
20-
^ 1 T 1 1 T
^
A
Non- o vige r ou s Females
Stage I
N-863
8 0-
60-
40-
20-
JAN 21-29
1981
Males
N = 476
^
^^ , s ^
E
10
Non -o vige rous Females
Stage II
5
N = 38 1
^^ r^ .
"H r^^
c
80-
6 0-
40-
2 0-
■
8 0-
p_,_^
Ovigerous Females
6 0-
N-4 5 4
J
n
40-
2 0-
•
r^ , ,
^ °
40-
3 0-
f\
Non
-ovigerous
Stage 1
N=24 4
Females
20-
H
10-
r^
^r^
■F=^ 1 r-
F
10 0-
MARCH 24
-31 1981
8 0-
6 0-
pJ
Males
N = 684
4 0-
1—1
20-
^
^
G
-T 1 — — r-
J~L
Non-ovigerous Females
Stage 1
r^^
1 N-436
r u
No n - o vige f ous Females
Stage II
N = l 7 I
Ovigerous Females
N = l 4
J
5 6 7 8 9 10 11 12 13 14 15 16 17
5 6 7 8 9 10 11 12 13 14 15 16 17
CARAPACE LENGTH (mm)
CARAPACE LENGTH (mm)
Figure 2.-Dichelopnvdalus leptoren/s numerical lenjjth-
frequency distributions by sex and reprcKJuctive stafje.
Table 6. — Percent total number of male, transitional, ancj female Pandalus mon-
tagui collectecj at all locations an(j depths in Penobscot Bay during five sampling
periods in 1980-81. (Females are categorized by reproductive stage.)
11/20-12/2
1/21-1/29
3/24-3/31
7/16-9/18
10/5-10/6
Sex/Stage
1980
1981
1981
1981
1981
Total
Total males
73.2
85.2
68.4
37.3
34.3
68.9
Transitionals
0.3
2.5
15.4
5.7
1.5
6.9
Females/Stage 1
7.8
6.1
15.9
50.4
61.2
18.2
Females/Stage II
0.3
0.0
0.0
6.7
3.0
1.2
Total
non-ovigerous
females
8.1
6.1
15.9
57.0
64.2
19.4
Ovigerous females
18.4
6.2
0.4
0.0
0.0
4.8
Total females
26.5
12.3
16.2
57.0
64.2
24.2
Total no.
individuals
332
871
800
405
67
2,475
224
STEVENSON and PIERCE: PANDALUS MONTAGUI AND DICHELOPANDALUS LEPTOCERUS
JULY 16 -SEPT 18 1981
Males
N»52 7
Non -0 viger ouB
Femal»«
Slaga 1
r n
N-5Se
H L
r ' ■ -^ 1 ■
. r
Non-ovlgaroua Females
Stage II
N-24
M
1 OCT 5-6 1981
Males
N-83e
N
Non-ovlgeroua Females
Stage I
N> 7 1 5
-_X
0
-1 — — ^
Non- o vigerous Females
Stage II
N>2 3
—n . r^
—r 1 1 1 r-
a 9 10 11 12 13 14 15 16
CARAPACE LENGTH (mm)
— I »
17 ia
were collected between November and April). A few
females were still carrying eggs the following June.
Hatching began in the winter and continued through
June. Pandalus montagui populations studied in
Penobscot Bay and Grand-Riviere spawned primari-
ly in their second and third years. Females in the
North Sea, on the other hand, were fully mature dur-
ing their first year (Mistakidis 1957; Allen 1963), but
there was no evidence that individual age-groups
spawned more often there than at Grand-Riviere or
in Penobscot Bay.
At least two age-groups of ovigerous P. montagui
were apparent in the winter samples (Fig. 30, G),
whereas only a single age-group of ovigerous D. lep-
tocenis was observed (Fig. 2D). Length-frequency
data suggested that older female P. montagui (age
2 + ) spawned before younger females (age 1); 57% of
the ovigerous females collected in November-
December were > 15 mm CL (Fig. 30), whereas only
30% remained in the same size group in late January
(Fig. 3G). Sample sizes were much too small,
however, to clearly indicate how many spawning
age-groups were present or whether older femaleo
spawned earlier than younger ones. Earlier comple-
tion of spawning by older females was reported by
Mistakidis (1957) in the Thames estuary. In
Penobscot Bay, the relative abundance of ovigerous
females was higher in moderate and deep waters and
in areas 2, 3, and 4 (Tables 5, 6).
The capture of a single 10 mm OL ovigerous
female P. montagui in January (Fig. 3G) indicates
that a few females mature and reproduce during
their first year. This shrimp could have started life as
a female or could have changed sex in the first year
and therefore never functioned sexually as a male.
Mistakidis (1957) reported that some 0 age-group
males in the Thames estuary changed sex and func-
tioned as females during their first year. Some in-
dividuals in both the Thames estuary and North-
umberland began life as females and matured in
their first year (Mistakidis 1957; Allen 1963).
Sex Transition
Unlike most other Pandalid species, the Penobscot
Bay population of D. leptoceru^ was not her-
maphroditic. Not a single transitional individual was
identified in the over 7,000 shrimp which were ex-
amined. Furthermore, males and females recruited
to the > 5 mm OL population in October of their first
year in nearly equal numbers (Fig. 2N, P). The ratio
of males to females for the entire survey period was
53:47 (Table 3). Pandalus montagui, on the other
hand, is a protandric (sequential) hermaphrodite.
Nearly 7% of the 2,475 individuals examined ex-
hibited external morphological characteristics typical
of transitional P. borealis (Allen 1959). The sex ratio
was 69% males to 7% transitionals to 24% females
(Table 6). Although P. montagui is clearly protan-
dric, some individuals in Penobscot Bay either begin
life as females or assume external female character-
istics by late November of their first year.^ These
^Individuals of protandric pandalid shrimp species which begin life
as females are referred ta as primary females; those which change
225
FISHERY BULLETIN: VOL. 83 NO. 3
NOV 20 -DEC 2 1980
Males
N=242
Non-0 vigerous Females
Stage I
N=26
rL
Transitionals
N=22
— 1 T"
1 0-
5 •
_^^
Non- 0 ¥ige r o u s Females
Stage I
N-53 F
r 1 ■=• ■ i
1 0
5 •
Ovtgerous Females
N-54
Figure 3.-Pandalus montagui numerical lenp^th-frequency (iistribu-
tions by sex (including transitionals) anti repnxiuctive stage.
10-
5
30
20-
10-
5 ■
MARCH
24
-'
51 1981
60-
pJ
Males
50-
1 —
N-547
40-
30-
20-
-^
LJ^
1 0-
5
1 '
r 1 1
1 r 1 1 1 r^* r-
H
Transitionals
N-' 23
Transtttonais
N=23
Non- ovigerous Females
Stage I
N = 204
1
2 0-
r^
— 1 Non-0 vigerous Fema
Stage 1
les
10-
5
^
N>I 2 7
1 , 1 •—\ , r— "=1
J
1
, , — .
30-
JULY 16-
SEPT 18 1981
Males
20-
N = 1 S 1
1 0-
'-l
5 •
— t I - — . . . —
— ,__
K
r4on - o vigerous Females
Stage II
N=27
CARAPACE LENGTH (mm)
females were obvious as a distinct size-group in the
November-December length-frequency data at 6-9
mm CL (Fig. 3B). At this time, these females made
up 15% of the newly recruiting 0 age-group. The
relative abundance of 0 age-group females was
considerably higher in the North Sea: 29-37% of
most samples in the Thames (Mistakidis 1957) and
about 50% in Northumberland (Allen 1963). On the
sex In their first year following the repression of male sex
characteristics and never function as males are called secondary
females; and those which function first as males and then change
sex are called hermaphroditic females (Mistakidis 1957). Since no
distinction could be made in this study between the three types of
female P. mxmtagui, we have avoided the use of this termin()lc)gy
altogether and simply distinguish between individuals which re-
mained as males during their first year, those which were females
when they were first captured in November-December of their first
year, and those which apparently changed sex during their first
winter.
other hand, only 11.2% of the age-1 P. montagui col-
lected in May 1965 in Grand-Rivifere were females
(Couture and Trudel 1969b).
Size (Age) at Sex Transition
Transitional P. montagui were collected during all
five sampling periods, but were most abundant in
late March (Table 6) following the end of the
breeding period. Sex transition apf)arently began in
Januar\', peaked in late March, and continued
through the summer and early fall, reaching a
minimum in late November. The rapid decline in the
relative abundance of males after January 1981 and
the accompanying increase in females after March
(Table 6) indicated that shrimp, which functioned as
males in the previous breeding season and became
226
STEVENSON and PIERCE: PANDALUS MONTAGUI AND DICHELOPANDALUS LEPTOCERUS
females prior to the subsequent breeding season,
assumed external female characteristics during the
winter and spring. The appearance of a distinct size-
group of 9-11 mm CL females in late January (Fig.
3F) which was not present 2 mo earlier (Fig. 3B),
suggests that transition was well underway by late
January. The two size-groups of non-ovigerous
females in January and March (Fig. 31) were as-
sumed to belong to the same age-group, the smaller
females being those which did not function as males
in their first year (they may have started life as
females) and the larger females being those which
were still males in November-December (Fig. 3A).
Transitional shrimp made up a larger percentage of
samples collected in moderate and deep waters and
in areas 3 and 4 (Tables 7, 8).
Transition of the younger age-group which was
first captured in November-December (Fig. 3A) was
incomplete since a great many shrimp remained as
males for another entire year before undergoing
Table 7.— Percent total number of male, transitional, and
female Pandalus montagui collected at all depthis and times
of year in four areas in Penobscot Bay during 1980-81.
(Females are categorized by reproductive stage.)
Sex/Stage
Area 1
Area 2
Area 3
Area 4
Total
Total males
82.3
63.4
67.1
77.9
68.1
Transitionals
1.6
3.0
11.5
12.3
7.1
Females/Stage 1
Females/Stage II
Total
14.0
CO
25.4
2.6
16.8
0.4
5.5
0.0
18.8
1.3
non-ovigerous
females
14.0
28.0
17.2
5.5
20.0
Ovigerous
females
2.2
5.7
4.2
4.3
4.7
Total females
16.1
33.6
21.4
9.8
24.8
Total no.
individuals
186
1,037
827
326
2,376
Table 8. — Percent total number of male, transitional, and
female Pandalus montagui collected in all areas and times of
year by deptfi range in Penobscot Bay during 1980-81.
(Females are categorized by reproductive stage.)
Shallow
Moderate
Deep
Sex/Stage
(12-25 m)
(25-50 m)
(50-85 m)
Total
Total males
82.4
61.6
75.3
68.7
Transitionals
1.1
5.8
7.1
5.9
Females/Stage 1
14.2
24.0
10.9
18.1
Females/Stage II
0.0
2.7
0.1
1.5
Total
non-ovigerous
females
14.2
26.6
11.1
19.6
Ovigerous females
2.3
5.9
6.6
5.8
Total females
16.5
32.6
17.6
25.4
Total no.
individuals
176
1,013
732
1,921
transition during their third spring (at age 2). Given
the fact that a few male and transitional shrimp > 15
mm CL were sampled at various times of year, the
possibility that a few individuals do not change sex
until their fourth year (age 3) could not be ruled out.
Even though the transition of younger (age 1)
shrimp in the spring was incomplete, a sizable
number of non-ovigerous Stage I shrimp which com-
pleted transition in their first year were collected in
March (Fig. 3J). These new females were consider-
ably larger (by about 2 mm CL) than their male
counterparts, suggesting that it was the larger,
faster growing, individuals which underwent transi-
tion at age 1. Allen (1963) also reported that the
largest 0 age-group males changed sex first.
Older shrimp which changed sex in their second
year had not yet appeared as females in March (Fig.
3J), suggesting that sex transition in older shrimp
was delayed; it may also have been less rapid, par-
ticularly since growth was considerably reduced
after the first year. Earlier studies of P. montagui in-
dicated that sex transition in two locations in the
North Sea persisted for most or all of the year.
Mistakidis (1957) noted that sex transition occurred
from May to December in the Thames estuary
whereas Allen (1963) collected transitional in-
dividuals throughout the year in Northumberland,
but primarily in June. The timing of minimal sex
transition in Penobscot Bay and Northumberland
was identical (November-December); Allen (1963)
reported that this was when males were sexually ac-
tive. Couture and Trudel (1969b) reported that most
sex transition occurred in October at Grand-Riviere;
a few transitionals were collected in July and August
but none in May and June. Sex transition in the
North Sea, as reported by Mistakidis (1957) and
Allen (1963), was accelerated in comparison with
Penobscot Bay; some individuals changed sex in
their first year, but most did so in their second year.
Ages at sex transition at Grand-Rivifere, on the other
hand, were the same as in Penobscot Bay, i.e., some
in their second year, most in their third year, and
some in their fourth year.
Seasonal Changes in Size (Age) Composition
Two size-groups of male D. leptocerus were ob-
served in the Penobscot Bay during the winter (Fig.
2 A, E, G) and only one in the summer (Fig. 2K);
similarly, female length-frequency distributions in
November-December were bimodal (Fig. 2B), but a
single size-group was dominant in the summer (Fig.
2L). Presumably, most of the older (age 2) males
either die or migrate out of the upper Bay in the
227
FISHERY BULLETIN: VOL. 83 NO. 3
spring since the younger age-group made up the en-
tire population in the summer. Most of the females
apparently spawn once and die after their eggs are
hatched since very few older females were found in
the winter. The presence of a few larger males in
October (Fig. 2N) suggested that a few survive into
their third fall and mate twice (or three times if they
mature during their first year). Further evidence
that most female mortality occurs following hatching
while male mortality is delayed until later in the
spring was indicated by the seasonal changes in
relative abundance of males and females (Table 3):
females decreased from 50 to 35% of the population
between early December and late January while
males decreased more slowly from 65% in January
to 48% in the summer.
Age-2 P. montagui which were either in transition
or were still males in March had mostly become
females by the summer (although a few transitionals
and large males still remained). The single large size-
group of first- maturing Stage I females in the sum-
mer (Fig. 3M) presumably included age-1 females at
a modal length of 13 mm CL and age-2 females at
about 15 mm CL. At the same time, there appeared
to be at least two size-groups of Stage II females in
July-September (Fig. 3N) which had carried eggs the
previous winter (Fig. 3C, G). Ovigerous females cap-
tured in November-December 1980 (Fig. 3C)
presumably included first- time spawners at 12-15
mm CL and one or two groups of repeat spawners at
15-19 mm CL. Excluding the single female at 10
mm, two or three age-groups of ovigerous females
were apparent in January (Fig. 30). As indicated
earlier, the relative abundance of the different age-
groups in November-December and January showed
that repeat spawners may have accounted for a
larger percentage of the ovigerous females earlier in
the winter.
Growth and Longevity
Male and female D. leptocents which hatched in the
winter of 1979-80 reached 8.0-8.5 mm CL by Octo
ber of their first year (Fig. 2N, P) and grew relative-
ly slowly during their first winter; by March they had
reached 7-10 mm CL and the females were slightly
larger than the males (Fig. 20, H). This difference in
size-at-age was also discernible in January (Fig. 2E,
F). Orowth was rapid during the spring of the second
year prior to the beginning of the breeding season:
males increased about 3 mm in carapace length by
the summer while females increased by 4 mm (Fig.
2K, L). The difference in modal lengths between
males and females had increased further by October
(Fig. 2N, P) as growth increased modal carapace
lengths by an additional 0.5-1.0 mm for both sexes.
Orowth between early October and late November
when ovigerous females were first sampled was
negligible, if October 1981 data can be compared
with November 1980 data. During this same short
period of time the relative abundance of the younger,
newly recruited, age-group (males and females) in-
creased dramatically. (A reduction in somatic growth
can be expected at a time of rapid egg development
since female growth ceases once their eggs have
"dropped" and they are unable to molt). This species
reached a maximum observed size of 19 mm CL (not
included in compiled length frequencies), but most in-
dividuals did not exceed 16 mm CL. Unless older in-
dividuals migrate completely out of Penobscot Bay
and were therefore not sampled during this survey,
the maximum lifespan of Z). leptocents in the Bay ap-
pears to be about 2 yr and 9 mo, although the bulk of
the population apparently survives for only 2 yr.
The first evidence of newly recruited 0 age-group
P. montagui was in November-December 1980 (Fig.
3A, B). Individuals which remained as males during
their second year grew from about 7-9 mm CL in
November-December of their first year to 8-10 mm
CL in March (Fig. 3H) and 10-13 mm CL in their sec-
ond summer (Fig. 3K). As was observed for D. lep-
tocerus, the growth rate increased in the spring.
Age-1 shrimp which became females during their
second spring reached 10-12 mm CL in March (Fig.
3J) and 12-15 mm CL in the summer (Fig. 3M). Com-
parison of November-December 1980 and January
1981 data (Fig. 3C, 0) with summer 1981 data sug-
gested that growth of mature females in the fall was
negligible; the same was true for the males. The
maximum observed size was 19.5 mm CL; females as
large as 17-18 mm CL were collected in the winter
(Fig. 3C, 0). These results suggested that P. mon^
tagui in Penobscot Bay normally spend 1-2 yr as
males and as many as 3 yr as females. The maximum
lifespan is probably 4 yr since shrimp that remain
males for 2 yr do not complete sex transition until
their third year and function as females in their third
and fourth years.
Growth at Grand-Rivifere was sufficiently slower
that males there were 2-3 mm CL smaller by the end
of their first year than they were in Penobscot Bay.
This difference in growth could be a result of lower
summer bottom temperatures in the Gulf of St.
Lawrence. A temperature range of - 1°C (in May) to
3°C (in October) was reported in 54 m at Grand-
Rivifere in 1965 (Couture and Trudel 1969a).
Temperatures recorded in lower Penobscot Bay dur-
ing the same months of the year at 40-60 m were
228
STEVENSON and PIERCE: PANDALUS MONTAGUI AND DICHELOPANDALUS LEPTOCERUS
considerably higher, i.e., 3°C west of Islesboro in
May 19706 and 11°-12°C at various stations in the
lower Bay in August 1976''. In Penobscot Bay, P.
montagui were smaller after their first year's growth
than in the two North Sea locations (Mistakidis 1957;
Allen 1963) but attained approximately the same size
by the end of the second year. Males in the Thames
estuary measured 10 mm average CL by November
of their first year, and in Northumberland (at 40-60
m depth) they averaged 9.5 mm CL by October; tran-
sitionals reached 12.5 mm CL by November of their
second year in both locations as compared with
11-13.5 mm CL males of the same age in Penobscot
Bay (Fig. 3A), while females in Northumberland
reached 14.8 mm CL by November of year 2 as com-
pared with 13-15 mm CL at the same age in
Penobscot Bay (Fig. 3C). One-year-old females in
Northumberland averaged 10.8 mm CL in October.
Allen's (1963) explanation for this difference be-
tween male and female lengths-at-age was that
shrimp which mature as females in their first year do
so 3-4 wk after males of the same age-group; since
growth virtually ceases in the fall and winter, the dif-
ference in length attained by the females in the first
year is maintained into the third year of life. In
Penobscot Bay, on the other hand, very few females
mature in their first year; however, if males mature
in their first year (this was not determined) and stop
growing in the fall before the females, Allen's ex-
planation might apply. It seems more likely that sex
transition is a function of size, not age, and that the
faster growing 0 age-group shrimp complete sex
transition in their first year. Another possible ex-
planation for the difference in size of females which
change sex in their second and third years is that
there may be two distinct periods of larval produc-
tion and/or survival. Length-frequency data collected
at two different periods during the winter (Fig. 3C,
G) did suggest that older females may have spawned
earlier than younger females. A 5-yr study of P.
borealis in the Sheepscot River of Maine* failed,
however, to reveal any consistent bimodality in lar-
val production during February-April even though at
least two age-groups of ovigerous females are com-
«Muirhead, C. R., and J. H. Wartha. 1971. Temperature-
salinity observations, Penobscot Bay, Maine, 1970. Open Data
Rep. NOS DR-13, U.S. Dep. Commer., NOAA, Natl. Ocean Surv.,
Off. Mar. Surv. Maps, Oceanogr. Div., Descr. Oceanogr. Sect.,
Rockville, MD.
'Central Maine Power Co., unpublished data, courtesy Richard
Birge, Environmental Studies Department, CMP, August, ME.
*Stickney, A. P. Environmental physiology of northern shrimp,
Pandalus borealis. Maine Dep. Mar. Resour., West Boothbay Har-
bor, ME, Annu. Rep. 1981-82, 15 p.
monly observed in commercial catch samples^. We
contend, therefore, that the most plausible explana-
tion for differences in the sizes of shrimp which
become females in their second and third years is a
difference in growth rates, especially since a similar
difference in size was observed between male and
female D. leptocerus in which sex remains fixed
throughout life.
Pandalus montagui which either began life as
females or became females early in their first year
were smaller than their male counterparts by
November-December of their first year (Fig. 3A, B).
It therefore seems probable that the smaller Stage I
(6.5-8.5 mm CL) females captured in late January
(Fig. 3F) did not grow as rapidly as the larger
females in the same age-group which apparently
completed sex transition in late December and early
January or as shrimp which remained as males for
the entire year (Fig. 3D). These differences in
length-at-age between 0 age-group males and both
groups of females were also evident in late March
(Fig. 3H, J). The accelerated growth rate of 0 age-
group individuals which changed sex during their
first year contrasts with the reported faster growth
of P. montagui in the North Sea and at Grand-
Rivifere which began life as females (Allen 1963;
Couture and Trudel 1969b).
Winter Migration
During November-December 1980, younger male
and non-ovigerous female D. leptocerus were
predominant in shallow water in area 1 (Figs. 4A,
5A) while the older age group predominated in
deeper water (Figs. 4B, C, 5B, C). By late January,
the older females were no longer being caught, and
the older males had disappeared completely from
depths < 50 m (Fig. 4D, E), but accounted for about
50% of the males collected in deep water in area 3
(Fig. 4F). There were older males in areas 2 and 3
(moderate and deep water) in March (Fig. 4G, H).
These results suggested that older male shrimp
migrated down the Bay into deeper water as the
winter progressed and as bottom water tempera-
tures dropped from about 8°C in early December to
1°C in late February and early March in the upper
Bay.i° Their disappearance from the catches.
9Diodati, P., S. H. Clark D. Mclnnes, R. Tichko, and D.
Sampson. 1983. Gulf of Maine northern shrimp stock status
-1983. Northern Shrimp Technical Committee, November 1983, 9
P-
i°Birge, R. P. 1982. Surface and bottom water temperatures,
upper Penobscot Bay, Maine, March 1975 - December 1981. Cen-
tral Maine Power Co., Environmental Studies Department, Report
SI-82-3, 45 p.
229
FISHERY BULLETIN: VOL. 83, NO. 3
50-
40-
3 0-
20-
10-
10 0-
8 0-
6 0-
4 0-
2 0
NOV. 20- DEC 2 1980
n
Area 1
Shallow
N = 325
-1 1 1 1 1 1-"
Area 2
Moderate Depth
N-505
r
— f ■ T r » f ~1 ' r-
40-
Area 3
^
30-
Deep
N-230
^
2 0-
-
10-
^T '— 1 J
■
r ^-HlH ^
- r^T
Area 2
Moderate Depth
N-55
-=^ 1
40
30
20
10-
N0V20-DEC2 1980
8 0-
60
40-
20
Area 2
Moderate Depth
N=385
JAN 21-
29 1981
3 0-
p.
Area 1
20-
1 —
n
Shallow
N=1 1 7
10-
Ln
D
1
f T r r-
20-
Area 3
Deep
1 0-
N = 97 1 — ' L-
r-
J 1 ^
JAN 21-29 1981
—I 1 1-
Area 3
Deep
N-2 7 3
T 1 1 1
Area 2
Moderate Depth
N-52 E
T 1 1 1 I
?n-
Area 3
, — ' Deep
10-
N = 9 1
-
r^
L^ --- ,-
F
1 T — 1
80-
60-
4 0-
2 0-
2 0-
10-
— I 1 ' ' 1 \ 1 ' r~
MARCH 24-31 1981
Area 2
Moderate Depth
N=423
MARCH 24-31 1981
Area 2
Moderate Depth
N=290
2 0-
10-
r^n
Area 3
Deep
N-102
-. F=»— .
H
. » '
r-
-i-F=i-
5 6 7 8 9 1011 12131415 16 17
CARAPACE LENGTH (mm)
CARAPACE LENGTH (mm)
Figure 4. -Male DichelopandaLus ieptoceru.s numerical length-
frequency distributions by area and depth range.
230
STEVENSON and F'lERCE: PANDALUS MONTAGU! AND DICHELOPANDALUS LEPTOCERUS
however, may still have been a result of mortality
rather than migration. The depth-area length-
frequency data also revealed that slightly larger
shrimp of both sexes and age-groups were captured
in deeper water further down the Bay, suggesting
that larger individuals are more likely to migrate
than smaller ones.
Older male P. montagui also migrated down the
Bay into deeper water during the winter: older age-1
males were more abundant than younger 0 age-
group males in areas 2 and 3 (moderate and deep
water, respectively) in November-December 1980
(Fig. 6A, B, C) and by late January nearly all the
older males were in deep water in area 3 (Fig. 6D, E,
F), but were not as abundant as the younger males in
deep water in area 4 (Fig. 6G). There was no clear
evidence that the larger males in either age-group
2 0J
NOV 20- DEC 2 1980
Area 1
~~
Shallow
10-
r^ L-, r
N=10 0
A
^ 11
ZO-
, — =1 — I —
^ r^
n
Area 2
Moderate Depth
IC-
N = 9 1
^ B
1 ■ — 1
40-
30
20
10
Area 2
Moderate Depth
N=255
^^TL
Area 4
Deep
N=ei
■^
1 r1 I n
10 11
12 13 14 15 16 17
CARAPACE LENGTH (mm)
Figure 6. -Male Pandalus montagui numerical length-frequency
distributions by area and depth range.
were more frequent in deeper water and not enough
females were collected during any single sampling
period to permit an analysis of differential distribu-
tion of different age-groups by depth.
Allen (1963) reported an offshore migration of
age-1 males to deeper water in the spring and sum-
mer in Northumberland waters; Couture and Trudel
(1969a) observed the same phenomenon in Grand-
Rivifere in the summer as the temperature exceeded
6°C and reported that it was triggered by the onset
of maturity; earlier maturing males migrated sooner
than later maturing males, indicating that migration
was a function of size, not age. Mistakidis (1957) and
Allen (1963) both reported an offshore migration of
P. montagui females in the fall; Allen, however,
reported that the smaller females stay behind to
spawn in shallow water and that there was no
"massive" return migration in the spring whereas
Mistakidis reported a general offshore fall migration
of females and a return migration in the spring.
Allen (1963) reported that females in Northumber-
land which survived to spawn a third time were only
found in depths > 100 m.
CONCLUSIONS
This study of the life histories of Pandalus mon-
tagui and Dichelopandalus leptocerus in Penobscot
Bay has revealed some notable differences in repro-
ductive characteristics and (apparently) in longevity
between the two species. On the other hand, growth
rates and migratory behavior were similar.
Most importantly, P. montagui is hermaphroditic;
D. leptocerus is not. In 1980-81, some transitional P.
montagui were observed during all five sampling
periods, but were most common in the early spring;
most individuals change sex at the end of their sec-
ond year but some do so during their first year and a
few may not change sex until their third year. Some
individuals apparently begin life as females; 15% of
the 0 age-group which recruited to trawl catches at
5-10 mm CL in November-December 1980 were
females. Ovigerous P. montagui were collected over
a longer time period, owing, at least in part, to the
presence of more age-groups in the spawning popula-
tion. Most D. leptocerus females spawn during their
second year, although a few also spawn in their first
year; ovigerous females were collected primarily in
late November-early December. Pandalus montagui
spend 1-2 yr as males; individuals which undergo sex
transition in their second year may function as
"emales during their second, third, and fourth years
/hile those which change sex in their third year may
only function as females for 2 yr. Judging from the
231
FISHERY BULLETIN: VOL. 83, NO. 3
length-frequency data collected during this study, it
is unlikely that very many P. montagui survive in the
Bay beyond age 4. No D. leptocenis females older
than age 2 were caught in the Bay although some
males remained until their third fall (age, 2 yr and 9
mo). Conclusions concerning longevity were com-
plicated by the fact that larger individuals of both
species migrated down the Bay into deeper water as
the winter progressed and were not captured and by
the difficulty of inferring age from length data for
the larger size-groups, particularly for P. montagui.
Both species were similar with respect to growth
and migratory behavior. Growth decreased with in-
creasing age and was seasonal, i.e., rapid in the
spring and summer of the first year and the spring of
the second year and negligible in the fall and winter.
Males of both species reached 7-9 mm CL at age 1
and 11-13 mmCL at age 2. The data suggested that
early (age 1) transitional P. montagui also grow con-
siderably more rapidly than the remainder of their
age group which undergo sex transition at age 2. The
slowest observed growth rate was for P. montagui
which apparently begin life as females and therefore
never undergo sex transition. For D. leptocerus,
females grow more rapidly than males and differen-
tial growth is a "fixed" sexual attribute. For P. nwn-
tagui, the fact that the faster growing individuals
change sex a year earlier and therefore function as
females for an additional year (assuming that fast-
and slow-growing shrimp have identical lifespans)
means that more rapid growth and early sex transi-
tion increase the reproductive potential of the
population, as long as enough males remain in the
population to mate with the females. Female maturi-
ty is clearly a function of size, not age.
The life cycle of P. montagui in Penobscot Bay was
quite different in several respects from the life cycles
of populations which have been studied in the North
Sea and at Grand-Riviere, Quebec. Pandahis mon-
tagui populations in two locations in the North Sea
(Mistakidis 1957; Allen 1963) appeared to grow more
rapidly in their first year of life than in Penobscot
Bay and were composed of a considerably greater
proportion of early maturing females, many of which
never functioned as males. Growth over the entire
lifespan was considerably more rapid in Penobscot
Bay and the North Sea than at Grand-Riviere
(Couture and Trudel 1 969b), but the relative scarcity
of females which do not function first as males and
the delay of most sex transition until the third year
were common to the Canadian and United States
populations. In addition to a difference in the timing
of maximum sex transition from age 2 (Penobscot
Bay and Grand-Riviere) to age 1 (North Sea), the
seasonal intensity of sex transition was not the same
in three of the populations. Most transitionals were
observed in March in Penobscot Bay, in June in
Northumberland (Allen 1963), and in October at
Grand-Riviere (Couture and Trudel 1969b). Eggs
were carried by females in both North Sea locations
and in Penobscot Bay during the winter (November-
March); at Grand-Riviere most ovigerous females
were observed in October.
In Penobscot Bay and the North Sea, sex transi-
tion tended to follow the end of the breeding season,
whereas in Grand-Riviere, maximum sex transition
coincided with the time when most females were
carrying eggs (unless sex transition was more com-
mon later in the fall when no samples were
collected), suggesting that there was a 12-mo inter-
val between the appearance of external female
characteristics and spawning at Grand-Riviere, and a
6-9 mo interval in Penobscot Bay and Northumber-
land. More rapid growth rates in the latter two loca-
tions would explain the shorter time intervals
between sex transition and spawning. The reproduc-
tive cycle in Grand-Riviere was seemingly con-
tinuous, beginning in July and ending in June
(Couture and Trudel 1969b).
Although an offshore migration of larger male P.
montagui was observed in Penobscot Bay, Grand-
Riviere, and Northumberland, this migration oc-
curred in the winter following the end of the spawn-
ing season in the Bay and in spring and summer,
prior to spawning, in the other two locations. Similar
movements of larger females have been noted in
both North Sea populations in the fall. Unlike the
other migrations, the one observed in Penobscot Bay
was not a spawning migration and may instead have
been a response of older shrimp to declining winter
temperatures in the shallower waters of the upper
Bay. The departure of significant numbers of older
shrimp from the Bay could certainly affect any con-
clusions concerning the size or age structure of
either population and their estimated maximum
lifespans.
ACKNOWLEDGMENTS
The authors wish to acknowledge Frank Spencer,
Director of the Fisheries Technology Division, and
Penn E stab rook. Director of the Bureau of Marine
Development, both of the Maine Department of
Marine Resources (DMR), whose support made this
project possible. Thanks are also due to Mike Brown,
formerly a DMR employee and leader of this project;
to Mike Dunton, the captain of the RV Explorer and
to the late Paul DeRocher, captain of the RV
232
STEVENSON and PIERCE: PANDALUS MONTAGUI AND DICHELOPANDALUS LEPTOCERUS
Challenge; to Curt Crosby for assisting with the field
work; to Margaret Hunter, who supervised the com-
puter analysis of the data; to Pat Hoyt and Vicki
Averill, who typed many copies of the manuscript; to
Patti Millette and Kim Knowlton who drafted and
photographed the figures; to Richard Birge of Cen-
tral Maine Power Company who kindly supplied us
with temperature data for Penobscot Bay; and to
Steve Clark of the Northeast Fisheries Center
Woods Hole Laboratory, National Marine Fisheries
Service, for his constructive review comments.
This research was supported by NOAA Grant NA-
SI AA-D-00035 to the University of Maine and the
University of New Hampshire Sea Grant College
Program and by the Fisheries Technology Division
of the Maine Department of Marine Resources.
LITERATURE CITED
Allen, J. A.
1959. On the biology of Pandalus borealis Kr(?yer, with refer-
ence to a population off the Northumberland coast. J. Mar.
Biol. Assoc. U.K. 38:189-220.
1963. Observations on the biolog>' of Pandalus ymmtagui
[Crustacea: Decapoda]. J. Mar. Biol. Assoc. U.K. 43:
665-682.
Balsiger, J. W.
1981. A review of Pandalid shrimp fisheries in the northern
hemisphere. Proc. Int. Pandalid Shrimp Symp., Univ.
Alaska Sea Grant Rep. 81-3:7-35.
Berkeley, A. A.
1930. The post-embryonic development of the common
Pandalids of British Columbia. Contrib. Can. Biol. Fish.,
New. Ser. 6:79-163.
Couture, R., and R. Trudel.
1969a. Biologie et ecologie de Pandalus mimtag^n Leach
(Decapoda Natantia). I. Distribution et migrations, a Grand-
Riviere (Gaspe), Quebec. Nat. Can. 96:283-299.
1969b. Biologie et ecologie de Pandalus montagui Leach
(Decapoda Natantia). IL Age, croissance et reproduction.
Nat. Can. 96:301-315.
Jagersten, G.
1936. Uber die Geschlechtsverhaltnisse und das Wachstum
bei Pandalus. Ark. Zoo). 28A(20):l-26.
Leloup, E.
1936. VL - Les transformations des gonades et des carac-
t^res sexuels externes chez Pandalus montagui Leach
(D^capode). Bull. Mus. Hist. Nat. Belg. 12(19):l-27.
McCrary, J. A.
1971. Sternal spines as a characteristic for differentiating
between females of some Pandalidae. J. Fish. Res. Board
Can. 28:98-100.
Mistakidis, M. N.
1957. The biology of Pandalus montagui Leach. Fish.
Invest, Minist. Agric, Fish. Food, (G.B.), Ser. II, 21(4),
52 p.
Rathbun, M. J.
1929. Canadian Atlantic fauna. 10. Arthropoda. 10 m. Deca-
poda. Biol. Board Can., Atl. Biol. Stn., St. Andrews, N.B.,
Can., 38 p.
Scattergood, L. W.
1952. The northern shrimp fishery of Maine. Commer. Fish.
Rev. 14(1):1-16.
Simpson, A. C, B. R. Howell, and P. J. Warren.
1970. Synopsis of biological data on the shrimp Pandalus
montagui Leach, 1814. FAO Fish. Rep. 57:1225-1249.
Squires, H. J.
1966. Distribution of decapod Crustacea in the northwest
Atlantic. Ser. Atlas Mar. Environ., Am. Geogr. Soc. Folio
12. 4 p.
1968. Some aspects of adaptation in decapod Crustacea in
the north-west Atlantic. Fish. Res. Board Can. Stud. 1260,
p. 215-223.
Warren, P. J.
1973. The fishery for the pink shrimp Pandalus montagui
in the Wash. Minis. Agric, Fish. Food., Lab. Leafl. (New
Ser.) 28, Suffolk, 46 p. Fisheries Laboratory, Lowestoft,
Engl.
Wigley, R. L.
1960. Note on the distribution of Pandalidae (Crustacea,
Decapoda) in New England waters. Ecolog>' 41:564-570.
Wollebaek, a.
1908. Remarks on decapod crustaceans of the North Atlantic
and the Norwegian fjords. Bergens Mus. Aarb. 12:1-77.
233
I
i
VISUAL THRESHOLD FOR SCHOOLING IN NORTHERN ANCHOVY
ENGRAULIS MORDAX
John Hunter and Ragan Nicholl'
ABSTRACT
The visual threshold fur schooling was determined for two groups of 50 adult northern anchovy in the
laboratory. The index of dispersion and the mean distance to the nearest neighbor were used to measure
changes in schooling as a function of light intensity. The threshold light intensity for schooling, (i x 10" "
Wcm''-(2.6 X 10"'' mc), was estimated to occur at a depth of 30 m on a starlit night and at 38 mduringa
full moon, when the chlorophyll concentration is 0.2 mg Chi a ni"'^. At 2.0 mg Chi a ni"-^ the threshold oc-
curs at a depth of 8 m on a starlit night and at 20 m under full moon light. Sufficient light appears to exist at
night within the upper 10 m for schooling to occur in most of the habiUit of the anchovy. The vertical
distribution of newly spawned anchovy eggs indicated that the maximum depth of spawning may be similar
to the maximum depth of schooling and that the visual threshold for schooling could be used to forecast max-
imum spawning depth in the sea.
Vision plays a primary role in the maintenance of
most fish schools in the sea. Other sense organs, par-
ticularly the lateral line, are important in coor-
dinating movements and spacing of fish within the
school (Pitcher et al. 1976), but it is unlikely that
lateral line sense alone is sufficient for maintaining
the integrity of schools at night in the sea. In fact, a
large number of laboratory studies indicate that if
light is sufficiently reduced, fish no longer maintain
schools (Whitney 1969; Blaxter 1970). Thus the
visual threshold for schooling and the depth of pene-
tration of light probably determine the maximum
depth at which pelagic fishes are able to school at
night in the sea.
Our objective was to determine the visual thresh-
old for schooling in adult northern anchovy,
Engraulis mordax, and to use this information to
forecast the maximum schooling depth for anchovy
at night in the sea. This calculation is of ecological in-
terest because the maximum depth for schooling is
probably also the maximum depth for spawning and
for nocturnal feeding. Anchovy spawn only at night
and visual recognition of other fish is probably as
essential for spawning as it is for schooling. During
what we believe was spawning behavior, several
males rapidly pursued a female over an irregular
path, a tactic probably not possible using senses
other than vision. This is a casual laboratory observa-
tion and requires further documentation, however.
'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La .Jolla, CA
92038.
Northern anchovy feed at night as well as in the day
(Loukashkin 1970; Hunter and Kimbrell 1980). Light
may not be necessary for filter feeding, but it is
essential for particulate feeding, although somewhat
higher light levels may be required for feeding than
for schooling (Hunter 1968). Anchovy migrate
toward the surface at sunset (Mais 1974), and schools
are less frequently detected at night using sonar and
not detected with echo sounders (Smith 1970).
Nevertheless, no doubt exists that schooling con-
tinues at night because the anchovy fisher^' is typi-
cally a night fishery and because profiles of schools
are detectable at night owing to the bioluminescent
disturbances their movements produce (Squire
1978).
METHODS
Apparatus and Laboratory Procedures
Two groups of 50 northern anchovy (group 1,
mean length = 10.5 cm SL; group 2, = 9.8 cm SL)
were maintained in a 4.6 m diameter tank supplied
with running seawater (group 1 , mean temperature
= 16.9°C; group 2, 21.0°C). To simplify photo-
graphic analysis the school of 50 fish was constrained
to a somewhat two dimensional form by maintaining
them in water 45 cm deep. The fish were fed adult
Artemia at the daily time of 1000, and the tank was
cleaned 1 h after feeding.
The tank, which was constructed of blue vinyl, was
located in a light tight rectangular enclosure in which
the walls and ceiling were covered with white vinyl
Manuscript accepted August 1984.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
235
FISHERY BULLETIN: VOL. 83, NO. 3
to diffuse the Jight. Four light sources were equally
spaced around the periphery of the tank; the top of
each being just below the tank rim. Each source con-
sisted of a 30 W tungsten microscope lamp with
reflector enclosed in a tube. On top of the tube were
two color filters; a green acrylic plastic filter (#2414,
Rohm and Haas), and a sealed petri dish containing a
5% CUSO4 solution (by weight). To diffuse the light a
translucent white acrylic filter (#W-2447, Rohm and
Haas) was placed on top of the color filters and light
transmitted by the white filter entered a white opal
glass globe (13 cm diameter) that formed the top of
the source. The lamps were operated for 5 h (10% of
lamp life) before they were used to produce test
levels of irradiance. These sources were used to pro-
duce four test levels of irradiance during a 12-h
night. Additionally, four tungsten 100 W household
lamps (unfiltered) with reflectors were used for the
daytime level of irradiance. These lamps were placed
at regular interv-als around the perimeter of the tank
near the ceiling. Light from these lamps reflected off
the ceiling providing a uniformly diffuse illumination.
The spectrum produced by the four sources (Table 1)
resembles the greenish spectrum tj^jical of anchovy
habitat, but the spectrum used in the day was not dif-
ferent from a standard curve for a tungsten lamp
and consequently contained an unnaturally high pro-
portion of longer wavelength energy. Our term for
the condition when all lamps were off was darkness;
under these conditions light was not detectable by a
dark adapted human observer and the irradiance was
below the sensitivity of a 931 A photomultiplier
which can detect about 5 x lO-*' mc (meter candle).
To record the effect of light on the schools the fish
were photographed from above the tank using a 35
mm automatic camera and flash attachment. The
camera was controlled by a timer, and photographs
were taken at 30-min intervals for 5 h during the
12-h day, at night in darkness, and at night at the
test levels produced by the four sources. Night
photographs were taken during a 5-h period com-
mencing 2 h after the end of the 12-h day. Ten
photographs were usually analyzed at each light level
for each group, but in several tests, 1 or 2 photo-
graphs were not analyzed because not all 50 fish
could be seen.
Two indices of schooling were calculated for each
photograph: an index of dispersion (Pielou 1969), and
the mean distance to the nearest neighbor (Hunter
1966). The dispersion index was calculated by super-
imposing a grid containing 326 quadrats over the
projected image of the tank and counting the number
of fish occurring in each quadrat. The variance mean
ratio (s'^/x) for the number of fish per quadrat was the
index of dispersion. The index was calculated for
each photograph, and an average index was com-
puted for each light treatment (n = 8-10 photo-
graphs). A dispersion index of 1 indicates a random
distribution, whereas higher values indicate aggrega-
tion (Pielou 1969) and imply the existence of school-
ing. Values < 1 imply a uniform distribution over the
grid. The mean distance to the nearest neighbor was
computed for a random subsample of 10 fish in a
photograph. All 50 fish in a photograph were
numbered and the subsample of 10 was selected by
drawing the fish numbers from a table of random
numbers. For each of the 10 fish in the subsample
the distance in centimeters to its nearest neighbor
was measured (distance between heads), a mean
distance calculated for each photograph, and means
Table 1.— Spectral functions used to estimate the depth of occurrence of the
visual threshold for schooling under the various water types and incident irra-
diances including spectral irradiance in the laboratory apparatus, moonlight at
3 m below water surface, starlight at the earth's surface (Munz and McFarland
1977), and the relative sensitivity of the dark adapted anchovy eye (Engraulis
encrasicholus, Protasov 1964).
Wavelengths
Energy per 25 nm interval
(nm)
(W cm")
Relative
sensitivity
Interval
Laboratory
Moonlight
Starlight
Mean
luminaires
luminaires
at 3 m depth
at surface
anchovy eye
400
400-412
3.411 X 10-"
425
413-437
1.346 X 10"
6.109 X lO'"
1.978 X 10"
0.16
450
438-462
3.402 X 10"
6.689 X 10'°
2.418 X 10"
0.53
475
463-487
6.822 X 10 "
6.820 X 10 '°
2.291 X 10 "
0.85
500
488-512
9.631 X 10 "
7.072 X 10-">
2.374 X 10"
1.00
525
513-537
1.069 X 10'°
7.067 X 10'°
2.449 X 10"
0.75
550
538-562
9.618 X 10 "
7.283 X 10 '°
5.125 X 10"
0.42
575
563-587
5.297 X 10 "
6.881 X 10 '°
2.838 X 10"
0.22
600
588-612
'9.494 X 10'^
5.481 X 10'°
3.874 X 10"
0.08
'Wavelength Interval = 588-600 nm.
236
Hl'NTKR and N'lCHOLL: NORTIIKRN ANCHdXV SCIIOOI.INC TIIKKSIIOLD
for each lig-ht treatment. These measurements are
indices of only one characteristic of a fish school, the
tendency of individuals to maintain contact with each
other and thereby remain in a social group. The
polarization of individuals in a school is frequently in-
cluded in definitions of schooling as the cohesive
movements of a school require that fish maintain
relatively constant headings and individual distances
which gives the polarized appearance of moving
schools. This characteristic of fish schools was not
measured in our study, thus the visual threshold we
estimated was one for the maintenance of schooling
in the broadest sense, that is the existence of a group
maintained by visual attraction.
Radiometric Procedures, Calibrations,
and Computations
Radiometric equipment used in this study con-
sisted of an Optronics spectroradiometer (model
714-V) (calibrated against a radiometric standard)
and a photometer (Gamma Model 700). The spectro-
radiometer was used to measure the spectral irra-
diance produced by the sources at full lamp output
but the treatment levels of irradiance were below the
sensitivity of the spectroradiometer. Absolute
measurements of light intensity were made 25 cm
above the water surface (the difference between this
position and within the water would be < 10%). The
light treatments were varied by placing neutral den-
sity filters in each of the light sources; the neutral
density filters were calibrated on an optical bench.
Test levels we used were computed from the filter
factors for the neutral density filters. The photo-
meter was used to check irradiance levels prior to a
test, but we believe the computed values to be more
accurate. Irradiance distribution in the tank was
mapped using the photometer and the treatment
values weighted by tank area so that they represent-
ed the average irradiance 25 cm above water
surface.
Our laboratory estimates of the visual threshold
for schooling were used to calculate the maximum
possible depth of schooling in the sea for various
levels of incident irradiation and water types.
Threshold values in W cm"^ were converted to an-
chovy effective units (W cm-'^^nch. eff.) by weighting
the spectrum in the apparatus by the relative sensi-
tivity of the scotopic curve of the anchovy Engraulis
encrasicholus from an electroretinogram by Pro-
tasov (1964) (Table 1). Two levels of night illumina-
tion were used, full moon at 3 m depth (2.78 x 10 ~^
W cm -2), and starlight at the earth's surface (1.08 x
10" 10 W cm"^) (both measurements from Munz and
McFarland 1977). The depth (meters) in the sea (Z)
at which a given threshold (E,) value occurred was
calculated using the equation of Baker and Smith
(1982):
In
where £■„ is the incident radiation (full moon or star-
light) in anchovy effective units. K, is the wave
length specific attenuation coefficient and is the sum
of coefficients for pure water (K,,), dissolved organic
matter iK,j), and chlorophyll a (K,). Tables of coeffi-
cients, and equations for calculating these attenua-
tion coefficients, are given by Baker and Smith
(1982). In our calculations we assumed that the
dissolved organic matter was constant at 0.7 mg 1 ~ '
which is typical of the anchovy habitat. We calcu-
lated K^ for a range of chlorophyll (Chi) a concentra-
tions ranging from 0.1 to 10 mg Chi a m -^ and at 25
nm intervals from 425 to 600 nm for each Chi a con-
centration. Each K, value for 25 nm increments was
weighted by the appropriate anchovy scotopic
sensitivity, and the average anchovy weighted
^t anch. eff. ^as used in the final calculation of Z.
Many uncertainties and possible biases exist in
such an extrapolation from laboratory- to sea condi-
tions: Cloud cover was not considered nor were
possible effects of bioluminescence; spectral irra-
diance values for full moon and starlight of Munz and
McFarland (1977) may not be representative of con-
ditions in the anchovy habitat although they are
relatively close to those given in photometric units
by Brown (1952); variation in dissolved organic mat-
ter is not considered; the radiance distribution over
360° in the tank probably does not resemble that in
the sea (only downwelling irradiance was considered
here); use of the action spectrum based on an electro-
retinogram of a dark adapted E. encrasicholus eye
instead of one for schooling of E. mordax; and of
course, the usual statistical uncertainties. Despite
these uncertainties and biases we believe our esti-
mates of schooling depth are the most accurate to
date thanks to the models developed by Baker and
Smith (1982).
RESULTS AND DISCUSSION
The schooling threshold based on the index of
dispersion was between 4.8 x 10"^^ and 7.8 x 10" '^
W cm-2 (Fig. 1; Table 2). At the lower value and in
darkness the index of dispersion (s^/x fish per
237
FISHERY BULLETIN: VOL. 83. NO. 3
2.4 -
2.3
1.7 -
1.6
1.5 -
1.4
13
1.2
1.1
1.0
0.9 •-
2xSE
• -Group 1
o- Group 2
ci
SCHOOLING
THRESHOLD
(Geometi
TIC mean) T
1 ir
RANDOM
"Dark" 10"
'2 10"" 10''° 10'^ 10-8 "Daylight"
IRRADIANCE Wcm"^
FiciKK I.-\'isual threshold for schooling in northern anchovy.
Schooling is indicated by the index of dispersion (s^/x)- A ratio of 1
implies no schooling as it indicates a random distribution. Each
point is a mean calculated from 8-10 photographs and bars are ± 2
X standard error of the mean. No error bars are given for one value
(2.34 ± 0.47) because it falls far beyond the rest of the values. Mean
dispersion is shown for four test levels of downwelling irradiance
(log scale), "dark" (below the sensitivity of a 931 A photomultiplier).
and "daylight" (1.496 x 1 0 -■'' W cm " 2) which was the norma! day-
time level of irradiance in the apparatus.
quadrat) did not differ from unity indicating that the
fish were randomly distributed. Hence no schooling
existed at the lower irradiance value and in darkness,
whereas at the higher value the fish were clearly
aggregated. These values delimit a region of about 2
log units of irradiance where one cannot be certain if
schooling occurs or not. The actual threshold for
schooling must fall somewhere in that region, and we
have arbitrarily considered the threshold value to be
the geometric mean irradiance of the above two irra-
diances (6 x 10"^^ W cm"-) thereby reducing the
uncertainty in the threshold value to about 1 log unit.
In subsequent tables and figures we give the upper
and lower bounds of the region as well as the
threshold value, however.
The variance of the dispersion index, a measure of
the variation in school dispersion among photo-
graphs, increased sharply at irradiances above the
threshold indicating a wide variation in the disper-
sion of fish among photographs. This can be expected
because schooling fish react to fright stimuli, feed-
ing, and many other conditions by altering interfish
distances, thereby changing the cohesion or degree
of dispersion of the school (Blaxter and Hunter
1982). At light levels below the visual threshold, fish
are unable to respond socially to such stimuli, hence
the variation among photographs is low.
Mean distance to the nearest neighbor followed
the same pattern as we have described for the index
of dispersion. Values in darkness and at the lower
Table 2.— Mean and standard deviation of the Index of dispersion and
mean distance to the nearest neighbor for various irradiance levels.
Schooling
indices
Mean distance
Dispersion
to nearest
Irradiance
(W cm 2)
ir
(-
dex
5'/X)
neighbor
(cm)
Number
of
Group
X
S
X
S
photographs
1.496 X 10'
("daylight")'
1
1.28
0.29
17.50
3.71
10
1
2
1.52
1.28
0.30
0.11
12.15
24.61
4.10
4.94
10
10
'8.92 X 10'
1
2
1.25
2.34
0.10
0.74
12.19
19.49
2.52
5.50
10
10
M.079 X 10'
1
2
1.17
1.34
0.09
0.27
16.65
21.72
3.86
7.14
10
10
M.777 X 10 '"
1
2
1.07
1.49
0.15
0.21
18.48
18.05
3.86
6.62
9
10
'7.785 X 10 "
1
1.05
0.09
21.87
5.39
8
2
0.99
0.07
30.40
5.14
10
1
1.04
0.12
21.20
4.16
9
Dark'
1
1.04
0.12
19.61
4.83
9
2
0.98
0.07
34.12
6.36
10
'Unfiltered tungsten lamp.
'Filtered lamp - spectrum given In Table 1.
'Below sensitivity of 931A photomultiplier.
238
HINTER an.1 NRHOl.l.: NdRTHKRN ANCHOVY SCIIOOl.INC THRESHOU)
40 r
<- tr
UJ o
O 03
5 X
< O
30
?^Z 20
10
•-Group 1
o-Group 2
:2xSE
•1^
"Dark" 10"
10"
10
10
10"
10"^ "Daylight"
IRRADIANCE W cm-^
Figure 2. - \'isual threshold for schooling in northern anchovy is in-
dicated by changes in the mean distance to nearest neighbor. Each
f)oint is a mean calculated from 8-10 photographs and bars are ± 2
X standard error of the mean. Mean distance to the nearest
neighbor is shown for four test levels of irradiance (log scale), "dark"
(below the sensitivity of a 931 A photomultiplier), and "daylight" ( 1 .5
X 10 ~ ■"• W cm - ") which was the normal daytime level of irradiance
in the apparatus.
type and incident li^ht intensity. An order of mag'ni-
tude decline in incident irradiation can be expected
under the darkest storm clouds (Brown 1952); under
these conditions schooling may not be possible at the
highest chlorophyll concentrations.
It seems appropriate to use these visual thresholds
as estimates of the maximum depth of spawning
because spawning probably also depends upon the
ability of anchovy to see one another. We calculated
the vertical distribution of newly spawned anchovy
eggs (0-4 h old, type "S") using data from the un-
published vertical distribution study of Pommeranz
and Moser (1983). We selected sets of vertical sam-
ples at two stations for which surface Chi a concen-
trations had been measured and then calculated a
mean Chi a concentration for an inshore and offshore
series of net hauls. We then estimated the maximum
depth for schooling assuming that the surface Chi a
was equivalent to an integrated value for the water
column as required by the Baker and Smith 1982
model. Spawning occurred closer to the surface at
the inshore station which had a high Chi a concentra-
irradiance values were not statistically different.
Above the threshold the mean distance to nearest
neighbor was lower than that in darkness indicating
closer spacing among pairs, but no trend with light
intensity seemed to exist above the threshold range
(Fig. 2). For the purpose of estimating a threshold,
however, we believe the index of dispersion is prefer-
able because the criterion for randomness is well
defined and the dispersion index takes into account
all 50 fish, whereas we used only 10 random pairs per
photograph for the nearest neighbor measurements
which reduced its precision.
Our calculations indicate that in water of low
chlorophyll concentration (0.2 mg Chi a m'-^) the
threshold irradiance for schooling occurs at a depth
of 38 m during a full moon and at a depth of 30 m on
a starlit night (Fig. 3). The method of calculation is
described in the Methods section on radiometric pro-
cedures. Light attenuates rapidly as Chi a concentra-
tion increases up to about 2 mg m"'^ total chloro-
phyll; at 2.0 mg Chi a m"'^ the schooling threshold
occurs at a depth of only 8 m on a starlit night and at
20 m under full moonlight. Above 2 mg Chi a m"^
light attenuates more slowly with increasing Chi a
concentration with the threshold at 10 mg Chi a m"'^
falling at 5 m in starlight and at 12 m in full moon-
light. These calculations indicate that sufficient light
exists at night for northern anchovy to school within
the upper 10 m of nearly all habitats under clear
skies, but the maximum possible depth of the school-
ing would be expected to vary greatly with water
Surfacer
10
'g 20
a. 30
LU
Q
40
50
Surface
50 L^
FULL MOON LIGHT
SCHOOLING
NO SCHOOLING
STAR LIGHT
SCHOOLING
0.1 0.5 1.0 1.5 2.0 2.5
Chi a (mgm"3)
3.0 10.0
Figure 3. - Maximum depth of schooling of northern anchovy in
waters of various chlorophyll concentrations (Chi a) under starlight
and full moon. Coefficients used in calculations are in Table 1 and in
Methods section. Darkly shaded area indicates proportion of water
column where no schooling is expected, lightly shaded area indicates
depth range of schooling threshold. Centra! dotted line is the
geometric mean.
239
FISHERY BULLETIN: VOL. 83, NO. 3
tion (1.5 mg m"-^) than at the offshore station which
had a lower concentration (0.24 mg Chi a m"'^). At
the onshore station only 4% of the eggs occurred
below 20 m, whereas at the offshore station 31%
were below 20 m. This difference is particularly
striking because the inshore samples were taken
under a full moon, whereas the moon was in the first
quarter when the offshore station was occupied. At
both stations the predicted maximum depth for
schooling was close to the observed maximum depth
for newly spawned eggs (Fig. 4). We may have
underestimated the depth of schooling for the off-
shore (low Chi a) station as we used a starlight value
of Munz and McFarland (1977) because no data ex-
isted for 1/4 moon. Spawning occurred prior to
moonset since spawning occurs between the time of
1800 and 2400 and moonset varied from about the
time of 2130 to 0200 (19-25 March 1980). In addi-
tion, the offshore station had a deeper mixed layer
(about 35 m) than the inshore station (about 10 m)
and vertical distribution of anchovy eggs and larvae
also may be affected by the depth of the mixed layer
(Ahlstrom 1959). Regardless of these uncertainties,
these data indicate that underwater visibility may
set the maximum depth for spawning of anchovy.
although other factors, such as low temperature,
might constitute an additional barrier to spawning
schools. Thus fish visual thresholds may be a conve-
nient way to establish a general function for esti-
mating the maximum depth of spawning for anchovy
and perhaps other pelagic spawning clupeoids in all
habitats. Such a general function, that could account
for much of the variation in the maximum depth of
eggs, could be quite useful in three dimensional
models of larval transport or predation. A spawning-
depth, water-type function based on visual
thresholds seems particularly attractive owing to the
considerable cost of accurately measuring the ver-
tical distribution of eggs and larvae even in a single
habitat let alone the cost for estimating it for all
possible spawning habitats of the population.
To compare the northern anchovy schooling
threshold to literature values we converted our
radiometric measurements to lux or meter candles
(mc), by weighting the spectral irradiance in the
apparatus by the human photopic curve, as the
literature values are largely in photometric units (see
reviews by Whitney 1969 and Blaxter 1970). The
visual threshold for anchovy schooling (2.6 x 10^^
mc, Table 3) is about an order of magnitude higher
Surfacer
10
^ 20
E
t 30
UJ
Q
40
50
1.5 mg Chi a m 3
FULL MOON
SCHOOLING
THRESHOLD
0.24 mg Chi a m"3
FIRST 1/4 MOON
^
SCHOOLING
J
THRESHOLD
NO SCHOOLING
' ' ' ' ' ' ' ' '
0 20 40 60 80
NO SCHOOLING
I I ' I
0 20 40 60
PERCENT OF NEWLY SPAWNED EGGS
^ Depth of mixed layer
Figure 4. -Comparisons of the estimated depths of schooling of northern anchov^' and
the observed depths of spawning. Estimated depth of schooling calculated from visual
threshold estimates (W cm-2^^^|^ ^^^^^ an assumed dissolved organic matter of 0.7 mg
1 ~ ', and the average Chi a concentration and moon phase at the station (1/4 moon
phase assumed to be equivalent to starlight) using the model of Baker and Smith (1982).
Observed spawning depths at the two stations are indicated by a frequency histogram
for newly spawned anchovy eggs where the y axis indicates the depth stratum of the
plankton tow and the x axis indicates the percentage of newly spawned eggs taken at
each of the 10 m vertically stratified tows. Data are from Pommeranz and Moser (1980)
atifl are for the total number of newly spawned eggs taken over a 4-8 d interval.
240
HUNTEK and NICHOLL: NORTHERN ANCHOVV SCHOOl.INC THRESHOLD
Table 3. — Upper and lower bound and geometric mean for the
visual threshold for schooling of adult northern anchovy,
Engraulis mordax, in the various energy units.
Energy units
Schooling'
No
schooling^
Geometric
mean^
7.785 X 10 " 6.051 x 10
Radiometric
(W cm ') 4.777 x 10
Anchovy effective'
(W cm 'anch. eff.) 3.079 x 10 '° 5.018 x 10 '^ 3.900 x 10 "
Photometric* (mc) 2.048 x 10' 3.337 x 10' 2.594 x 10'
'Lowest irradiance level at which schooling occurred.
'Highest irradiance level at which anchovy failed to school.
'Geometric mean of the irradiance at the upper and lower
bounds of the threshold.
'Weighted by ERG action spectra for Engraulis encrasicholus
dark adapted retina (413-612 nm) (Protasov 1964).
^Weighted by the 1964 human photopic response (413-600 nm).
than that for jack mackerel (3.5 x lO"'' mc, Hunter
1968), a species associated with anchovy in the
California Current. Visual thresholds for schooling in
fishes range from about 1 x 10"-^tol x 10"' mc
with about 90% (14/16) of the literature values being
higher than anchovy (Blaxter 1970). We do not at-
tach much importance to such specific differences
because criteria for schooling differ widely and radio-
metric procedures in the older studies were primitive
by today's standard. We suspect the threshold for
jack mackerel may have been lower than the north-
ern anchovy because of use of a uniform and highly
reflective background in the apparatus and the use of
photometric brightness as a unit of measurement. In
our work the brightness to the sides and below was
much lower than the downwelling irradiation
whereas this was not the case in the jack mackerel
experiment.
ACKNOWLEDGMENTS
We thank Mike Sokol (Southampton College, NY)
for constructing the apparatus and for conducting
some of the experiments and Sandor Kaupp (Univer-
sity of California at San Diego) who provided advice
and assistance throughout the study. We also thank
Tilman Pommeranz and Geoffrey Moser for permit-
ting us to use their unpublished data on vertical
distribution of anchovy eggs, and Paul Smith, Tilman
Pommeranz, Roger Hewitt, and J. H. S. Blaxter for
reviewing the manuscript.
LITERATURE CITED
Ahlstrom, E. H.
1959. Vertical distribution of pelagic fish eggs and larvae off
California and Baja California. U.S. Fish Wildl. Serv., Fish.
Bull., 60:107-146.
Baker, K. S.. anjd R. C. Smith.
1982. Bio-optical classification and model of natural waters.
2. Limnol. Oceanogr. 27:500-509.
Blaxter, J. H. S.
1970. 2. Light 2.3 Animals 2.32 Fishes. In 0. Kinne (editor).
Marine Ecology, Vol. 1, Part 1, p. 213-320. Wiley-Inter-
science, Lond.
Blaxter, J. H. S., and J. R. Hunter.
1982. The biology of clupeoid fishes. Adv. Mar. Biol. 20:1-
223.
Brown, D. R. E.
1952. Natural illumination charts. U.S. Navy Bur. Ships Pro-
ject NS 714-100, Rep. No. 374-1, Wash., D.C.. 11 p.
Hunter, J. R.
1966. Procedure for analysis of schooling behavior. .J. Fish.
Res. Board Can. 23:547-562.
1968. Effects of light on schooling and feeding of jack mack-
erel, Trachurus symmetricus. J. Fish. Res. Board Can.
25:393-407.
Hunter, J. R., and C. A. Kimbrell
1980. Egg cannibalism in the northern anchovy, Enffraulij^
mordax. Fish. Bull.. U.S. 78:811-816.
Loukashkin, A. S.
1970. On the diet and feeding behavior of the northern
anchovy, Engraulis moi-dux (Girard). Proc. Calif. Acad. Sci.,
Ser. 4, 37:419-458.
Mais, K. F.
1974. Pelagic fish surveys in the California Current. Calif.
Dep. Fish Game, Fish Bull. 162, 79 p.
Munz, F. W., and W. N. McFarland.
1977. Evolutionary adaptation of fishes to the photic environ-
ment. In F. Crescitelli (editor). The visual system in verte-
brates. Vol. 7 (Part 5), p. 193-275. Handb. Sens. Physiol.
PlELOU, E. C.
1969. An introduction to mathematical ecology. Wiley-
Interscience, N.Y., 286 p.
Pitcher, T. J., B. L. Partridge, and C. S. Wardle.
1976. A blind fish can school. Science 194:963-965.
Pommeranz, T., and H. G. Moser.
1983. Vertical distribution study R/V Ellen B. Scripps March
19-April 4, 1980. Admin. Rep. LJ-83-01, 368 p.
Protasov, V. R.
1964. Some features of the vision of fishes. [In Russ.] A. N.
Severtsov Inst. Anim. Morphol., Acad. Sci. U.S.S.R., p. 29-
48. Marine Laboratory, Aberdeen, U.K., Transl. No. 949.
241
FISHERY BULLETIN: VOL. 83. NO. 3
Smith, P. E. Squire, J. L., Jr.
1970. The horizontal dimensions and abundance offish schools 1978. Northern anchovy school shapes as related to problems
in the upper mixed layer as measured by sonar. In G. B. in school size estimation. Fish. Bull., U.S. 76:443-448.
Farquhar (editor). Proceedings on biological sound scattering Whitney, R. R.
in the ocean, p. 563-600. MC Rep. 005, Maury Cent. Ocean 1969. Schooling of fishes relative to available light. Trans.
Sci., Dep. Navy, Wash., D.C. Am. Fish. Soc. 98:497-504.
!
242
DISTRIBUTIONAL PATTERNS OF FISHES CAPTURED ABOARD
COMMERCIAL PASSENGER FISHING VESSELS
ALONG THE NORTHERN CHANNEL ISLANDS, CALIFORNIA
Milton S. Love.i William Westphal,' and Robson A. Collins^
ABSTRACT
We surveyed fishes taken aboard commercial passenger fishing vessels alon^ the four northern Channel
Islands (San Miguel, Santa Rosa, Santa Cru?, and Anacapa) within the Southern California Bight. P'ourteen
species declined in abundance along the Northern Channel Island chain. Colder water forms decreased to
the east, while temperate species declined to the west. In the shallowest depth interval (0-36 m). the mean
lengths of four rockfish species increased toward the west. In general, the size of these four species also in-
creased with depth. We believe these phenomena are linked to the differences in water temperature be-
tween the islands- with cold, California Current water dominant in the west, and warmer Southern Califor-
nia Bight water entrained in the east.
The mainland coast of California is distinguished by
two faunal provinces: A warm-temperate Californian
Province lies south of Point Conception and a cold-
temperate Oregonian Province exists to the north
(Seapy and Littler 1980). In shallow waters, the fish
fauna of the Californian Province is a mixture of
eurythermic temperate and subtropical species,
while the Oregonian Province is predominantly a
colder temperate region, with few subtropical
species present.
Recent studies examining the distributional pat-
terns of marine intertidal invertebrates (Littler
1980; Seapy and Littler 1980), algae (Murray et al.
1980), and seabirds (Hunt et al. 1980) around south-
em California islands imply there is a replication of
these two mainland faunal provinces along the 88
km, east-west lying, northern Channel Islands (San
Miguel, Santa Rosa, Santa Cruz, Anacapa) (Fig. 1).
Oregonian Province species dominate the western
end of the chain, while the fauna of the eastern end is
more Californian.
There is little published on the biogeography of
fishes around the northern Channel Islands. Ebeling
et al. (1980a, b) examined the fish populations of
Santa Cruz Island kelp beds, and Hubbs (1967, 1974)
stated that the fish communities of San Miguel were
closely related to those of central California, while
about Santa Cruz fish were typical of southern Cali-
iVANTONA Research Group, Moore Laboratory of Zoology,
Occidental College, Los Angeles, CA 9004 L
^Marine Resources Branch, California Department of Fish and
Game, 1301 W. 12th, Long Beach, CA 90813.
fornia. No other work has been published on this
topic.
In this paper, we describe one aspect of the north-
ern Channel Islands' fish fauna, utilizing data
gathered by the California Department of Fish and
Game in their Commercial Passenger Fishing Vessel
creel census. This census (fully described in Methods)
counted, measured, and noted the location and depth
of capture of fishes taken by hook and line on sport-
fishing passenger vessels in southern California.
Data from this study could not give an unbiased
estimate of species composition. Most angling in-
volved fishing with live bait (primarily northern an-
chovies, Engraulis mordax) or with lures simulating
fishes, and angling techniques were similar along the
island chain. Thus, the sample was biased toward
relatively large-mouthed, piscivorous species.
However, the purpose of this study was to ascertain
distributional patterns of whatever species were
taken by these methods, rather than attempting to
describe entire fish communities.
METHODS
Fishes taken aboard commercial passenger fishing
vessels (CPFV) were sampled by the senior author
and by California Department of Fish and Game per-
sonnel from April 1975 to December 1978. The sam-
pling units (trips) were chosen randomly, and the
population sampled consisted of all regularly sched-
uled trips by CPFV's operating south of Point Con-
ception to the Mexican border.
The sampler assigned to each boat boarded the
Manuscript accepted August 1984.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
243
FISHERY BULLETIN: VOL. 83, NO. 3
SANTA. BARBARA
Figure 1 . - Location and block numbers of sampling sites about the northern Channel Islands, C A.
boat at the beginning of the trip and remained
aboard, measuring and identifying all fish caught by
the passengers, until the boat returned to dock. A
particular effort was made to measure every fish
landed, even those returned alive to the water
because of undesirability or in compliance with bag
or size limit regulations. Also noted were the number
of anglers aboard the vessel, the hours of fishing, and
the location and depth of fishing effort.
Each fish was placed on a plastic measuring sheet
held in a two-sided aluminum frame and the length
marked. Total length (tip of snout to tip of depressed
caudal fin) was recorded for all fish except members
of the jack (Carangidae) and mackerel (Scombridae)
families, from which fork length was taken.
A portion of the caudal fin was clipped from each
fish measured so that the fish could be recognized
later. When fish were brought aboard too rapidly for
all to be measured, samplers gave immediate priority
to those being returned to the water and measured
the remaining fish at the end of fishing or during a
break in activity. When samplers were uncertain of
the identification of a fish, they retained it for
positive identification. After completing a trip, the
samplers tallied and recorded by species the data col-
lected. Individual fish lengths were measured on the
plastic sheet with a meter stick.
The California Department of Fish and Game has
divided marine waters off California into numbered
blocks. For this study, we utilized data from block
numbers 684-690 and 707-712 (Fig. 1). Care was
taken to remove data from mainland fishing sites in
block number 684. Block 710 was Santa Rosa Island
alone.
We measured fish abundances by catch per unit
effort, which was defined as number of fish taken per
angler hours (where angler hours = number of
anglers x number of hours fished).
RESULTS
One hundred and nineteen trips were made, and
the catches from 3,712 anglers were sampled. A
total of 23,089 fishes of 78 species were tallied, of
which 49 are listed in Table 1. Rockfishes (particu-
larly bocaccio, Sebastes paucispinis; blue rockfish, S.
mystimcs; and olive rockfish, 5. serranoides) and
kelp bass, Paralabrax clathratus, were numerically
dominant. Among the 20 most abundant species,
only 4 {Paralabrajc clathratus; chub mackerel. Scom-
ber japonictts; lingcod, Ophiodon elongatus; ocean
whitefish, Caulolatiliis princeps) were not rock-
fishes.
We stratified our data by depth (36 m intervals).
244
LOVE ET AL.: DISTRIBUTIONAL PA'ITKRNS OF KISHKS
Table 1.— Partial list of fishes taken aboard commer-
cial passenger fishing vessels during sampling from
April 1975 to December 1978 around the northern
Channel Islands. Only those species where 10 or more
individuals were tal<en are listed.
Sebastes paucispinis
3,183
Sebastes mystinus
3,074
Paralabrax clathratus
2,985
Sebastes serranoldes
2,632
Sebastes goodei
1,619
Sebastes atrovirens
1.509
Sebastes mlniatus
1,119
Sebastes caurinus
1,069
Scomber japonicus
671
Sebastes chlorostichus
632
Sebastes rufus
491
Sebastes carnatus
409
Sebastes entomelas
372
Sebastes constellatus
332
Ophoidon elongatus
304
Sebastes rosaceus
296
Sebastes ovalis
235
Caulolatllus prlnceps
215
Sebastes levis
197
Sebastes elongatus
195
Sebastes auriculatus
156
Sebastes rosenblatti
148
Semicossyphus putcher
142
Sebastes rubrlvinctus
121
Sebastes eos
120
Sebastes hopkinsi
105
Sebastes chrysomelas
102
Scorpaena guttata
60
Sebastes serrlceps
54
Medialuna californiensis
49
Sebastes pinniger
46
Sebastes rastrelliger
43
Genyonemus lineatus
36
Sarda chiliensis
33
Eopsetta jordani
32
Sebastes gilli
21
Sphyraena argentea
20
CItharlchthys sordidus
19
Scorpaenichthys marmoratus
19
Trachurus symmetricus
19
Sebastes simulator
18
Chromis punctipinnis
17
Prionace glauca
17
Serial a lalandei
17
Sebastes ensifer
15
Seriphus politus
15
Sebastes nebulosus
12
Paralichthys californicus
10
Sebastes ruberrimus
10
As virtually all fishing effort in waters deeper than
72 m was carried out in the eastern part of the chain,
no analyses were conducted of catches in these
depths. Most species' abundance trends occurred in
the shallowest (0-36 m) depth interval. No samples in
0-36 m were taken in blocks 688, 689, and 709, and
none in 37-72 m in blocks 690, 709, 720, 411, and
712.
Fourteen species (Table 2) decreased in abundance
along the island chain in 0-36 m (Table 3, Kolmo-
gorov-Smirnov goodness of fit test). Of these, eight
species {Ophiodon elongatics; Paralabrax clathratus;
Pacific bonito, Sarda chiliensis; Scomber japonicus;
China rockfish, Sebastes nebulosus; yellowtail,
Seriola lalandei; Pacific barracuda, Sphyraenxi
argentea; jack mackerel, Trachurus symmetricus)
were absent around either the extreme eastern or
western end of the chain. The abundance of seven
species {Paralabrax: clathratus, Sarda chiliensis,
Scomber japonicus, Scorpa£na. guttata, Seriola
lalandei, Sphyraena argentea, Trachurus symmetri-
cus) decreased toward the west and seven {Ophiodon
elongatus; copper rockfish, Sebastes caurinus; S.
miniatus; S. mystinus; S. nebulosus; S. paucispinis;
S. serranoides) decreased toward the east.
The catch per unit effort (CPUE) of six species
{Ophiodon elongatus, Sebastes caurinus, S. miniatus,
S. mystinus, S. paucispinis, S. serranoides) increas-
ed in the next (37-72 m) depth interval (Table 4). The
largest increases occurred around Anacapa (blocks
684, 707) and the eastern end of Santa Cruz (685,
708). In most instances, catches increased by a factor
of 10 or more in these four blocks. The CPUE of
three species {Sebastes miniatus, S. serranoides, and
S. paucispinis) were over 100 x as great in several
blocks.
There was a cline in the mean lengths of four
species {Sebastes caurinus, S. mystinus, S. paucispi-
nis, S. serranoides) in the shallowest depth interval
along the island chain (Fig. 2). All four species were
largest in the shallow waters of the more westerly
islands, particularly San Miguel.
We compared mean lengths of each species be-
tween blocks within the 0-36 m and 37-75 m depth
intervals using the Student-Newman-Keuls multiple
range test (Sokal and Rohlf 1969). In the shallowest
interval, Sebastes caurinus, S. mystinus, and S. ser-
ranoides were largest off San Miguel, while S.
paucispinis lengths were greatest at San Miguel and
Santa Rosa. Two groupings, San Miguel-Santa Rosa
and Santa Cruz-Anacapa, were evident in three
species {Sebastes mystinus, S. paucispinis, S. ser-
ranoides) as mean lengths of these tended to form
somewhat discrete units. For Sebastes caurinus, San
Miguel, Santa Rosa, and the west end of Santa Cruz
formed one entity - eastern Santa Cruz and Anacapa
another.
For these four species, mean lengths were, in most
instances, greater in each block in deeper (37-75 m)
waters. Though some of the groupings of 0-36 m ex-
isted, there was some breakdown of this pattern. In
Sebastes paucispinis, for instance, the mean lengths
of Santa Rosa (block 688) and Anacapa (707) fish
were similar, though they were different in 0-36 m.
245
FISHERY BULLETIN; VOL. 83, NO. 3
Table 2. — Catch per unit effort x 100, of 14 species taken about the northern Channel Islands in 0-36 m.
Block numbers are arranged approxinnately west to east. The unit of effort is number of fish taken per
angler hours (where angler hours = number of anglers x number of hours fished), tr = <0.01.
Blocks:
690
712
711
710
687
686
685
708
Ophlodon elongatus
Paralabrax clathratus
Sarda chlliensis
Scomber japonicus
Scorpaena guttata
Sebastes caurinus
Sebastes minlatus
Sebastes mystlnus
Sebastes nebulosus
Sebastes paucispinis
Sebastes serranoldes
Seriola lalandel
Sphyraena argentea
Trachurus symmetricus
684 707
1.1
0.80
0.41
0.23
0.33
0.02
0.03
0.03
tr
0.09
0.0
3.62
7.10
0.78
2.65
31.85
2.97
68.33
2.11
22.10
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.06
0.0
0.02
0.0
0.0
0.97
0.52
0.0
0.21
15.00
0.43
16.88
0.01
0.0
0.0
0.07
0.0
0.0
0.04
0.03
0.05
1.17
2.84
7.63
29.68
1.19
1.31
1.45
0.34
0.53
0.16
0.26
2.92
1.30
0.31
1.26
0.0
0.0
0.04
0.01
tr
0.86
9.70
17.01
8.85
16.05
3.06
7.61
3.00
1.02
0.21
8.51
2.08
2.07
0.36
0.86
0.0
0.0
0.06
0.0
0.03
0.82
0.06
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
21.31
42.72
16.09
0.69
1.56
3.46
0.41
0.63
0.19
0.86
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.92
0.0
0.0
0.0
0.0
0.14
0.0
0.0
0.0
tr
tr
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.03
0.0
I
k.
\
14* 15* «• 17'
1 »»I CONCEPTION^
n
"*
**
1— 1__ 1
i
1^
X
n*
I.
SANTA BARBABA
V
""Tt^ ""V^
V
«v.,
/^
\.
Sk
\
^y
V
^^
f
^
s
^ "" ~~~ -~~- -. ^"^K
\
7 ^^^ 5^^-^
7 "■ 'N
\
\ A
\ \ r-^K
\ A Z ^
V
\ ' ^
^-kj
\ ^-^
z ^—
r— — ^
W / jjj — r^
^
'
'"■^'^^li MB^ -^r^^ i ^
^^^ ^^r T 1 ^
\^^ / 4r-Ci*--<r^
w.
^^ "^V- ^~*^ ^
\
L SANTA ROSA 1
y
■^^~ ^^^tf^^jrf ^
V «
^1 * *
\
X
^m ' —
^4
\
^
\ __
\
s» ^
^__ __ _
L
y
^ -i- ^
^1. ^- ::^ " ~~-\
"--.
^^ -i::-"^ ^-i::^
s _ :::^ ^^
N
\ : :^
\
:i y
N
^
■^^
Figure 2. -Mean lengths of four species in two depth intervals (0-36 m and 36-76 m) captured along the northern Channel Islands. Dots
represent means; bars represent 95% confidence intervals.
246
LOVE ET AL.: DISTRIBUTIONAL PATTERNS OF FISHES
Table 3. — Fourteen species demon-
strating significant catch per unit effort
trends (Koimogorov-Smirnov goodness of
fit test) along the northern Channel Islands
in 0-36 m.
Ophiodon elongatus
Paralabrax clathratus
Sarda chlliensis
Scomber japonicus
Scorpaena guttata
Sebastes caurinus
Sebastes miniatus
Sebastes mystlnus
Sebastes nebulosus
Sebastes paucispin/s
Sebastes serranoides
Seriola lalandei
Sphyraena argentea
Trachurus symmetricus
1.64
0.009
1.89
0.002
2.72
< 0.001
1.72
0.002
2.39
< 0.001
2.24
< 0.001
1.57
0.014
2.10
< 0.001
2.69
< 0.001
1.49
0.024
1.97
0.001
2.52
< 0.001
1.92
0.001
2.43
< 0.001
proximity to Point Conception and to the California
Current (Reid et al. 1958; Neushul et al. 1967;
Kolpack 1971; Seapy and Littler 1980). At Point
Conception, as the land extends eastward, the cold
California Current continues flowing southward. As
it flows offshore, the eastern edge surrounds San
Miguel Island and some water spills into the Santa
Barbara Channel, flowing along the northern sides of
Santa Rosa and Santa Cruz Islands (slowly warming
as it travels). Much of the California Current con-
tinues to flow southeastward and is later entrained in
a slow-moving and warm counterclockwise eddy
(Southern California Eddy) within the Southern
California Bight. Areas influenced by this eddy, such
as Anacapa Island, the southern sides of Santa Rosa
and Santa Cruz Islands, and, to a certain extent, the
Table 4.— Comparison of catch per unit effort x 100 of six species between two depth intervals (0-36 m and 37-72 m).
Block numbers are arranged approximately west to east.
Blocks
Depth
690
688
712
711
710
687 686
685
708
684
707
Ophiodon elongatus
0-36
37-72
Sebastes caurinus
0-36
37-72
Sebastes miniatus
0-36
37-72
Sebastes mystinus
0-36
37-72
Sebastes paucispinis
0-36
37-72
Sebastes serranoides
0-36
37-72
nr = <0.01.
1.1
0.80 0.41 0.23
100.02
2.84 —
7.63 29.68
33.28
2.92
1.30 0.31
1.19
1.26
— 12.41 —
9.70 —
17.01 8.85 16.05
17.08
2.08 -
2.07 0.36
0.86
— 18.21 —
21.31
42.72 16.09 0.69
4.11 —
0.33
0.02
0.03
0.03
tr'
0.09
1.14
—
0.08
1.53
4.08
0.38
1.31
1.45
0.34
0.53
0.16
0.26
6.41
—
0.92
8.36
7.68
3.61
0.0
0.0
0.04
0.01
tr'
0.86
6.25
—
0.29
2.04
3.61
0.68
3.06
7.61
3.00
1.02
0.21
8.51
12.77
—
5.28
16.92
57.21
7.41
0.0
0.0
0.06
0.0
0.03
0.82
13.81
—
0.54
10.21
22.81
10.25
1.56
3.46
0.41
0.63
0.19
0.86
1.63
—
2.89
2.91
22.81
0.28
Similarly, the distinctions between mean lengths of
S. serranoides in 0-36 m off Santa Rosa versus
Anacapa were not evident in 37-75 m. There was no
difference in S. mystinus mean lengths between
Santa Rosa, Santa Cruz, and Anacapa.
DISCUSSION
Temperature Regime
Previous studies indicate that temperature plays a
major role in the community structure of inverte-
brates and algae along the northern Channel Islands
(Littler 1980; Murray et al. 1980; Seapy and Littler
1980), and water temperature was correlated with
patterns we observed in fish species abundances and
size frequencies. Water temperatures surrounding
these islands are strongly influenced by their relative
northern sides of Santa Rosa and Santa Cruz, are
warmer than areas bathed by the California Current
alone. Surface water temperature differences may
be as much as 12° C between San Miguel and
Anacapa, and 8°C between the west end of Santa
Cruz and Anacapa (Hubbs 1967).
Figure 3 exemplifies this condition. It represents
the mean of surface temperatures observed by the
NOAA-7 satellite on 8 d throughout 198P. Though
1981 was a relatively warm water year within the
Southern California Bight, the influence of the
California Current is plain around San Miguel, much
of Santa Rosa, and the western end of Santa Cruz
Islands. Warm water from southern California
bathes southern and eastern Santa Cruz and the
^Data taken from observations on 29 January, 15 February, 22
March, 16 May, 4 August, 30 September, 11 October, and 25
November 1982.
247
FISHERY BULLETIN: VOL. 83. NO. 3
(0-36m)
550
500
450
400
350-
300
250
200
SEBASTES PAUCISPINIS
550r
500 4
450-
400
350-
300
250-
200
690 7-I2 710 6^ 6^
BLOCK NUMBER
(37-75m)
\ I
6te 667 665 664 767
BLOCK NUMBER
i
E
E
X
»-
z
LU
-1
-J
<
o
400r
350
300
250
\ \ I
♦
SEBASTES CAURINUS
400r
350-
300-
f 250-
6§?rflr7trTlcrs67^fe7te^4
BLOCK NUMBER
\
♦ I
668 6^7 6^5 768 767
BLOCK NUMBER
500r
450
400
350
300-
250
I
SEBASTES SERRANOIDES
500r
450 t
400- }
350
I 4 300
250
690 712 711 710 6^7 6^ 6^ 767 6^
♦ I
6^6^6^7 6^5 765 6^
350r ♦
300
250
BLOCK NUMBER
♦ ♦
BLOCK NUMBER
SEBASTES MYSTINUS
350r
^ 300
\ ♦
250
690 712 711 710 687 686 685 768 6^4 767
♦
♦
♦ ♦ f
BLOCK NUMBER
688 667 6^5 766 6^4 767
BLOCK NUMBER
Figure 3. -Mean surface temperatures about the northern Channel Islands, based on 8 d throughout 1982 (see text footnote 3).
southeastern corner of Santa Rosa Islands. Warm
water occurred close to shore around Anacapa
Island, while cooler (perhaps upwelled) conditions
occurred slightly offshore to the east.
Fish Distribution
Data from our study suggest that the fish com-
munities of the northern Channel Islands resemble
those of the central and southern California main-
land. San Miguel and Santa Rosa harbor a more
temperate fauna than Santa Cruz and Anacapa. A
number of species characteristic of southern Califor-
nia (i.e., Sarda chiliensis, Scomber japonims,
Seriola lalandei, SphyraeTia argentea) were not
found off San Miguel or Santa Rosa, while other
southern California species {Scorpaena guttata and
Paraiabrax dathratits) were less abundant around
248
LOVE ET AL.: DISTRIBUTIONAL PAITERNS OF FISHES
the western islands. Similarly, fishes more charac-
teristic of the Oregonian Province (Ophiodon
elongatus, Sebastes caurimcs, S. nebulosus) were less
abundant or absent off Santa Cruz and Anacapa.
Evidence from Miller and Lea (1972) bolsters this
impression. Nineteen species have geographic range
limits along the island chain; of these, 9 (Anoplar-
chus purpurescens, Artedius harringtoni,
Chirolophis nugator, Hippoglossus stenolepis,
Nautichthys oculofa^ciatus, Radulinus vinculiis,
Sebastes nebulosics, Stichaeopsis'? sp., Synchirus gilli)
are temperate and 10 {Alloclinus holderi, Caranx
caballus, Chaenopsis alepidota, Cryptotrema coral-
linum, Gibbonsia erythra, Gnathephis catalinensis,
Gobiesox rhessodon, Leiocottus hirundo, Mobula
japonica, Paraclinus integrippinis) are subtropical
or tropical. With only one exception (Radulinus virv-
cuhis), species on the list typical of the Oregonian
Province have their southern limit about San Miguel
or Santa Rosa, while most southern forms are
limited to Anacapa and Santa Cruz.
Around Anacapa and the eastern end of Santa
Cruz, six species [Ophiodon elongatus, Sebastes
caurinus, S. miniatu^, S. mystinus, S. paucispinis,
S. serranoides) found in shallow water (0-36 m) to
the west were more abundant over deeper (37-72 m)
reefs. This is an example of "isothermic submer-
gence" (Briggs 1974). Discussing the mainland
southern California fish fauna, Briggs noted that
cooler preferring, temperate species sought deeper,
cooler waters in the warmer parts of their ranges.
All six species are temperate forms, all are found in
shallower waters off central California than along
the mainland of the Southern California Bight.
' The increased length of four rockfishes (Sebastes
caurinus, S. mystinus, S. paucispinis, S. ser-
ranoides) in shallow water around the western
islands is at least partially due to a variant of iso-
thermic submergence. Among rockfishes, juveniles
are more eurythermic than adults (Miller and Geibel
1973; Love 1978), favoring shallower, warmer
waters. Juveniles of these four species were found in
shallow waters along all the islands (though in
decreasing abundance toward the warmer east),
while adults were abundant in shallow waters only in
the cooler, more westerly part of the island chain.
Might the trend toward decreased mean sizes in
the eastern section be, in part, due to relatively high
fishing pressure? There are no records of total fish-
ing effort, stratified by depth, around these islands.
However, the California Department of Fish and
Game does have data on total angler-hours within
each block, derived from operator log-book records.
We present these data for 1975-78 in Table 5. It is
Table 5. — Partyboat effort about the northern Channel
Islands, 1975-78.
Year
No. anglers
No. anglers-hours
Block 684
1978
11,129
56,571.5
1977
3,295
14,743.4
1976
6,152
27,250.5
1975
7,465
35,296.5
133,861.9
Block 685
1978
3,048
14,596.0
1977
2,765
13,951.4
1976
4,689
23,135.5
1975
7,088
32,997.9
84,680.8
Block 686
1978
951
4,588.0
1977
1,044
5,293.9
1976
1,500
7,941.0
1975
2,504
11,803.2
29,626.1
Block 687
1978
947
4,534.0
1977
1,213
6,400.0
1976
2,115
9,928.0
1975
3,193
16,016.5
36,878.5
Block 688
1978
1,397
6,723.4
1977
1,363
6,838.5
1976
2,745
15,161.5
1975
2,840
15,425.0
44,148.4
Block 689
1978
1,259
5,986.4
1977
1,318
6,423.0
1976
1,951
9,193.5
1975
1,692
7,795.5
29,398.4
Block 690
1978
4,732
19.885.3
1977
5,065
23,292.7
1976
6,204
27,576.5
1975
6,565
28,374.0
99,128.5
Block 707
1978
3,994
19,580.6
1977
1,498
7,297.0
1976
877
3,974.5
1975
2,448
11,636.5
-
42,488.6
Block 708
1978
4,650
23,008.0
1977
5,931
28,793.8
1976
2,701
13,807.4
1975
2,202
10,268.0
75,877.2
Block 709
1978
1,615
7,796.0
1977
582
2.975.5
1976
499
2,208.0
1975
1,129
6,229.0
19,208.5
Block 710
1978
5,556
24,435.0
1977
2,800
13,792.5
1976
1,019
4,964.4
1975
2,390
12,544.0
55,735.9
Block 711
1978
764
3,661.5
1977
1,264
6,528.0
1976
556
2,459.0
1975
739
3,530.0
16,178.5
249
FISHERY BULLETIN; VOL. 83. NO. 3
our experience that much of the fishing effort in
these blocks is in the two depth regimes discussed
here. Thus we believe the figures in Table 5 are
reflective of the relative fishing effort between
blocks.
The data indicate that Anacapa (blocks 684, 707)
and eastern Santa Cruz (blocks 685, 708) were in-
deed among the most heavily fished areas. On the
other hand, the westernmost section of San Miguel
(block 690), with generally the largest fish size fre-
quencies, was also fished intensively. There are other
discrepancies between fishing pressure and size fre-
quencies (Fig. 2). Though block 686 (mid-Santa Cruz)
is only moderately fished, Sebastes serranoides mean
lengths (0-36 m) are similar to those of the more
heavily impacted areas to the east. The drop in S.
mystinus length (0-36 m) begins in block 687
(western Santa Cruz), another moderately fished
site. In fact, both S. mystinus and 5. caurirms taken
in adjacent block 710 (eastern Santa Rosa) are larger
than block 687, even though more fishing took place
in block 710. This is not to imply that differences in
fishing effort between areas may not play a role.
Rather, we believe that the response to temperature
by these species is also important.
The marine fauna of the Southern California Bight
is notable for its temporal fluctuation. Studies of
both fossil (Fitch 1969) and present day records
(Hubbs 1948; Radovich 1961; Stephens et al. in
press) indicate considerable fluctuation in relative
abundance between temperate and tropically derived
species. Much of this faunal variability is due to
unstable water temperature patterns over the con-
tinental shelf. Weakening of the California Current
allows for a northerly flow of subtropical water and
its associated fauna. During periods of strong
California Current, temperate forms increase in
abundance. Data for this paper were gathered dur-
ing the end of a cold cycle (1976) and the beginning
of a warm one (which continues to the present -
1984).
Juveniles and adults may move with insurgent
water masses. This is particularly true of such
pelagic or semipelagic species as Seriola lalandei,
Sphyraena argentea, Sarda chiiiensis, and Scomber
japonicus. All occur about Santa Cruz and Anacapa
Islands (and throughout much of the Southern
California Bight) in warmwater periods. During the
strong 1983 El Nino, the tropical yellowfin tuna,
Thunrms aibacares, and skipjack tuna, Euthynnus
pelamis, ventured far north of their usual range up
to Santa Cruz Island. Even relatively sedentary
species may follow currents. The finescale trigger-
fish, Batistes polylepis, was an early migrant into
southern California at the beginning of the warm
cycle in the mid-1970's and remains relatively com-
mon about inshore reefs as far north as Santa
Barbara.
Larval transport and subsequent species recruit-
ment may be affected by changes in water masses.
During 1983, a number of warm- temperate species
(including rock wrasse, Halichoeres semicinctus;
garibaldi, Hypsypops rubicunda; spotted sandbass,
Paralabrax maculatofasciatics; Seriola lalandei;
Sphyraena argentea; salema, Xenistius califomien-
sis) recruited off Santa Barbara, well north of their
usual range.* Similar unusual northerly recruitment
of Semicossyphtcs pulcher and Catalina goby,
Lythrypmcs dalli, occurred during the same period
off central California.^
Young of-the-year of warm-temperate species
have recruited north of their usual range in past
warm periods, e.g., 1957-58 (Radovich 1961). In
many cases, such as that of the opaleye, Girella
nigricans, off Monterey, only a single year class (i.e.,
1958) survives, leading in succeeding years to
populations of similar-sized individuals.^ During the
early 1970's, we observed that the population of
Semicossyphus pulcher around San Miguel, was com-
posed entirely of large individuals. Perhaps these,
too, were the survivors of a successful year class dur-
ing the 1957-58 warmwater period.
Conversely, during the years of strengthened
California Current, species more representative of
central California recruit south. The early 1970's
were a relatively cool water period and temperate
species such as kelp greenling, Hexagrammos deca-
grammus; Ophiodon elongatus; Sebastes mystinus;
and S. serranoides young-of-the-year successfully
recruited in southern California (Stephens and Zerba
1981; Stephens et al. in press). These maintained
themselves in the locally cool habitat at the head of
Redondo Submarine Canyon, well after they disap-
peared from much of the Bight. Water temperature
is also responsible for the continuation of long-term
temperate species remnant populations on the
southern sides of several Baja California points
(Hubbs 1960). Here, upwelling water creates suit-
able conditions for a number of temperate species,
which are either missing from, or found in deeper
water off of, southern California.
*S. Anderson and .1. McCullauj;;h, Marine Science Institute,
University of California, Santa Barbara, CA 93106, pers. commun.
November 1983.
*D. Miller, California Department of Fish and Game, 2201 Garden
Road, Monterey, CA 93940, pers. commun. January 1977.
^F. Henry, California Department of Fish and Game, 2201
Garden Road, Monterey, CA 93940, pers. commun. November
1983.
250
LOVE ET AL.: DISTRIBUTIONAL PATTERNS OF FISHES
It is likely that a continuing warmwater regime
has or will alter the species' composition we found.
For instance, we might expect less successful year
classes among the rockfishes about the eastern
islands. Stephens et al. (in press) noted the essen-
tially complete failure of Sebastes mystinus and 5.
serranoides recruitment off Palos Verdes and
Redondo Beach (on the southern California main-
land) during this current warmwater cycle. On the
other hand, warmwater species, such as Paralabrojx
dathratus or Scorpaena guttata, might recruit more
successfully around the previously cool westerly
islands. Migratory species, such as Seriola lalandei,
Sphyraena argentea, or Scomber japonicus may also
be more abundant about these westerly islands.
ACKNOWLEDGMENTS
We thank A. W. Ebeling for reviewing an early
draft and S. Warschaw for typing the manuscript. J.
Svejkovsky (Scripps Institution of Oceanography-
Satellite Oceanography) supplied the satellite sea
surface temperature data. This work was supported,
in part, by Federal Aid to sportfish restoration
(Dingell-Johnson) funds.
LITERATURE CITED
Briggs, J. C.
1974. Marine zoogeography. McGraw-Hill Co., NY, 475 p.
Ebeling, A. W., R. J. Larson, and W. S. Alevizon.
1980a. Habitat groups and island- mainland distribution of
kelp-bed fishes off Santa Barbara, California. In D. M.
Power (editor). The California islands: Proceedings of a
Multidisciplinary Symposium, p. 403-431. Santa Barbara
Mus. Nat. Hist.
Ebeling, A. W., R. J. Larson, W. S. Alevizon, and R. N. Bray.
1980b. Annual variability of reef-fish assemblages in kelp
forests off Santa Barbara, California. Fish. Bull., U.S.
78:361-377.
Fitch, J. E.
1969. Fossil records of certain schooling fishes of the Califor-
nia Current system. Calif. Coop. Oceanic Fish. Invest. Rep.
13:71-80.
HUBBS, C. L.
1948. Changes in the fish fauna of western North America
correlated with changes in ocean temperature. J. Mar. Res.
7:459-482.
1960. The marine vertebrates of the outer coast. Syst. Zool.
9:134-147.
1967. A discussion of the geochronolog>' and archeology of
the California Islands. In R. N. Philbrick (editor). Pro-
ceedings of the Symposium on the Biology of the California
Islands, p. 337-341. Santa Barbara Botanic Gardens,
Santa Barbara, CA.
1974. Review and comments. Marine zoogeography. Copeia
1974:1002-1005.
Hunt, G. L., .Ik.. R. L. Pitman, and H. L. Jones.
198(1. Distrihulioti and abundance of seabirds breeding on the
California ('hannel Islands. In U. M. Power (editor), The
California islands: Proceedings of a Multidisciplinary Sympo-
sium, p. 443-460. Santa Barbara Mus. Nat. HisL
KuLl'ACK, R. L.
1971. Oceanography of the Santa Barbara Channel. In R. L.
Kolpack (editor). Biological and oceanographical survey of the
Santa Barbara Channel oil spill 1969-1970. II. Physical,
chemical and geological studies, p. 90-180. Allan Hancock
Found., Univ. S. Calif., Los Angeles, CA.
Littler, M. M.
1980. Overview of the rock intertidal systems of southern
California. In D. M. Power (editor). The California islands:
Proceedings of a Multidisciplinary Symposium, p. 265-306.
Santa Barbara Mus. Nat. Hist.
Love, M. S.
1978. Aspects of the life history of the olive rockfish, Sebajites
serranoides. Ph.D. Thesis, Univ. California, Santa Barbara,
185 p.
Miller, D. J., and J. J. Geibel.
1973. Summary of blue rockfish and lingcod life histories; a
reef ecology study; and giant kelp, Macrocystif pyrifera,
experiments in Monterey Bay, California. Calif. Dep. Fish
Game, Fish Bull. 158, 137 p.
Miller, D. J., and R. N. Lea.
1972. Guide to the coastal marine fishes of California. Calif
Dep. Fish Game, Fish Bull. 157, 235 p.
Murray, S. N., M. M. Littler, and I. A. Abbott.
1980. Biogeography of the California marine algae with
emphasis on the southern California Islands. In D. M. Power
(editor). The California islands: Proceedings of a Multidisci-
plinary Symposium, p. 325-340. Santa Barbara Mus. Nat.
Hist.
Neushul, M., W. D. Clarke, and D. W. Brown.
1967. Subtidal plant and animal communities of the southern
California Islands. In R. N. Philbrick (editor). Proceedings
of the Symposium on the Biology of the California Islands, p.
37-55. Santa Barbara Botanic Gardens, Santa Barbara. CA.
Radovich, J.
1961. Relationships of some marine organisms of the north-
east Pacific to water temperatures. Particularly during 1957
through 1959. Calif. Dep. Fish Game, Fish Bull. 1 12, 62 p.
Reid, J. L., Jr., G. I. Roden, and J. G. Wyllie.
1958. Studies of the California Current system. Calif. Coop.
Oceanic Fish. Invest. Rep. 5:27-56.
Seapy, R. R., and M. M. Littler.
1980. Biogeography of rocky intertidal macroinvertebrates of
the southern California Islands. In D. M. Power (editor). The
California islands: Proceedings of a Multidisciplinary Sympo-
sium, p. 307-324. Santa Barbara Mus. Nat. HisL
SOKAL, R. R., and F. J. ROHLF.
1969. Biometry; the principles and practice of statistics in
biological research. W. H. Freeman, San Francisco, CA, 776
P-
Stephens, J. S., Jr., and K. E. Zerba.
1981. Factors affecting fish diversity on a temperate reef.
Environ. Biol. Fishes 6:111-121.
Stephens, J. S., Jr, K. E. Zerba, P. Morris, and M. S. Love.
In press. Factors affecting fish diversity on a temperate reef
II: The fish assemblage of Palos Verdes Point, 1974-81.
Environ. Biol. Fishes.
251
MORPHOLOGICAL DEVELOPMENT, IDENTIFICATION, AND BIOLOGY OF
LARVAE OF PANDALIDAE, HIPPOLYTIDAE, AND CRANGONIDAE
(CRUSTACEA, DECAPODA) OF THE NORTHERN NORTH PACIFIC OCEAN
Evan B. Haynes>
ABSTRACT
All published descriptions of pandalid, hippolytid, and crangonid larvae of the northern waters of the North
Pacific Ocean are summarized. Included are recent changes in nomenclature, definitions of terms used in
describing the larvae, and procedures for preparing larvae for examination. The general morphology of lar-
vae of the three families is reviewed, and development of the morphological characters used for their iden-
tification is discussed. Principal morphological characters and number of larval stages of known larvae in
each family are tabulated. Pandalid larvae are keyed to species and stage of development. A synopsis of the
most important morphological characters used for identification is given for larvae of each family, genus,
and species. Biologj' of the larvae is reviewed.
Larvae of the Pandalidae, Hippolytidae, and Cran-
gonidae (order Decapoda, tribe Caridea) are common
inhabitants of the neritic meroplankton of the north-
ern (temperate and arctic) waters of the North
Pacific Ocean. About 135 species of shrimps are
found in these waters, and larvae have been de-
scribed, at least in part, for 46 species. Many of these
descriptions, especially of hippolytids and cran-
gonids, are scattered in various foreign scientific
journals.
This report summarizes the morphology of de-
scribed larvae of the Pandalidae, Hippolytidae, and
Crangonidae of the northern North Pacific Ocean
and gives instructions for examining them. Develop-
ment of the characters used for identification is
discussed, and a generalized key to stage is given.
Larvae of each family, genus, and species are charac-
terized morphologically, and the principal mor-
phological characters and the number of the larval
stage are tabulated. Illustrated keys to species and
stages are provided for 9 of the 13 pandalid species
recorded from the northern North Pacific Ocean. De-
scriptions of larvae of the remaining four species of
pandalids have not been published although their
probable morphology has been discussed (Haynes
1980a). References to the published descriptions of
larvae of each species and a review of the biology of
the larvae are provided.
In the synopses of species, I have selected the most
distinguishing larval characters; however, these
>Northwest and Alaska Fisheries Center Auke Bay Laboratory,
National Marine Fisheries Service, NOAA, P.O. Box 210155, Auke
Bay, AK 99821.
characters may not always be repeated for similar
species, and additional characters may be needed for
a specific diagnosis. Other distinguishing characters
for the larvae discussed here can often be found in
the original published descriptions.
An annotated listing of published descriptions
precedes the synopsis of each species. When two or
more descriptions are listed, the most complete
description is given first. Whenever a "?" appears
after a species name or stage in the listings, the
author of the original description was uncertain of
the identification. In these cases, references to the
corrected or verified identification are included in
the listing. For a few species, descriptions of larvae
are based on specimens from the Atlantic Ocean. It
should be noted that morphological characters of lar-
vae of the same species from different geographical
areas may vary somewhat (Haynes 1978a).
Taxonomic Nomenclature
I used Rathbun's (1904) nomenclature of Panda-
lidae except for Pandalus tridens. After considering
both the larval and adult morphology of P. tridens
(see Rathbun 1902), I give this species full specific
rank (Butler 1980; Haynes 1980a) rather than sub-
specific rank as P. montagui tridens, a Pacific sub-
species of P. montagui Leach 1814.
Nomenclature of the Hippolytidae follows Hol-
thuis' (1947) revision of the genus Spirontocaris
sensu lato. Holthuis' revision, based on adult mor-
phology, has been verified from larval morphology
(Pike and Williamson 1961; Haynes 1981).
Nomenclature of the Crangonidae is based on the
Manuscript accepted August 1984.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
253-^^
FISHERY BULLETIN: VOL. 83, NO. 3
revision by Kuris and Carlton (1977), with one excep-
tion. I use only Crangon, rather than Crangon and
Neocrangon, because I agree with Butler (1980) and
consider Zarenkov's (1965) separation of the genus
Crangon into two subgenera, Crangon s.s. and
Neocrangon, to be invalid.
The synopsis of characters of Crangon septem-
spinosa larvae also applies to the characters of C. af-
finis larvae. Needier (1941), Kurata (1964b), and
Tesmer and Broad (1964) have described these as
two species, but according to Makarov (1967), the
two species are synonymous. Descriptions of the lar-
0. 5 mm
FiGi'RE 1.- Lateral view and body parts of a diagrammatic decapod shrimp larva. (A) A,, antennule; A^, antenna; C, carapace; Md, mandi-
ble; Mx,. maxillule; Mx.^, maxilla; Mxp,, maxilliped 1; Mxp^, maxilliped 2; Mxp.,, maxilliped 3; P,, pereopod 1; P^, pereopcxi 2; P,, pereopf)d 3;
Pj, pereopod h; Pl.^, pleopfxl 2; Pl^,, pleopod .5; S,, somite 1; S^, somite 6; T, telson; U, uropod; ad, anteroventrail denticles; as, antenna! spine;
254
HAYNES: PANDALIDAE, HIPPOLYTIDAK, ANDCRANGONIDAE LARVAE
vae of C. affmis and C. septemspinosa are very
similar. More comments on nomenclatxire for certain
species are given in the synopses.
Definition of Terms
I follow Williamson's (1969) terminology for
decapod larvae and Haynes' (1979) terminology for
larval appendages (Fig. 1). The terms are defined as
follows:
abbreviated development- less than five zoeal
stages,
carapace length -straight-line distance between the
0.25 mm
0. 5 mm
Figure I.- Continued -ds, dorsal spine; pi, posterolateral spine; pt, pteryRostomian spine; so, supraorbital spine; r, rostrum; rt, rostral
teeth. (B) A,, antennule; ac, aesthetascs; ap, antennule peduncle; if, inner flagellum. (C) A^. antenna; f, flagellum; ps, plumose setae; sc,
scale; ss. scale seg:ments. (D) Md, mandible; cl, curved lip; ip, incisor process; mp, molar process; p, palp; sp, subterminal process. (E) Md.
mandible; Im, lacinia mobilis. (F) Mx,, maxillule; b, basipodite; c, coxopodite; en, endopodite; st, subterminal seta. (G) MXj. maxilla. (H)
Mxpj, maxilliped 1; ep, epipodite.
255
FISHERY BULLETIN: VOL. 83, NO. 3
posterior margin of orbit and the middorsal pos-
terior margin of the carapace.
denticles -toothlike projections on anteroventral
margin of the carapace.
developed pereopods- segmented pereopods direct-
ed vertically under cephalothorax.
juvenile -young form, usually small, sexually im-
mature, and generally resembling adult.
larva -a free- swimming phase in the life cycle of the
individual whose morphology (such as body form,
appendages, and spination) and habit are different
from the adult. The term applies to both zoea and
Figure \.-Continued-(l) Mxp^, maxilliped 2. (J) Mxp,, maxilliped 3; b, basipodite; c, coxopodite; ca, carfjopodite; da, dactylopodite; ex, ex-
opodite; en, endopodite, is, ischiopodite; me, meropodite; pp, protopodite; pr, propodite. (K) P,, pereopod 1. (L) P2, pereopod 2; ch, chella.
256
HAYNES: PANDALIDAE, HIPPOLYTIDAE, ANDCRANGONIDAE LARVAE
megalopa. (For shrimp, the change from larva to
adult is usually somewhat gradual and may include
more than one molt.)
megalopa- larva with fully setose natatory pleopods^
on some or all abdominal somites.
setation formula of telson- setae or spines along the
terminal margin of the telson are numbered begin-
ning at the middle of the telson. Thus, 7 + 7 means
^In the Decapoda. the development of setose pleopods does not
always provide a convenient and clear distinction between zoeal and
postzoeal stages. Several species of Pandalidae metamorphose
gradually into the postzoeal stage (see Haynes 1976). The term
"megalopa", therefore, may include a single stage or several stages
depending upon the species. In this paper, the number of larval
stages includes all stages before the juvenile stage, regardless of
whether the megalopa has one or more stages.
that the telson has seven pairs of setae along the
terminal margin. The first pair is the medial pair,
setose - having setae (bristles),
spine -a sharp, pointed projection, usually long and
narrow,
spinose-with many spines,
spiniform - shaped like a spine,
spinule - small spine,
spinulose - with small spines,
stage - intermolt.
subchelate - the dactylopodite (finger) folds against
the preceding segment (propodite), as in the first
pereopod of crangonid adults,
length -total body length: distance (mm) from the
anterior tip of the rostrum to the posterior tip of
0.5 mm
0. 5 mm
Figure l.-Contmued-{M) P^, pereopod 4. (N) Pleopod; ai, appendix interna; en, endopodite; ex, exopodite. (0)
Tail fan; al, anal spine; en, endopodite; ex, exopodite; ts, telsonic spines.
257
FISHERY BULLETIN: VOL. 83, NO. 3
telson, excluding telsonic setae or spines.
unabbreviated development -five or more zoeal
stages.
undeveloped pereopod-unsegmented pereopod
directed anteriorly under cephalothorax.
zoea- larva vi^ith natatory setae on maxillipeds, wfith-
out setose natatory pleopods on some or all abdom-
inal somites 1-5.
Examination Procedure
It is usually necessary to dissect the animal and
mount certain appendages on a slide before the iden-
tification characters can be used. Visibility of
segmentation is often improved by clearing speci-
mens for several days in 10% KOH or full-strength
lactic acid. Larvae can be dissected with pins
designed for mounting small insects. (The pins are
available from most biological supply companies.)
After dissecting the larva, place the appendage in a
drop of mounting medium (I use Turtox^ CMC red
mounting medium) and cover with a cover glass.
Gently press the cover glass to splay hairs and setae
and make them easier to examine and count. After
mounting the appendages, examine them using a dis-
secting microscope.
GENERAL MORPHOLOGY OF LARVAE
Pandalid, hippolytid, and crangonid larvae have
three major body regions (Fig. 1): head, thorax, and
abdomen. The head and thorax are coalesced and are
dorsally covered by a common, unjointed cephalo-
thoracic shield, the carapace. The body is divided into
19 true somites which, with their appendages (Fig.
1), are grouped as follows:
1) The head, five indistinguishable fused somites, is
covered by the anterior portion of the carapace
(C) and has the first five pairs of appendages:
antennules (or first antennae) (AJ, antennae (A2),
mandibles (Md), maxillules (Mxj), and maxillae
(Mx,).
2) The thorax is composed of eight somites that are
dorsally fused with, and covered by, the carapace.
Each somite has a pair of appendages: Somites
1-3 each have a pair of maxillipeds (Fig. lA,
Mxpi.;j); somites 4-8 each have a pair of pereopods
(Fig. lA, P,.5).
3) The abdomen is composed of six somites (Fig. 1 A,
Si.^) and a terminal segment, the telson (T). The
'Reference to trade name does not imply endorsement by the Na-
tional Marine Fisheries Service, NOAA.
first five somites each have a pair of pleopods
(Fig. lA, Pl?.^). The sixth somite has uropods (U).
The uropods, when present with the telson, com-
prise the tail fan.
CHARACTERS USEFUL FOR
IDENTIFICATION OF LARVAE
Understanding the development of morphological
characters is necessary for identifying genus,
species, and stage of larval development. The follow-
ing discussion emphasizes the characters most useful
for identification. It should be noted, however, that
these characters are based on relatively few species
of a limited number of genera. For instance, in the
family Hippolytidae, the subterminal seta is ap-
parently absent in larvae of Hippolyte clarki from
British Columbia (Needier 1934) but present in lar-
vae of H. inermis and H. varians from European
waters (Williamson 1957a). The seta may also be
present in undescribed Hippolyte larvae from the
northern North Pacific Ocean. Characterization of
the family Pandalidae is based on only two genera,
Pandalapsis and Pandalus. In the northern North
Pacific Ocean, described larvae of these two genera
develop exopodites only on pereopods 1-2 or 1-3,
never on pereopods 1-4. Other genera of the family
(e.g., Plesionika) may develop exopodites on pereo-
pods 1-4 (Williamson 1957b). Additional descriptions
of decapod larvae from the northern North Pacific
Ocean will undoubtedly modify the morphological
characterizations given here.
Rostrum
In pandalid larvae, the rostrum (Fig. lA, r) is
always long (at least one-third the carapace length).
For most species of Pandalidae, the rostrum is styli-
form in Stage I and does not have teeth (Fig. lA, rt)
until about Stage III. The exceptions are Pandalop-
sis coccinata, P. dispar, and Pandalus platyceros. In
these species, the rostrum is curved in Stage I and
has teeth in all larval stages (Berkeley 1930; Kurata
1964a; Price and Chew 1972). In Stage I Pandalus
preTisor, the rostrum curves ventrally between the
eyes (Mikulich and Ivanov 1983).
The rostrum of hippolytid larvae may be absent,
or, if present, from minute to long. The rostrum is
usually without dorsal or ventral teeth in all stages.
European specimens oiEualus gaimardii, an excep-
tion, have two dorsal rostral teeth in the last zoeal
stage (Stage V) (Pike and Williamson 1961). If the
rostrum is short to long in Stage I, it is also styli-
form, except in Stage I Lebbeus groenlandicus (Fig.
258
HAYNES: PANDALIDAE, HIPPOLYTIDAE. ANDCRANGONIDAE LARVAE
Figure 2. - Stage I zoeae of Lehbeus groenlandicus
showing slightly sinuous rostrum and posterolateral
spines on abdominal somites 4 and 5.
2) and L. polaris, which have a sHghtly curved
rostrum (Haynes 1978b, 1981). In Stage I Hepta-
carpus camtschaticus, the rostrum is minute and
curves slightly dow^nward following the dorsal con-
tour of the eyes (Haynes 1981).
In crangonid larvae, the rostrum is long, spini-
form, and without teeth in all larval stages except for
Stage I zoeae of Sclerocrangon zenkevitchi and S.
boreas, which lack a rostrum, and Stage I zoeae of
Paracrangon echinata, which have a spinulose
rostrum (Birshteyn* and Vinogradov 1953; Kurata
1964b; Makarov 1968).
Spines on the Carapace
The presence or absence of certain spines on the
carapace is useful for distinguishing between
families and identifying one or more stages. The lar-
val carapace (Fig. lA, C) may have supraorbital
spines (so), pterygostomian spines (pt), antennal
spines (as), and anteroventral denticles (ad). Supra-
orbital spines are absent in all larval stages of the
Crangonidae. For pandalid and hippolytid larvae,
supraorbital spines are usually absent in Stage I and
the megalopa, but present in the intermediate zoeal
stages. However, there are some exceptions to these
generalizations. Larvae oiPandalus hypsinotus have
supraorbital spines only in Stages II and III, and lar-
vae of P. kessleri have supraorbital spines only in
Stage II (Kurata 1955; Haynes 1976). Larvae of P.
••Translator's spelling of "Birstein".
prensor are without supraorbital spines in all larval
stages (Mikulich and Ivanov 1983). In the Hippolyt-
idae, Spirontocaris spinus, S. lilljeborgii, and prob-
ably S. phippsil have supraorbital spines in all larval
stages (the spines are minute in Stage I). Spirorir
tocaris ochotensis has minute supraorbital spines in
Stage I; whether supraorbital spines develop later is
unknown. Lebheus groenlandicus, a species with
abbreviated development, has supraorbital spines
only in Stage II and the megalopa (Stage III) Pike
and Williamson 1961; Haynes 1978b, 1981). In all
three families, pterygostomian spines are usually
present in all larval stages. Antennal spines are often
absent in Stage I but usually develop in later stages.
Anteroventral denticles are most prevalent in the
early stages and usually, but not always, disappear
during larval development. Branchiostegal and
hepatic spines are rarely, if ever, present in the lar-
val stages.
Eyes
Development of the eyes is the same for nearly all
members of the three families. The eyes are com-
pound and sessile in Stage I and are stalked in later
stages. The exception. Stage I Pandalopsis cocci-
nata, has compound eyes that are only partially
attached to the carapace (Kurata 1964a).
Antennules
In the Pandalidae and nearly all hippolytid and
259
FISHERY BULLETIN: VOL. 83, NO. 3
crangonid larvae, the peduncle of the antennule (Fig.
IB, ap) is unsegmented in Stage I and becomes three
segmented later, usually in Stage II. The exceptions
are Stage I Sderocrangon boreas, which has a 3-seg-
mented antennule; Stage II Eualiis suckleyi and E.
fabricii, which have 2-segmented peduncles; and
both Stages I and II Lebbeiis polaris and L. groenlan-
dicus, which have unsegmented peduncles.
In Stage I pandalid and hippolytid larvae, the inner
flagellum (Fig. IB, if) of the antennule is usually a
plumose seta, whereas in Stage I crangonid larvae, it
is usually a setose spine. The only described excep-
tions are Stage I larvae of Pandaltis prensor, Sdero-
crangon boi'eas, S. salebrosa, and 5. zenkeiitchi. In
Stage I Pandalus prensor, the inner flagellum is
spine shaped and has a few simple setae medially. In
Stage I S. boreas, S. salebrosa, and S. zenkevitchi,
the inner flagellum is an oblong projection that is
naked except for a few minute, simple setae termi-
nally (Birshteyn and Vinogradov 1953; Makarov
1968; Haynes 1978b, 1981; Mikulich and Ivanov
1983).
Antennae
Segmentation of the tip of the antennal scale (Fig.
IC, sc, ss) is an important characteristic for distin-
guishing crangonid larvae from pandalid and hippo-
lytid larvae. In crangolid larvae, the scale tip is
unsegmented in all stages. In pandalid and hippolytid
larvae, the scale tip is unsegmented in only four
species: PayidalopRis coccinata, Pandalus kessleri, P.
prensor, and possibly Heptacarptis ( = Spirontocaris)
tridens (Needier 1934; Kurata 1955, 1964a, b;
Mikulich and Ivanov 1983). The absence of segmen-
tation of the scale tip of Pandalopsis coccinata, Pan-
dalus kessleri, and P. prensor is related to the ex-
tremely precocious development of these species.
Hepta<:arpus tridens, however, has unabbreviated
development (Needier 1934) and, presumably, a
segmented tip. Needier (1934) may not have ob-
served segmentation of the scale in H. tridens
because she based her description on unstained lar-
vae (staining emphasizes segmentation (Haynes
1976)).
Mandibles
Mandibles (Fig. ID) are described for most pan-
dalid larvae, but descriptions of mandibles for hippo-
lytid and crangonid larvae in the northern North
Pacific Ocean are usually limited to Stage I. I have
supplemented these limited descriptions with infor-
mation on larvae from other areas, particularly the
North Sea. Descriptions of late stage larvae from the
northern North Pacific Ocean are needed, however,
to verify development of mandibles in hippolytid and
crangonid larvae.
Zoeae of Pandalidae, Hippolytidae, and Crangoni-
dae have similar mandibles in all stages, and both
molar and incisor processes are present. In Stage I,
the incisor processes of the left and right mandibles
are typically biserrate or triserrate. The number of
teeth increases in later stages. In some species, the
left mandible also has a subterminal tooth and a
lacinia mobilis (movable spine adjacent to incisor pro-
cess; Fig. IE). The subterminal tooth and lacinia
mobilis are usually, if not always, absent on the right
mandible. In the Crangonidae, the incisor process
eventually becomes a molar process, usually at the
megalopa.
The most distinctive character of the mandible is
the absence of a palp in the zoeal stages. This palp
first appears in the megalopa or first juvenile stage
of Pandalidae and in the megalopa or later stages of
the Hippolytidae. In one exception, Pandalopsis coc-
cinata, the palp is present and segmented as early as
Stage I (Kurata 1964a). The palp is absent in all
stages of Crangonidae, including the adults.
The mandibular palp of the Hippolytidae may
develop somewhat later than the mandibular palp of
the Pandalidae. For instance, in some species of
Hippolytidae, the palp may not appear until as late as
the third or fourth juvenile stage (Lebour 1936), and
in some genera, such as Hippolyte, the absence of the
palp in the adult may mean the palp is absent in the
larvae also. The palp eventually becomes three
segmented in the Pandalidae and two segmented in
the Hippolytidae.
Maxillules
Lebour (1930) stated that Pandalus larvae have no
subterminal seta (Fig. IF, st) on the basipodite of the
maxillule (F^ig. IF, Mx,, b). Yet, the seta is present in
some or all larval stages of Pandalus kessleri, P.
tridens, P. stenolepis, P. borealis, P. goniurus, P. jor-
dani, P. hypsinotus, and Pandalopsis coccinata. The
seta is also present in the early stages of Pandalus
montagui, P. projnnquus, Pandalina brevirostris,
and Dichelopandahis bonnieri that were collected
from waters off Great Britain (Needier 1938; Kurata
1955, 1964a; Pike and Williamson 1964; Modin and
Cox 1967; Lee 1969; Haynes 1976, 1978a, 1979,
1980a). The subterminal seta is absent in hippolytid
and crangonid larvae described from the North
Pacific Ocean but is present in larvae of Hippolyte in-
ermis and H. varians from waters off Great Britain
(Lebour 1931). According to Gurney (1942) and Pike
260
HAVNKS:1'ANDAL11)AK. llll'I'OI.VTlDAK. ANDCRANGtWIDAE LARVAE
and Williamson (1964), the seta is probably the
vestige of an exopodite; however, Williamson (1982)
regards it as a vestigial epipodite or pseudoepipodite.
Maxillae
Development of the scaphognathite (exopodite) of
the maxilla (Fig. IG) is related to development of the
larvae. Most species that lack precocious develop-
ment have a scaphognathite that is not lobed proxi-
mally and has only a few (usually < 12) plumose
setae only on its outer margin. The scaphognathite
gradually becomes lobed proximally in subsequent
stages, and the outer margin becomes fringed with
many plumose setae. In species with precocious
development, the scaphognathite is lobed proximally
and fringed with many plumose setae in Stage I.
The number of plumose setae is sometimes used
for distinguishing Stages I or II of similar species.
For instance. Stage I zoeae oiPandalus horealis and
P. goniums are similar morphologically, and in these
species the scaphognathite has 12 and 5 plumose
setae, respectively. In later stages, however, the
number of plumose setae fringing the scaphogna-
thite becomes too great to be practical for distin-
guishing zoeae of similar species.
Maxillipeds
The number of natatory setae on the exopodite of
each maxilliped (Fig. IH-J) is helpful for distinguish-
ing Stage I hippolytid and crangonid zoeae from
Stage I pandalid zoeae. All Stage I hippolytid and
most Stage I crangonid zoeae have 4, 5, 5 natatory
setae on the exopodites of maxillipeds 1-3. In the
Pandalidae, all Stage I pandalid zoeae, except Pan-
dahis stenolepis, have ^ 8 natatory setae on the ex-
opodites of at least two pairs of maxillipeds. Stage I
P. stenolepis, however, cannot be differentiated from
Stage I hippolytid and crangonid zoeae based only on
natatory setae because Stage I P. stenolepis also has
4,5,5 natatory setae on the exopodite of each max-
illiped.
The absence or reduction in numbers or size of
natatory setae on the exopodites of maxillipeds is
associated with markedly precocious development.
This is especially true for Pandalopsis coccinata,
Sclerocrangon boreas, and S. zenkevitchi. Each of
these species has only one zoeal stage before molting
to the megalopa. In P. coccinata, the natatory setae
are absent from the third maxilliped. In 5. boreas,
the number of natatory setae on maxillipeds 1-3 is 2,
3, 4, respectively; and the setae are reduced in size.
Sclerocrangon zenkevitchi zoeae do not have nata-
tory setae on the maxillipeds.
Apparently, the absence or reduction in size of
natatory setae prevents zoeae from being planktonic.
Zoeae of S. boreas and S. zenkevitchi (collected at
sea) cling to the pleopods of the adult (Birshteyn and
Vinogradov 1953; Makarov 1968). Zoeae of P. cocci-
nnta are rarely, if ever, taken in plankton tows
(Kurata 1964a).
Pereopods
The presence of exopodites (Fig. IJ, ex) on certain
pereopodal pairs is an important morphological
character for identifying shrimp larvae. Exopodites
are present on pereopods 1, 1 and 2, 1-3, or 1-4,
depending on genus or species (Fig. IK-M).
Species with unabbreviated development usually
develop an exopodite on each pereopod. In most
species with > 5 zoeal stages, the exopodites are
characteristically small, naked, and nonfunctional at
Stage I but functional (have natatory setae) at Stage
II or III. Development of exopodites on pereopods
tends to be suppressed in species with < 5 zoeal
stages.
In the Pandalidae, species that have segmented
pereopods directed vertically under cephalothorax
(i.e., developed pereopods) in Stage 1- Pandalopsis
coccinata, Pandalopsis dispar, Pandnlus kessleri,
Pandalus danae, Pandalics hypsinotus, and Pari'-
d/ilus prensor- also have exopodites or vestigial exo-
podites on pereopods 1 and 2. Species that have
unsegmented pereopods directed anteriorly under
cephalothorax (i.e., undeveloped pereopods) in Stage
I -Pandalus tridens, P. stenolepis, P. borealis, P.
goniurus, and P. jordani -a\so have exopodites on
pereopods 1-3 (the exopodites are undeveloped in
Stage I and develop in later stages). An exception is
P. platyceros, which in Stage I has developed pereo-
pods and exopodites on pereopods 1-3 (Haynes
1980b).
Of the Hippolytidae, only larvae of the genus
Lebbeus have developed pereopods in Stage I.
Lebbeus polaris has vestigial exopodites on
pereopods 1 and 2 in Stage I and on pereopod 1 in
Stage II. Lebbeus groenlandicus has vestigial exo-
podites on pereopods 1 and 2 in Stage I and no exo-
podites on pereopods in Stages II or III (Haynes
1978b, 1981).
In the Crangonidae, most species with developed
pereopods in Stage I {Argis crassa, A. lar, A. deno-
tata, Sclerocrangon boreas, and S. salebrosa) are
either without exopodites or have rudimentary exo-
podites. An exception is S. zenkevitchi, which has an
exopodite on pereopod 1 in Stage I (Birshteyn and
Vinogradov 1953).
261
FISHERY BULLETIN: VOL. 83. NO. 3
Which pereopods have exopodites can differ for
different species of a genus. For example, the genus
Pandahis includes larvae that have exopodites on
pereopods 1 and 2 or 1-3 (Haynes 1980a). The genus
Eualus includes larvae that have exopodites on
pereopods 1-3 or 1-4 (Haynes 1981). Larvae of
Crangon typically have an exopodite only on
pereopod 1; however, larvae of C. franciscorum
angustimana have exopodites on pereopods 1 and 2
(Haynes 1980b).
Abdomen
The presence or absence of posterolateral spines
(Fig. lA, pi) on the abdomen is often an important
character for identif^'ing the families of caridean lar-
vae. Specimens of pandalid larvae from the northern
North Pacific Ocean do not have posterolateral
spines. Crangonid larvae, however, usually have
posterolateral spines on somite 5, except for larvae
of Sclerocrangon boreas and S. zenkeintchi (Birsh-
teyn and Vinogradov 1953; Makarov 1968). Larvae
of Hippolytidae also have posterolateral spines.
Posterolateral spines are present on somites 4 and 5
in Lebbeiis larvae and on somite 5 in Hippolyte lar-
vae, but are absent in Heptacarpus larvae.
The number of abdominal somites with postero-
lateral spines is not always the same for all species of
a genus. For instance, Spirontocaris larvae and most
Eualus larvae have posterolateral spines on somites
4 and 5, or 5. In some species oiEualua, the postero-
lateral spines may be absent.
Most pandalid and hippolytid larvae lack dorsal
spines or teeth on the abdomen. The only known
exception is Spirontocaris spinus, which has a
distinct dorsal tooth on the posterior margin of
abdominal somite 3 in the megalopa (Stage VI) (Pike
and Williamson 1961).^
Of the described crangonid larvae of the northern
North Pacific Ocean, only Crangon septemapinosa, C.
affinis, C. alaskensis, and C. franciscorum angusti-
mana have a dorsal spine (Fig. lA, ds) on somite 3
(Makarov 1967; Loveland 1968; Haynes 1980b).
Paracrangon echinata has dorsal spines on somites
1-5 (Kurata 1964b).
Some zoeae have spinules on the posterior margins
of abdominal somites. These spinules are present in
zoeae of Pandaliis platyceros, P. tridens, P. steno-
iepis, Eualus suckleyi, E. fabricii, Argis crassa, A.
dentata, and Crangon communis. The number and
size of spinules decrease in later stages.
*This spine is present in ail subsequent stages (juvenile and adult)
and should probably not be regarded as a larval character.
Telson
The shape of the telson is useful in determining the
stage of development of caridean larvae. For most
Stage I-III pandalid and hippolytid larvae, the
posterior margin of the telson is about twice the
width of the anterior margin. At about Stage IV, the
shape of the telson narrows posteriorly, and from
Stage IV on, the posterior margin of the telson is
noticeably less than twice the anterior width. Even-
tually, the telson narrows posteriorly, as in the adult.
Although the telson remains triangular in all stages
of crangonid larvae, it is somewhat narrower in the
megalopa or first juvenile stage than in earlier
stages.
For caridean larvae with unabbreviated develop-
ment, the typical number of telsonic setae (Fig. 1 0,
ts) is 7 -I- 7 in Stage I and 8 -i- 8 in later stages.
These numbers of telsonic setae are seldom exceeded
in later stages and are often reduced by either loss or
transformation of certain pairs (usually pairs of 2 or
3) into small setae or hairs.
A larger number of telsonic spines are more com-
monly associated with abbreviated development than
with unabbreviated development (Gurney 1942; Pike
and Williamson 1964), and this is generally true for
caridean larvae of the North Pacific Ocean. For ex-
ample, Pandalus kessleri, a species with four larval
stages, has 16 -h 16 telsonic setae in Stage I, and
Pandahpsis coccinata, a species with three (or two)
larval stages, has 28 + 28 telsonic setae in Stage I
(Haynes 1980a). Examples can also be found in the
other families of Caridea. In the Crangonidae,
Sabinea septemcarinata has 16 -(- 16 telsonic setae in
Stage I and three larval stages, whereas Sr/frorraw-
gon salehrosa has 22 + 22 telsonic setae in Stage I
and one larval stage (Williamson 1960; Makarov
1968). In the Hippolytidae, Lebbeus polaris has 9 + 9
telsonic setae in Stage I and four larval stages; L.
groenlandicus has a total of 21 telsonic setae in
Stage I and three larval stages (Haynes 1978b,
1981).
All larvae of Hippolytidae except larvae of the
genus Hippolyte have an anal spine (Fig. 10, al). For
Hippolyte larvae, the anal spine is absent in all
described stages. When pandalid and crangonid lar-
vae have unabbreviated development, the anal spine
usually appears at about Stage II in pandalid larvae
and about Stage IV in crangonid larvae.
However, the presence of an anal spine has little
value in the identification of pandalid and crangonid
larvae with abbreviated development. In pandalid
larvae with abbreviated development, the anal spine
first appears at different stages in different species.
262
HAYNES: PANDALIDAE, HIPPOLYTIDAE. ANDCRANGONIDAE LARVAE
For example, the spine is present in Stage I Pan-
dahis hessleri, but absent in P. hypsinotus until
Stage III. The stage at which the anal spine first ap-
pears in crangonid larvae with abbreviated develop-
ment has not been reported.
KEY TO STAGE OF DEVELOPMENT
Larvae of most of the species in this report can be
keyed to stage based on development of the eyes and
tail fan (Key I; Table 1). Key I is mostly applicable to
species whose larval development is not markedly
abbreviated (i.e., those with > 5 zoeal stages). In
species with unabbreviated development, exopodites
on pereopods are characteristically undeveloped in
Stage I and usually have natatory setae beginning at
Stage II or III. Most of the species excluded from the
key (Table 2) have < 4 zoeal stages, and exopodites
on pereopods are either absent in all stages, vestigial
in Stages I and II, or have natatory setae as early as
Stage I. Key I is limited because it does not differen-
tiate between the latest stages and uses only one or
two characters, which may be absent in damaged
specimens.
For pandalid shrimp. Key I can be supplemented
by keys to stages for each species (i.e.. Keys IV and
VI-XI, which have characters not given in Key I and
distinguish between the latest stages). With a few
Table 1.— Species included In keys.
Pandalidae Haworth 1825
HIppolytidae Bate 1888
Crangonidae White 1947
Pandalopsis Bate 1888
P. cocclnata Urita 1941
P. d/spar Rathbun 1902
Pandalus Leach 1814
P. boreal is Krdiyer 1838
P. danae Stimpson 1857
P. gon/urus Stimpson 1860
P. hypsinotus Brandt 1851
P. jordani Rathbun 1902
P. /(ess/en CzernlavskI 1878
P. platyceros Brandt 1851
P. prensor Stimpson 1860
P, stenolepis Rathbun 1902
P. tridens Rathbun 1902
Eualus Thallwltz 1892
E. barbatus (Rathbun 1899)
£. fabricii (Kr6yer 1841)
E. gaimardii (H. Milne Edwards 1837)
E. herdmani (Walker 1898)
E. macilentus (Krciyer 1841)
£. pusiolus (Krdyer 1841)
E. sucl<leyi (Stimpson 1864)
Heptacarpus Holmes 1900
H. brevirostris (Dana 1852)
H. camtschaticus (Stimpson 1860)
H. paludicola (Holmes 1900)
H. tridens (Rathbun 1902)
Hippolyte Leach 1815
H. clarki Chace 1951
Lebbeus White 1847
L. groenlandicus (Fabricius 1775)
L. Polaris (Sabine 1821)
Spirontocaris Bate 1888
S. arcuata Rathbun 1902
S. /////etoo/'g// (Danlelssen 1859)
S. murdochi Rathbun 1902
S. ochotensis (Brandt 1851)
S. phippsii (Kr(4yer 1841)
S. spinas (Sowerby 1805)
S. spinas var. intermedia
Makarov 1941
Argis Krciyer 1842
A. crassa (Rathbun 1899)
A. dentata (Rathbun 1902)
A. lar {Owen 1839)
Crangon Fabricius 1798
C. af finis de Haan 1849
C. alaskensis Locklngton 1877
C. communis Rathbun 1899
C. dalli Rathbun 1902
C. franciscorum angustimana
Rathbun 1902
C. septemspinosa Say 1818
Mesocrangon Zarenkov 1965
M. intermedia (Stimpson 1860)
Paracrangon Dana 1852
P. echinata Dana 1852
Sabinea J. C. Ross 1835
S. septemcarinata
(Sabine 1824)
Sclerocrangon G. O. Sars 1883
S. boreas (Phipps 1774)
S. salebrosa (Owen 1839)
S. zenkevitchi Birstein and
Vinogradov 1953
Table 2. — Species that cannot be keyed to stage of develop-
ment using Key I.
Pandalidae
Hippolytidae
Crangonidae
Pandalopsis
P. cocclnata
P. d I spar
Pandalus
P. danae
(Stage III)
P. hypsinotus
(Stage III)
P. kessleri
P. platyceros
P. prensor
P. stenolepis
(Stage III)
Lebbeus
L. groenlandicus
L. polaris
Argis
A. crassa
A. dentata
A. lar
Sclerocrangon
S. boreas
S. salebrosa
S. zenkevitchi
Sabinea
S. septemcarinata
263
FISHERY BULLETIN: VOL. 83. NO. 3
exceptions, Key I can be used to identify larval
stages of Pandalus hypsinotus, P. danae, and P.
stenolepis. The exceptions are in Stage III P. hyp-
sinotus, the endopodite of the uropods is setose and
nearly the same length as the exopodite, and in
Stage III P. danae and P. stenolepis, the endopodite
is setose and somewhat shorter than the exopodite.
Key I. — Generalized key to stages of most species of
pandalid. hippolytid, and crangonid larvae described
from waters of the northern North Pacific Ocean.
(This key cannot be used for all species, see Table 2 for
exceptions.)
1 . Uropods absent 2
Uropods present 3
2. Eyes sessile; telson with 7 + 7 setae. . . . Stage I
Eyes stalked; telson with 8 + 8 setae . . Stage II
3. Posterior width of telson about twice its
anterior width. Endopodite of uropod (Fig.
1 0, en) with relatively few setae and
noticeably shorter than exopodite (Fig. 1 0,
ex) Stage III
Posterior width of telson noticeably less than
twice its anterior width. Endopodite of
uropod setose and about as long as exopodite
Stage IV and later
LARVAL CHARACTERS OF FAMILIES
Crangonid larvae are relatively easy to distinguish
from pandalid or hippolytid larvae; however, pan-
dalid and hippolytid larvae often are difficult to
distinguish from each other, especially in the early
stages. Briefly, the characteristics of crangonid lar-
vae are 1) the tip of the antennal scale is always
unsegmented, 2) the inner flagellum of the antennule
is a setose spine or oblong projection, 3) an exopodite
is usually only on pereopod 1 and never on pereopods
3-5, and 4) in later stages, pereopod 1 is subchelate,
and the telson widens posteriorly. No known pan-
dalid or hippolytid larvae possess this combination of
characters.
The following set of characters, although not with-
out exceptions, is probably the most useful set for
distinguishing between pandalid and hippolytid lar-
vae of the northern North Pacific Ocean. Pandalid
larvae 1) always have a long rostrum (greater than
1/4 carapace length) that has teeth from Stage III
on, 2) the basipodite of the maxillule has a subter-
minal seta, 3) exopodites are only on pereopods 1-2
or 1-3, 4) the abdomen lacks posterolateral spines,
and 5) an anal spine is absent in Stage I. On the other
hand, hippolytid larvae 1) have a rostrum that is long
and without teeth (especially from Stage III on), 2) in
all stages, the basipodite of the maxillule lacks a sub-
terminal seta, 3) exopodites are on pereopods 1-2,
1-3. or 1-4 (rather than only on pereopods 1-2 or 1-3),
4) the abdomen has posterolateral spines, and 5) an
anal spine is present in Stage I (except larvae of the
genus Hippolyte).
Late-stage (Stage IV and later) pandalid and
hippolytid larvae can often be distinguished from
each other by shape of eyes and distance between
bases of antennules. The eyes of pandalid lai-vae
taper toward the base, and the distance between
bases of antennules is more than the width of an
antennule. The eyes of hippolytid larvae are almost
cylindrical, and the distance between antennules is
less than the width of an antennule. In Stages I-III,
distinctions in the shape of eyes and distance be-
tween bases of antennules are usually not useful.
Shape of the larva is often helpful in distinguishing
between pandalid and hippolytid larvae during the
initial sorting. Pandalid larvae, when viewed lateral-
ly, have nearly straight antennules, whereas the
antennules of many hippolytid larvae curve upward.
The abdomen of pandalid larvae appears slightly
longer than the abdomen of hippolytid larvae in rela-
tion to length of the larva as a whole. These two
characters are difficult to quantify and are best
learned through examination of specimens of known
identity. Additional morphological characters that
distinguish larvae of the Pandalidae, Hippolytidae,
and Crangonidae are given in the synopsis of each
family.
PANDALIDAE
(Genera Pandalopsis and Pandalus)
In all stages, rostrum long, styliform, or slightly
sinuate; plumose seta on inner tlagellum of anten-
nule (Fig. IB, A|, if); maxillule with or without
subterminal seta (Fig. IF', Mx,, st) on basipodite; ab-
domen without dorsal spines, keels, or posterolateral
spines; pereopod 1 never subchelate. In Stage I,
supraorbital spine absent; rostrum with teeth in
some species; anal spine absent in some s})ecies. In
early stages of most species, antennal scale seg-
mented at tip. In Stages I and 11 of some species with
abbreviated development, vestigial exopodites on
pereopods 1 and 2 or 1-3. In later stages, developed
exopodites on pereopods 1 and 2 or 1-3, never on 1-4;
setose setae on endopodite of each pleopod (Stage V
264
HAYNES: PANDALIDAE. HIPPOLYTIDAE, AND CRANGONIDAE LARVAE
Table 3.— Principal morphological characteristics and number of larval stages of known larvae of pan-
dalid shrimp of the northern North Pacific Ocean. + = yes; - = no.
Pereopods
No. of
Pereopods
poorly
Spinules on
Denticles
telson
No. of
bearing
developed
abdominal
on carapace
spines in
larval
Species
an exopodite
in Stage 1
somites
margin
Stage 1
stages
Pandalopsis coccinata
1-2
—
—
—
28 + 28
3
P. dispar
1-2
—
—
—
12 + 12
7
Pandalus kessleri
1-2
—
—
—
16 -t- 16
4
P. danae
1-2
—
—
—
7-1-7
6
P. hypslnotus
1-2
—
—
—
7 -H 7
7
P. platyceros
1-3
—
+
+
8-1-8
5
P. prensor
1-2
—
—
—
9 + 9
5
P. tridens
1-3
-1-
+
-1-
7 ^- 7
8
P. stenolepis
1-3
+
+
-1-
7 -H 7
6
P. boreal is
1-3
+
—
—
7 -H 7
6
P. goniurus
1-3
+
—
—
7-1-7
6
P. jordani
1-3
+
—
—
7-1-7
13
on); telson does not widen posteriorly, has > 1 pair of
lateral spines (Stage FV on).
The principal morphological characters and
number of larval stages of known larvae of pandalid
shrimp of the northern North Pacific Ocean are sum-
marized (Table 3, modified from Haynes 1980b).
Genus Pandalopsis Bate
Larval development abbreviated; larvae relatively
large (> 10.0 mm in Stage I). In all described stages,
rostrum with teeth; carapace without denticles;
antennal flagellum as long as or longer than body;
thoracic appendages noticeably long and thin; ab-
dominal somites without spines or spinules, somites
not flared laterally. In Stage I, pereopods seg-
mented; telson with at least 12 -i- 12 setae; telson
jointed with abdominal somite 6.
Pandalopsis coccinata Urita
Only Stage I described, known parentage; figure 7
in Kurata (1964a).
Eyes partially fused with carapace; antennal fla-
gellum same length as body; mandibular palp with 3
segments; seta on basipodite of maxillule; rudimental
exopodite on maxilliped 3 and pereopods 1 and 2;
telson discoid with 55 or 56 setae (Fig. 3). Length:
Stage 1, 15.5 mm. Range: Japan (Kurata 1964a), no
depth given.
Pandalopsis dispar Rathbun
Possibly 7 larval stages.
Stage I, known parentage; Stages II, III, and V?,
from plankton; figures 11-13 in Berkeley (1930).
1 . 0 mm
Figure 3. -Telson, Stage I zoea of Pandalopsis
coccinata.
In all stages, basipodite of maxillule without sub-
terminal seta. In Stage I, eyes sessile; antennal fla-
gellum about 1/4 longer than body. Telson fan
shaped in early stages. Until at least Stage V, man-
dibles without palps; developed exopodites on maxil-
liped 3 and pereopods 1-2. Length: Stage I, 10.0
mm. Range: Pribilof Islands, Bering Sea to Man-
hattan Beach, OR; depth, 46-649 m (Butler 1980).
Key II. — Larval stages of Pandalopsis dispar.
1. Rostrum curves dorsally (Fig. 4); exopodites
on pereopods without natatory setae . . . Stage I
265
FISHERY BULLETIN; VOL. 83, NO. 3
Figure 4. -Carapace, Stage I zoea of
Pandalopsis dispar.
i
1 . 0 mm
Rostrum horizontal; exopodites on pereopods
with natatory setae 2
2. Uropods absent; length of larvae < 13.0
mm Stage II
Uropods present; length of larvae • 13.0
mm 3
3. Endopodite of uropod noticeably shorter
than exopodite; length of larvae = 16.0
mm Stage III
Endopodite and exopodite of uropod same
length; length of larvae > 16.0 mm
Stage IV and later^
Genus Pandalus Leach
Most species with unabbreviated development. In
all stages, thoracic appendages not especially long or
thin. In Stage I, larvae usually 5-6 mm long; rostrum
usually without teeth; pereopods usually undevelop-
ed and tucked under cephalothorax; telson with 7 -t-
7 setae; telson not jointed with abdominal somite 6.
In early stages of some species, anteroventral
margin of carapace with denticles; posterior margin
of abdominal somites with spinules.
Pandalus borealis Kr<>yer'
Six larval stages.
•'A later larval stage, probably Stage V or VI, characterized by
rostrum with 25 dorsal spines: 1 spine near tip, 14 dorsal spines, 10
ventral spines. Chela of pererjjKxl 2 (Fig. 1, P^,, ch) developed, and
carpopodite (Fig. 1, ca) with a few faint segments; abdominal
somites and pleopods essentially adult; telson narrows posteriorly
and has 7 + 7 slightly plumose, terminal setae and 6 pairs of single
lateral spines. Length: .30.0 mm (Berkeley 1930).
'Larvae of ParuidLuK harealia and Pandaliuf goniurus are often
Stages I-V, VI (megalopa), and VII and VIII (ju-
veniles); all stages from both known parentage
and plankton; figures 1-7 in Haynes (1979).
Stage I, known parentage; Stages II-VII from
plankton; figures 1-3 in Kurata (1964a).
Stage I, known parentage; Stages II-VI from
plankton; figures 7 and 8 in Berkeley (1930).
Stages I-V from plankton; described as "P. propin-
quus (?)" by Stephensen (1912); figures 22-31 in
Stephensen (1912).
Stage III from plankton; described as "Spironto-
caris larva Nr. 4" by Stephensen (1916); figure
11 in Stephensen (1916). Also described as P.
propinquics, Stage VI? by Stephensen (1916);
figure 17 (chelae only) in Stephensen (1916).
Stage IV from plankton; described as "Dynuis
typus" (?) by Kr0yer (1861, as cited in Stephen-
sen 1935). No figures.
"Post larval" from plankton; Plate VII in Sars
(1900). Probably megalopa of P. borealis (see
Haynes 1979).
Not Stages I-VIII P. borealis as described by Sars
(1900) and figured in Plates I-VI. Correct iden-
tity, Caridion gordoni (see Berkeley 1930; Le-
bour 1930).
In all described stages, carapace and abdominal
somites not flared laterally; basipodite of maxillule
found together in plankton. They are esf)ecially similar in the early
stages and are difficult to distinguish. For identification of these two
species, I have included Table 4, which lists by larval stage the most
readily observable differences for both species. In general, larvae of
P. goniuni.'i are smaller than those of P. horeiilin. In SUiges I-III, P.
goninruK larvae have fewer setae on the antennal scale and certain
mouth parts than /'. horeali.^ larvae. From Stage IV to megalo()a,
the rostrum of P. hureaU.^ has more dorsal teeth, pereopcni 2 is more
developed, and the pleopods are fringed with more setae than larvae
of P. jrowmrus (Haynes 1979).
266
HAYNKS: I'AiNDAI^lDAK, HM'POLYTIDAK, ANDCKANCONIDAK l.AKVAK
with subterminal seta. Carapace usually with denti-
cles on anteroventral margins in Stages I-V.
Rostrum without teeth until Stage III; rostral tip
bifid in Stage V. In Stage I, exopodites of maxillipeds
1, 2, and 3 with 5 or 6, 13 or 14, and 16 natatory
setae, respectively; pereopods tucked under cara-
pace; left mandible with a lacinia mobilis; basipodite
of maxillule with 9 spinulose spines terminally; sca-
phognathite of maxilla with 12 setae along outer
margin. Length: Stages I-VI, 6.5-20.2 mm. Range:
Sea of Japan to Chukchi Sea to Columbia River
mouth (northwestern United States); Barents Sea to
North Sea; western Greenland to Gulf of Maine;
depth, 16-1,380 m (Butler 1980).
Key HI. — Larval and first juvenile stages of Pandalus
borealis (see footnote 7 and Table 4).
1. Eyes sessile; pleopods absent; telson with 7
+ 7 setae Stage I
Eyes stalked; pleopods present as minute
buds; telson with 8 + 8 setae 2
2. Rostrum without teeth; pereopods 4 and 5
tucked under cephalothorax; uropods
enclosed Stage II
Rostrum with ^ 1 dorsal tooth at base; pereo-
pods 4 and 5 extend ventrally; uropods free ... 3
3. Rostrum with 1 or 2 dorsal teeth at base;
antenna] flagellum with 8 segments and
same length as scale; endopodite of uropod
about 1/3 length of exopodite Stage III
Rostrum with ^ 4 dorsal teeth; antennal
flagellum with > 15 segments and longer
than scale; endopodite of uropod > 1/2 length
of exopodite 4
4. Rostrum with 4-8 dorsal teeth (usually 6),
without ventral teeth; tip of rostrum styli-
form; pleopods with a few small setae at tip;
endopodite of uropod about 2/3 length of
exopodite Stage IV
Rostrum with > 8 dorsal teeth and ^ 4 ven-
tral teeth; tip of rostrum bifid; pleopods
setose; endopodite of uropod nearly as long
as expodite 5
5. Rostrum with 9-12 dorsal teeth and 4 or 5
small ventral teeth; carapace with supra-
orbital spine; telson with 2 spines on each
lateral margin; lateral margins of telson
nearly parallel Stage V
Rostrum with > 12 dorsal teeth and ^ 6
distinct ventral teeth; carapace without
supraorbital spine; telson with ^ 4 spines on
each lateral margin; lateral margins of telson
taper posteriorly 6
6. Mandibles without palps; exopodites on max-
illipeds and pereopods reduced in size; lateral
margins of telson converge posteriorly but
widen slightly at junction with posterior
margin Stage VI
(megalopa)
Mandibles with palps; vestigial exopodites on
maxillipeds and pereopods; telson with lat-
eral margins converging to narrow tip, as in
adult Stage VII
(first juvenile)
Pandalus danae Stimpson
Six larval stages.
Stage I, known parentage; Stages II-VI, from
plankton; figures 3-5 in Berkeley (1930).
In all described stages, carapace without denticles
on anteroventral margin; basipodite of maxillule
without subterminal seta; posterior margins of ab-
dominal somites without spinules. In Stage I,
thoracic appendages developed; naked exopodites on
pereopods 1 and 2; telson jointed with abdominal
somite 6. Length: Stages I-VI, 5.7-17.0 mm.
Range: Resurrection Bay, AK, to Point Loma, CA;
depth, intertidal to 185 m (Butler 1980).
Key IV. — Larval stages of Pandalus danae.
1. Eyes sessile; carapace without supraorbital
spine; exopodites on pereopods 1 and 2 with-
out natatory setae Stage I
Eyes stalked; carapace with supraorbital
spines; exopodites on pereopods 1 and 2 with
natatory setae 2
2. Rostrum without teeth; uropods enclosed . . .
Stage II
Rostrum with teeth; uropods free 3
3. Rostrum with 2 or 3 minute dorsal teeth at
base; endopodite of uropods noticeably
shorter than exopodite Stage III
Rostrum with ^ 8 teeth dorsally; endopodite
of uropods same length as exopodite 4
4. Pleopods small, slightly cleft buds; telson
widens slightly posteriorly Stage IV
267
FISHERY BULLETIN: VOL. 83, NO. 3
Table 4— Morphological characteristics for distinguishing between larvae of Pandalus
borealis and P. goniurus reared in situ in Kachemak Bay, Alasl<a (from Haynes 1979).
Stage and characteristic
Pandalus borealis
Pandalus goniurus
Stage I zoea:
Mean total length
Number of plumose setae
fringing antennal scale
Number of spines
terminally on basipodite
of maxillule
Number of plumose setae
on scaphognathite (in
addition to single
proximal seta)
Number of natatory setae
on each exopodite:
maxilliped 1
maxilliped 2
maxilliped 3
Stage II zoea:
Mean total length
Rostrum
Antennal flagellum
Antennal scale
Stage IV zoea:
Mean total length
Rostrum
Antennal flagellum
Propodite of pereopod 2
Pleopods
Stage V zoea:
Mean total length
Rostrum
Chela of pereopod 2
Pleopods
Stage VI (megalopa):
Mean total length
Rostrum
6.7 mm (range 6.5-7.3 mm;
25 specimens)
19
11
5-6
13-14
16
7.5 mm (range 6.7-8.2 mm;
25 specimens)
Number of plumose setae
fringing antennal scale
about 25
Number of natatory setae
on each exopodite:
maxilliped 1
7
maxilliped 2
16
maxilliped 3
18
pereopods 1, 2, 3
16, 16, 12
Stage III zoea:
Mean total length
9.5 mm (
10 specimens)
1-2 conspicuous teeth
8-segmented
about 30 setae
13.0 mm (range 12.6-13.2
mm; 10 specimens)
6-7 dorsal teeth
about 1 Vz times length of
scale, extending past
tips of plumose setae
projected anteriorly about
1/2 length of
dactylopodite
segmented, pleopod 2
about 1/2 height of
abdominal somite
16.0 mm (range 15.2-17.1
mm; 10 specimens)
9-12 dorsal teeth; tip bifid;
45 partially developed
ventral teeth
fully formed
with appendix interna;
fringed with plumose
setae; 2 as long or
longer than height of
abdominal somite
18.5 mm (range 17.4-20.2
mm; 5 specimens)
13-15 dorsal teeth,
6-7 ventral teeth
4.0 mm (range 3.7-4.2 mm;
10 specimens)
4
8
12
5.9 mm (range 4.5-5.3 mm;
10 specimens)
about 19
6
12
14
12, 8, 8
6.2 mm (range 6.0-6.6 mm;
10 specimens)
1 inconspicuous tooth
3-segmented
about 20 setae
7.7 mm (range 6.8-8.3 mm;
10 specimens)
2 dorsal teeth
longer than scale but not
extending past tips of
plumose setae
projected anteriorly only
slightly
unsegmented, pleopod 2
about 1/3 height of
abdominal somite
10.3 mm (range 8.2-11.3 mm;
10 specimens)
5-6 dorsal teeth; tip not
bifid (but may show
slight protuberance);
no ventral teeth
not fully formed, propodite
extension about 1/2
length of dactylopodite
without appendix interna;
2-4 simple setae
terminally; pleopod 2
about 2/3 height of
abdominal somite
13.8 mm (range 11,1-15.8
mm; 6 specimens)
8-9 dorsal teeth,
4-5 ventral teeth
268
HAYNES: PANDAI.IDAK. IIII'I'OLVTIDAK. ANnCKANCONII'AK LAKVAK
Pleopods distinct and biramous; sides of tel-
son parallel or narrow posteriorly 5
5. Carapace with supraorbital spine; exopodites
on maxillipeds and pereopods have natatory
setae Stage V
Carapace without supraorbital spine; exopo-
dites on maxillipeds and pereopods naked
and vestigal Stage VI
(megalopa)
Pandalus goniurus Stimpson
(see footnote 7)
Six larval stages.
Stages I-V, VI (megalopa), and VII (first juvenile),
all from both known parentage and plankton;
figures 1-7 in Haynes (1978a).
Stages I-VII from plankton; figure 2 in Makarov
(1967).
Stage I, known parentage; figure 1 in Ivanov
(1965).
In all stages, carapace and abdominal somites not
flared laterally; subterminal seta on basipodite of
maxillule. In Stages I-V, carapace usually with den-
ticles on anteroventral margin. In Stage I, pereopods
1 -5 tucked under carapace; exopodites of maxillipeds
1-3 with 4, 8, and 12 natatory setae, respectively;
lacinia mobilis on left mandible; 5 spinulose spines
terminally on basipodite of the maxillule; 5 setae
along outer margin of scaphognathite of maxilla.
Rostrum without teeth until Stage IV (in Stage
III. rostrum with beginning of a tooth at base);
rostral tip becomes bifid in Stage VI. Length:
Stages I-VI, 3.7-15.8 mm. Range: Sea of Japan to
Chukchi Sea to Puget Sound, WA; 5-450 m (Butler
1980).
Key v.— Larval and first juvenile stages of Pandalus
goniurus (see footnote 6 and Table 4).
1. Eyes sessile; pleopods absent; telson with 7
-t- 7 setae Stage I
Eyes stalked; pleopods present as minute
buds; telson with 8-1-8 setae 2
2. Rostrum without teeth; pereopods 3-5 tucked
under cephalothorax; uropods enclosed
Stage II
Rostrum either with undeveloped or devel-
oped teeth; all pereopods extended ventrally;
uropods free 3
3. Rostrum with undeveloped tooth at its base;
antennal flagellum 3 segmented and about
2/3 length of scale; endopodite of uropod
about 1/3 length of exopodite Stage III
Rostrum with ^ 2 dorsal teeth; antennal fla-
gellum with ^ 6 segments and longer than
scale (not including setae); endopodite of
uropod nearly same length as exopodite 4
4. Rostrum with 2 dorsal teeth; antennal flagel-
lum does not extend beyond plumose setae of
antennal scale; chela of pereopod 2 not form-
ed; width of telson increases posteriorly ....
Stage IV
Rostrum with > 2 dorsal teeth; antennal
flagellum extends beyond plumose setae of
antennal scale; chela of pereopod 2 nearly or
fully formed; lateral margins of telson nearly
parallel or narrow posteriorly 5
5. Carapace with supraorbital spine; rostrum
with 5 or 6 dorsal teeth, no ventral teeth; tip
of rostrum styliform (may have undeveloped
bifid tip); lateral margins of telson nearly
parallel Stage V
Carapace without supraorbital spine;
rostrum with dorsal and ventral teeth; tip of
rostrum bifid; lateral margins of telson
narrow posteriorly 6
6. One or two setae betw^een several posterior
dorsal teeth of rostrum; 2-segmented mandi-
bular palp without setae; exopodites of maxil-
liped 3 and pereopods present but reduced;
carpopodite of left and right pereopods 2
with 20-25 and 7-9 joints, respectively
Stage VI
(megalopa)
One or two setae between most, if not all,
rostral teeth; 3-segmented mandibular palp
with spiniform setae; no exopodites on maxil-
liped 3 and pereopods; carpopodites of left
and right pereopods 2 with 29 and 1 1 joints,
respectively Stage VII
Pandalus hypsinotus Brandt
Seven larval stages.
Stages I-VI, VII (megalopa), and VIII-IX (juven-
iles), known parentage; figures 1-6 in Haynes
(1976).
Stage I, known parentage; Stages II-V, from
plankton; figures 5-6 in Kurata (1964a).
Stage I, known parentage; Stages II and III, from
269
FISHERY tU'LLETIN: VOL. 83. NO. 3
plankton; figures 6 (only Stage I figured) in
Berkeley (1930).
In all described stages, carapace without denticles
on anteroventral margin; posterior margins of ab-
dominal somites without spinules. In Stage I,
thoracic appendages segmented, dactyli undevelop-
ed; naked exopodites on pereopods 1 and 2; telson
not jointed with abdominal somite 6. Beginning in
Stage III, basipodite of maxillule with subterminal
seta; anal spine present. Length: Stages I-VII,
5.5-12.8 mm. Range: Sea of Japan to western Ber-
ing Sea; Norton Sound to Puget Sound, WA; depth,
5-460 m (Butler 1980).
Key VI. — Larval stages of Pandalus hypsinotus.
1. Eyes sessile; naked exopodites on pereopods
Stage I
Eyes stalked; exopodites on pereopods with
natatory setae 2
2. Rostrum without teeth; uropods enclosed . . .
Stage II
Rostrum with ^ 1 dorsal tooth at base;
uropods free 3
3. Rostrum with dorsal tooth at base and no
ventral teeth; exopodites on maxilliped and
pereopods with natatory setae Stage III
Rostrum with ^11 dorsal teeth and ^ 2
small ventral teeth; naked, vestigial exopo-
dites on maxillipeds and pereopods 4
4. Rostrum with 11-13 dorsal teeth and 2 or 3
small ventral teeth; tip of rostrum not bifid;
mandibular palps unsegmented; telson
margins nearly parallel but widen slightly
posteriorly Stage IV
Rostrum with > 13 dorsal teeth and > 3 ven-
tral teeth; tip of rostrum bifid; mandibular
palp with 3 segments; telson slightly wider
at midlength or narrows posteriorly 5
5. Bilobed pleopods without setae; telson slight-
ly wider at midlength Stage V
Biramous pleopods with setae; telson nar-
rows posteriorly 6
6. Carpopodite of left and right pereopods 2
with 19 and 7 or 8 joints, respectively; pleo-
pods with setae only at tip; telson with 3
pairs of dorsolateral spines Stage VI
Carpopodite of left and right pereopods 2
with 24 or 25 and 10 joints, respectively;
pleopods setose; telson with ^ 4 pairs of
dorsolateral spines Stage VII
(megalopa)
Pandalus jordani Rathbun
Thirteen larval stages.
Stages I-XIII, known parentage; figures 1-7 in
Modin and Cox (1967).
Stages I-XIII, Stages XIV and XV (juveniles), all
from both known parentage and plankton; fig-
ures 1-15 in Rothlisberg(1980).
Stages I-VIII, known parentage; figures 5-11 in
Lee (1969).
In all described stages, carapace and abdominal
somites not flared laterally and lack denticles or
spinules; basipodite of maxillule without subterminal
seta (except possibly Stage I). Pereopods tucked
under carapace in Stage I. Rostrum without teeth in
Stage I; rostnun with undeveloped dorsal tooth in
Stage II; rostral tip bifid beginning at Stage VIII.
Length: Stages I-XIII, 5.1-16.3 mm. Range: Un-
alaska. AK, to San Nicolas Island, CA; depth, 36-457
m (Butler 1980).
Key VII. — Larval and first juvenile stages of Pandalus
jordani.
1. Eyes sessile; telson and abdominal somite 6
not jointed Stage I
Eyes stalked; telson and abdominal somite 6
jointed 2
2. Rostrum with precursor of first dorsal tooth;
uropods enclosed Stage II
Rostrum with ^ 1 movable dorsal tooth;
uropods free 3
3. Rostrum with 1 movable dorsal tooth; endo-
podite of uropod a bud with only a few setae
" Stage III
Rostrum with > 1 movable tooth; endopodite
of uropod > 1/2 length of exopodite and se-
tose 4
4. Posterior width of telson about twice
anterior width Stage IV
Posterior width of telson noticeably less than
twice anterior width 5
5. Lateral margins of telson widen slightly
posteriorly Stage V
270
IIAYNKS: I'ANDAl.lDAK. llll'l'(>l,> TIDAK. AM i CKANCONMDAK I.AKVAK
Lateral niarjiins of telsoii parallel (ir narrow
posteriorly 6
6. Rostrum with 5 developed dorsal teeth and 1
un(ieveloped dorsal tooth; antennal flaj^ellum
with If) segments and same lenjj;th as scale
Stage VI
Rostrum with ^ 5 developed dorsal teeth and
> 1 undeveloped dorsal tooth; antennal tla-
gellum with > 20 segments and longer than
scale 7
7. Rostrum with 5 developed dorsal teeth and
styliform tip; anal spine absent Stage VII
Rostnmi with > 5 developed teeth, tip of
rostrum with precursor of sub terminal tooth;
anal spine present 8
8. Rostrum with 7 developed teeth; lateral
margin of telson with 2 spines Stage VIII
Rostrum with > 7 developed teeth; lateral
margin of telson with ^ 3 spines 9
9. Rostrum with 9 developed teeth; inner flagel-
lum of antennule with 3 segments; outer
flagellum of antennule with 2 segments
Stage IX
Rostnun with > 9 developed teeth; inner
flagellum of antennules with ^ 4 segments;
outer flagellum of antennule with 3 segments
10
10. Rostrum with 10 developed teeth; medial
pair of terminal telsonic spines shorter than
adjacent pair Stage X
Rostrum with > 10 developed teeth; medial
pair of terminal telsonic spines same length
or longer than adjacent pair 11
11. Inner flagellum of antennule with 4 seg-
ments; medial pair of terminal telsonic spines
same length as adjacent pair Stage XI
Inner flagellum of antennule with 5 seg-
ments; medial pair of terminal telsonic spines
longer than adjacent pair 12
12. Rostrum with 12 developed dorsal teeth and
precursors of 3 ventral spines; terminal
margin of telson straight Stage XII
Rostrum with > 12 developed dorsal teeth
and precursors of > 3 ventral teeth; terminal
margin of telson convex 13
13. Carapace with supraorbital spine; pereopod 2
with unsegmented car|)us Stage XIII
(last larval stage)
Carapace without supraorbital spine; pereo-
pod 2 with segmented carpus Stage XIV
(first juvenile stage)
Pandalus kessleri Czerniavski
Voxxv larval stages.
Stages I-IV and Stage V (first juvenile), known
parentage; figures 2-6 (fig. 6, first juvenile stage)
in Kurata(1955). (Stages II-IV have a mixture of
zoeal and megalopal characters.)
Abbreviated larval development. In all described
stages, carapace without denticles along antero-
ventral margin; antennal scale not jointed at tip; 2
lateral setae proximally on exopodite of maxilliped 1 .
Stages II and III with transverse dorsal groove.
Rostrum with teeth beginning in Stage II. Supra-
orbital spines in Stage II only. In Stage I, antennal
flagellum 3/4 length of body; antennal flagellum
segmented throughout its length; telson with 30-34
setae; anal spine present; zoea longer than 8.1 mm.
In Stage III, mandible with unjointed palp. Vestigial
exopodites on pereopods 1 and 2 in Stages I and II.
Pleopods with plumose setae in Stage II. Length:
Stages I-IV, 8.1-10.8 mm. Range: Hokkaido, Japan
(no depth given) (Kurata 1955).
Key VIII. — Larval and first juvenile stages of Pandalus
kessleri.
1. Rostrum without teeth; eyes sessile .... Stage I
Rostrum with teeth, eyes stalked 2
2. Mandible without palp; uropods enclosed;
carapace with supraorbital spine Stage II
Mandible with palp; uropods free; carapace
without supraorbital spine 3
3. Rostral tip not bifid; telson widens posteri-
orly Stage III
Rostral tip bifid; telson margins parallel or
narrows posteriorly 4
4. Mandibular palp unsegmented; sides of
telson parallel; telson with 2 pairs of lateral
spines and 11-14 terminal seta Stage IV
Mandibular palp segmented; telson narrows
posteriorly; telson with 3 pairs of lateral
spines and several terminal setae vestigial as
hairs Stage V
(first juvenile)
271
FISHERY BULLETIN: VOL. 83, NO. 3
Pandalus platyceros Brandt
Five larval stages.
Stages I-V and Stages VI-X (juveniles), known
parentage; figures 1-6 in Price and Chew (1972).
Stage I, known parentage; Stages II, IV?, and V?,
from plankton; figures 9 and 10 in Berkeley
(1930).
In all described stages, rostrum with teeth, basi-
podite of maxillule without subterminal seta. In
Stages I-III, carapace flares laterally, lateral
margins with denticles; abdominal somites flare
laterally, lateral margins with spinules (Fig. 5). In
Stage I, pleopods present as buds; telson jointed with
abdominal somite 6. In Stages II and III, less flaring
of abdominal somites and smaller denticles and
spinules than in Stage I. Thoracic appendages devel-
oped in Stage I, except naked endopodites on pereo-
pods 1-3. Length: Stages I-V, 8.1-13.0 mm. Range:
Sea of Japan, Hokkaido; Unalaska Island, AK, to off
San Diego, CA; depth, intertidal to 487 m (Butler
1980).
Key IX. — Larval and first juvenile stages of Pandalus
platyceros.
1. Rostrum without ventral teeth (Fig. 6); eyes
sessile; pereopods with naked exopodites
Stage I
Rostrum with ventral teeth; eyes stalked;
pereopods with setose exopodites 2
2. Antennal flagellum with 6 segments and
flagellum only slightly longer than plumose
setae of scale; uropods enclosed Stage II
Antennal flagellum with ^15 segments and
flagellum at least twice length of scale;
uropods free 3
3. Antennal flagellum about twice length of
antennal scale; telson widens posteriorly;
telson with 1 pair of lateral spines .... Stage III
Antennal flagellum > 3 times length of
antennal scale; telson margins parallel or
converge posteriorly; telson with > 1 pair of
lateral spines 4
4. Carapace with supraorbital spines; mandibles
without palps; pereopod 2 with unsegmented
carpopodite; telson with 2 pairs of lateral
spines Stage IV
Carapace without supraorbital spines; mandi-
bles with palps; pereopod 2 with segmented
Figure 5. -Dorsal view of
body. Stage I zoea of Payi-
dalles platyceros.
L
1 . 0 mm
Figure 6. - Rostrum, Stage I zoea Pandalus platyceros.
carpopodite; telson with > 3 pairs of lateral
spines 5
5. Telson margins nearly parallel, distal margin
concave Stage V
(megalopa)
272
HAVNKS: PANnAl.lDAK. mi'l'dl-VTIHAE. ANDCKANCONIDAK LAKVAK
Telson narrows posteriorly, distjil margin
convex Stage VI
(first juvenile stage)
Pandalus prensor Stimpson
Five larval stages.
Stages I-V (larvae) and VI-IX (juveniles), known
parentage; figures 2-7 in Mikulich and Ivanov
(1983).
Abbreviated larval development characterized by
marked heterochrony in development of appendages.
In all described stages, supraorbital spine absent;
antennal flagellum segmented; antennal scale not
jointed at tip; pereopods developed. In Stage I,
rostrum curves ventrally between eyes; telson
discoid and jointed with abdominal somite 6;
natatory setae on exopodites of maxillipeds 1-3 and
pereopods 1-2. Length: Stages I-V, carapace length
1.42-1.75 mm. Range: coastal waters of southern
Okhotsk Sea, Sea of Japan, and southeastern Siberia
(Vladivostok and Possjet Bay); depth, 2-93 m
(Holthuis 1976; Mikulich and Ivanov 1983).
Key X. — Larval stages of Pandalus prensor.
1. Eyes sessile; rostrom bends ventrally be-
tween eyes Stage I
Eyes stalked; rostrom straight 2
2. Rostrum does not extend to anterior margin
of eye; telson discoid; uropods enclosed
Stage II
Rostrum extends beyond anterior margin of
eye; telson rectangular; uropods free 3
3. Pleopods uniramous and unsegmented; tel-
son with 7 pairs of terminal spines .... Stage III
Pleopods (pairs II- V) biramous and segment-
ed; telson with ^ 5 pairs of terminal spines ... 4
4. Ventral rostrum with 4 teeth; telson with 5
pairs of terminal spines Stage IV
Ventral rostrum with 6 teeth; telson with 3
pairs of terminal spines Stage V
Pandalus stenolepis Rathbun
Six larval stages.
Stages I and II, known parentage; Stages III-VII
(Stage VII, first juvenile), from plankton; figures
1 and 2 in Needier (1938); figure 73 in Gurney
(1942; Page 208 verifies subterminal seta on
maxillule).
In Stages I-IV, carapace flares laterally, lateral
margin with denticles; abdominal somites with
spinules and flared laterally. P^laring, size of den-
ticles, and spinules decrease in Stages II-IV. In
Stage I, pereopods tucked under carapace; telson not
jointed with abdominal somite 6; and flagellum of
antenna longer than antennal scale. Pleopods absent
until Stage III. Length: Stages I-VI, 6.0-14.0 mm.
Range: Unalaska Island, AK, to Hecata Bank, OR;
depth, 49-229 m (Butler 1980).
Key XI. — Larval and first juvenile stages of Pandalus
stenolepis.
1 . Eyes sessile; rostrum without teeth .... Stage I
Eyes stalked; rostrum with teeth 2
2. Rostrum with only dorsal teeth (4-5 teeth);
uropods enclosed Stage II
Rostrum with dorsal and ventral teeth;
uropods free 3
3. Rostrum with 8 or 9 dorsal teeth and 2 ven-
tral teeth; pleopod buds only slightly cleft
Stage III
Rostrum with > 9 dorsal teeth and > 2 ven-
tral teeth; pleopods biramous 4
4. Unjointed pleopods without setae .... Stage IV
Jointed pleopods with setae 5
5. Right and left pereopods 2 with endopodites
of same length; pleopods with a few setae;
each endopodite without an appendix interna
(Fig. IN, ai) Stage V
Right and left pereopods 2 with endopodites
of different lengths; pleopods setose; each
endopodite with an appendix interna 6
6. Carapace with supraorbital spine; setose
exopodite on each pereopod Stage VI
(megalopa)
Carapace without supraorbital spine; naked,
vestigial exopodite on each pereopods
Stage VII
(first juvenile stage)
Pandalus tridens Rathbun
Probably 8 larval stages.
Stage I, known parentage; Stages I-VII, from
plankton; figures 1-7 in Haynes (1976).
Stage I, known parentage; figure 1 in Ivanov
(1971).
273
FISHERY BULLETIN: VOL. 83, NO. 3
In all described stages, carapace and abdominal
somites not flared laterally; antennal scale relatively
long and narrow (about 5-7 times as long as wide). In
Stages I-III, but rarely in Stage IV, carapace with
denticles along anteroventral and posteroventral
margins; posterior margin of abdominal somites 1-5
fringed with spinules (Fig. 7). Rostrum sinuate, pro-
jects somewhat upwards in Stages I-III, remains
shorter than carapace as late as Stage VIII, without
teeth until Stage IV. Antennal flagellum shorter
than antennal scale through at least Stage V.
Length: Stages I- VII, 3.1-13.0 mm. Range: Bering
Sea to San Nicolas Island, CA; depth, 5-1,984 m
(Butler 1980).
Key XII.— Larval stages (Stages I-VII) of Pandalus
tridens.
1. Eyes sessile; carapace without supraorbital
spine; pereopods 1-3 without exopodites;
telson with 7-1-7 setae Stage I
Eyes stalked; carapace with supraorbital
spine; exopodites on pereopods 1-3; telson
with 8-1-8 setae 2
2. Uropods enclosed Stage II
Uropods free 3
3. Endopodite of uropod < 1/2 length of
exopodite Stage III
Endopodite of uropod > 1/2 length of
exopodite 4
4. Rostrum with 2 dorsal teeth; endopodite of
uropod about 3/4 length of exopodite; telson
widens posteriorly Stage IV
Rostrum with > 2 dorsal teeth; endopodite of
uropod nearly same length as exopodite;
lateral margins of telson nearly parallel 5
5. Antennal flagellum with 5 segments and
about 2/3 length of antennal scale; chela of
pereopod 2 slightly developed (Fig. 8); pleo-
pod 2 about 1/4 height of abdominal somite
2 Stage V
Antennal flagellum with ^ 20 segments and
as long as or longer than antennal scale;
chela of pereopod 2 well formed (Fig. 9);
pleopods 2 at least 1/2 height of abdominal
somite 2 6
6. Rostrum with 6 dorsal teeth; pleopods
without setae; telson slightly wider near
center Stage VI
Figure 7. -Abdomen, Stage II zoea
of Pandalus tridens showing spinules
on posterior margins of somites.
0.25 mm
Figure 8. -Chela of pereopod 2, Stage V zoea of
Pandalus tridens.
274
HAYNES: PANDALIDAE, HIPPOLYTIDAE, AND CRANGONIDAE LARVAE
Rostrum with 7 dorsal teeth; pleopods tipped
with a few setae; telson margins nearly
parallel Stage VII
Figure 9. -Chela of pereopod
2, Stage VI zoea of Pandalns
tridens.
0.25 mm
HIPPOLYTIDAE
(Genera Eualus, Heptacarpus, Hippo lyte,
Lebbeus, and Spirontocaris)
In all described stages, rostrum absent to long,
usually spiniform (slightly sinuate in species with
abbreviated development); plumose seta rather than
long setose spine on inner flagellum of antennule;
exopodites on pereopods 1-2, 1-3, or 1-4; abdomen
without dorsal spine or keels on somite 3 (megalopa
of Spirontocaris spinus with a minute dorsoposterior
spine on abdominal somite 3); posterolateral spines
absent, on abdominal somites 4 and 5, or only on
abdominal somite 5 (spines may be lacking in mega-
lopa); pereopod 1 never subchelate; anal spine pres-
ent in all stages (exception: at least Stage I of Hyp-
poly te). Rostrum may have teeth in last zoeal stage
(megalopa); supraorbital spine usually absent in
Stage I. Stages I-III, antennal scale nearly always
jointed or partially jointed at tip. Stage I, exopodites
of maxilliped 1-3 with 4, 5, 5 natatory setae; about
Stage V, setose setae on endopodite of each pleopod;
telson does not widen posteriorly, has more than 1
pair of lateral spines.
The principal morphological characters and
number of larval stages of known larvae of hippolytid
shrimp of the northern North Pacific Ocean are sum-
marized in Table 5.
Table 5. — Principal morphological characteristics and nunnber of larval stages of known larvae of hippolytid
shrimp of the northern North Pacific Ocean. + = yes; - = no; ? = unknown.
Pereopods
Postero-
Supra-
bearing
lateral
orbital
Pereopods
an exopodite
spines on
Tel
sonic
No. of
spine in
In
in later
abdominal
spi
nes in
larval
Species
Rostrum
Stage 1
Stage 1
zoeal stages
somites
Stage 1
stages
Eualus barbatus
?
7
+
7
?
E. fabricii
+
—
'5
1-3
4,5
7
+
7
?
E. gaimardii
+
—
M
1-3
5
7
+
7
6
E. herdmani
—
—
—
?
—
7
+
7
?
E. macilentus
-1- =
—
—
?
—
7
+
7
?
E. pusiolus
+ ^
?
—
1-4
—
7
+
7
6-7
E. suckleyi
+
—
'5
1-3
5
7
+
7
?
Heptacarpus brevirostris
—
—
—
?
—
7
+
7
?
H. camtschaticus
+ '
—
'5
1,2
—
7
+
7
?
H. paludicola
—
—
—
?
—
7
+
7
?
H. tridens
—
—
—
?
—
7
+
7
?
Hippolyte clarki
-1-
—
'1
?
5
7
+
7
?
Lebbeus groenlandicus
+
—
5
—
4, 5
9(10)
+
10(11)
3
L. polarls
+
—
5
—
4, 5
9
+
9
4
Spirontocaris arcuata
-1-
—
'5
1, 2
—
7
+
7
?
S. liUjeborgii
-t-
-1-
'5
1, 2
4
7
+
7
6
S. murdochi
+
—
'5
1,2
4, 5
7
+
7
?
S. ochotensis
—
-1-
'5
1,2
4,5
7
+
7
?
S. phippsii
4-
+
'5
1,2
4,5
7
+
7
6
S. spinus
+
+
'5
1,2
4,5
7
+
7
6
S. spinus var. intermedia
+
—
^5
1,2
4,5
7
+
7
?
'Undeveloped pereopods. 'Minute.
275
FISHERY BULLETIN: VOL. 83, NO. 8
Genus Eualus Thallwitz
In Stage I, rostrum absent to long; carapace
without supraorbital spine; tip of antennal scale
jointed; pereopods absent or, if present, undevelop-
ed; anal spine present. Exopodites first appear on
pereopods 1-3 or 1-4 in Stage III. Posterolateral
spines absent, on abdominal somites 4 and 5, or only
on abdominal somite 5.
Eualus barbatus (Rathbun)
Only Stage I described, known parentage; figure 3
in Ivanov (1971).
Carapace without rostrum, supraorbital spine, or
denticles; pereopods absent; abdominal somites with-
out posterolateral spines or denticles but with
isolated hairs on dorsal surface of abdominal somites
3 and 4; abdominal somite 3 with indistinct row of
setae on dorsal surface. Length: 4.5 mm. Range:
Pribilof Islands, AK, to Hecata Bank, OR; depth,
82-507 m (Butler 1980).
Eualus fabricii (KrOyer)
Only Stages I and II described, known parentage;
figure 5 in Haynes (1981).
Not "Spirontocaris larva Nr. 3, Spirontocaris
fabricii!" as described by Stephensen (1916) (see
Haynes 1981).
Not "SpirontocarisAarvaie No. 3? Spirontocaris
fabricii (Kr0yer)" as described by Stephensen
(1935) (see Haynes 1981).
Not Spirontocaris fabricii as described by Frost
(1936) (see Haynes 1981).
Not "Eualus fabricii (Kr<)yer)" as described by
Pike and Williamson (1961) (see Haynes 1981).
In all stages, posterolateral spines on abdominal
somites 4 and 5. In Stage I, antennal flagellum about
1.5 times length of antennal scale; minute spinules
along dorsoposterior margins of abdominal somites 4
and 5 (spinules absent in Stage II); supraorbital spine
absent (small in Stage II). In Stages I and II, pereo-
pods 1-3 with undeveloped exopodites. In Stage II,
exopodites of maxillipeds 1-3 with 4, 9, and 11 nata-
tory setae, respectively; telson not jointed with ab-
dominal somite 6. Length: Stages I and II, 3.5-4.3
mm. Range: Sea of Japan, Okhotsk Sea; Chukchi
Sea to British Columbia; in northwestern Alan tic,
from Foxe Basin and West Greenland to Massachu-
setts Bay (eastern United States); depth, 4-255 m
(Butler 1980).
Eualus gaimardii (H. Milne Edwards)
Six larval stages.
Stages I-VI, known parentage; also Stages I and
11 from plankton; figure 2 in Pike and William-
son (1961).
Last zoeal stage from plankton, described as
"Spirontocaris-larva No. 2A" by Stephensen
(1935), probably E. gaimardii forma gibba (see
Pike and Williamson 1961, p. 198). No figure.
Stage V (?), described as "Spirontocaris B" by
Frost (1936), probably £". gaimardii {orma. gibba
(see Pike and Williamson 1961, p. 198); figure 4
in Frost (1936).
Stage I, known parentage; described as Spironto-
caris gaimardii by Lebour (1940); figure 1 in
Lebour(1940).
Stage I, known parentage; figures 21-23 in
Williamson (1957a: figures from Lebour 1940).
In all described stages, rostrum long (about 1/3
carapace length); no subterminal seta on maxillule.
Rostrum without teeth until Stage V. In Stage V,
rostrum with 2 dorsal teeth; in Stage VI, rostrum
with 3 dorsal teeth. Supraorbital spine in Stages
II-V. Carapace with 3 or 4 denticles on anteroventral
margin in Stages I-IV. Antennal flagellum does not
extend beyond antennal scale until Stage V. Nata-
tory setae on exopodites of maxillipeds 1-3: 5, 7, 7
natatory setae, respectively, in Stage II; 5, 9, 9 in
Stage HI; and 5, 10, 10 in Stages IV and V. In
Stages I-V, posterolateral spine on abdominal somite
5. Length: Stages I-VI, 2.9-5.4 mm. Range: cir-
cumpolar, southward to North Sea; Cape Cod, MA;
Sitka, AK; Siberia; depth, 10-900 m (Holthuis 1947).
Eualus herdtnaHt (Walker)
Only Stage I described, known parentage; describ-
ed as "Spirontocaris herdmani" by Needier
(1934). No figure.
Stage I, known parentage; Pike and Williamson
(1961: description from Needier 1934). No
figure.
Carapace without rostrum or supraorbital spine
but with 3 anteroventral denticles; abdomen without
posterolateral spines; anal spine minute. No length
given. Range: Sitka, AK, to Puget Sound, WA;
depth, 18-232 m (Butler 1980).
Eualus macilentus (KrOyer)
Only Stage I described, known parentage; figure 2
in Ivanov (1971).
276
IIAVNKS; I'AMiAl.lDAK. HII'I'Ol.Vl'IDAK. ANDCKANCONIDAK LAk\ AK
No supraorbital spine; 4 denticles on anteroventral
martjin of carapace; pereopods absent; abdomen
witliout spines or denticles. Lenj^th: 3.0 mm.
Range: West Greenland to Nova Scotia; Bering and
Okhotsk Seas; depth. 150-540 m (Holthuis 1947).
Eualus pusio/ijs (Kr0yer)
Larvae described from Atlantic specimens.
Seven or eight larval stages.
Stage I, known parentage; Stages I-VII, from
plankton; figure 3 in Pike and Williamson (1961).
Last zoeal stage, from plankton, described as
"Spirontocaris C" by Frost (1936); figure 5 in
Frost (1936).
Stage L known parentage; described as "Spironto-
cay-is pusiola" by Bull (1938); figure 1 in Bull
(1938).
Stage I, known parentage; figures 27-30 in
Williamson (1957a); figures from Bull (1938).
It! all described stages, 3 denticles on anteroven-
tral margin of carapace; no spines, denticles, or dor-
sal setae on abdominal somites. Rostrum minute in
Stage L only slightly larger in other stages, without
teeth in all stages. Exopodites of maxillipeds 1-3,
with 5,8, and 8 natator\' setae, respectively, in Stage
II. In Stages V-VIII, pereopods 1-4 with setae.
Length: Stages I-VIII, 2.2-4.8 mm. Range: Sea of
Japan to Chukchi Sea and British Columbia; Gulf of
St. Lawrence to Cape Cod, MA; Europe from the
southwestern Barents Sea to Spain; depth, intertidal
to 1.381 m (Butler 1980).
Eualus suckleyi (Stimpson)
Only Stages I and II described, known parentage;
figTjres 3 and 4 in Haynes (1981).
In Stage I, anteroventral margin of carapace with
3 or 4 denticles; undeveloped exopodites on pereo-
pods 1-3. In Stage II, carapace with supraorbital
spine, without denticles along anteroventral margin.
In Stage II, maxillipeds 1-3 with 4, 5, and 5 natatory
setae, respectively; pereopods 1-5 present but
undeveloped. Length: Stage I, 3.0-3.5 mm; Stage
II, 3.5-4.2 mm. Range: Okhotsk Sea to Chukchi Sea
to about Grays Harbor, WA; depth, 11-1,025 m
(Butler 1980)."
Genus Heptacarpus Holmes
Only Stage I described. Rostrum minute to absent;
no supraorbital spine; pereopods absent or pairs 1 -5
present but undeveloped; abdominal somites without
posterolateral spines; exopodites develop on pereo-
pods 1 and 2; tip of antennal scale not always jointed.
Heptacarpus brevirostris (Dana)
Stage I, known parentage; described as Spironto-
caris brevirostris by Needier (1934). No figures.
Carapace without anteroventral spines; antennal
scale partially jointed at tip. Length: Stage I, 1.5
mm. Range: Aleutian Islands, AK, to San Fran-
cisco Bay, CA; depth, intertidal to 128 m (Butler
1980).
Heptacarpus camtschaticus (Stimpson)
Stage I, known parentage; figure 8 in Haynes
(1981).
Carapace without spines; minute rostrum curves
slightly downward following dorsal contour of eyes;
undeveloped exopodites on pereopods 1 and 2; abdo-
men without spines or spinules. Length: Stage I.
2.9 mm. Range: Sea of Japan to Chukchi Sea and
Strait of Georgia, WA; depth, intertidal to 108 m
(Butler 1980).
Heptacarpus paludicola (Holmes)
Stage I, known parentage; described as Spironto-
caris paludicola by Needier (1934); figure 1 in
Needier (1934).
Antennal scale partially jointed at tip; abdomen
without posterolateral spines. Length: Stage I, 2.0
mm. Range: Tava Island, AK, to San Diego, CA;
depth, intertidal to 10 m (Butler 1980).
Heptacarpus tridens (Rathbun)
Stage I, known parentage; described as Spironto-
caris tridens by Needier (1934); figure 1 in
Needier (1934).
Carapace without anteroventral spines; antennal
scale unsegmented. Length: Stage I, 3.0 mm.
Range: Aleutian Islands, AK, to Cape Flatter^', WA;
depth, intertidal to 110 m (Butler 1980).
Genus Hippo lyte Leach
Only Stage I described. Antennal scale without
joints at tip.
277
FISHERY BULLKTIN: VOL. 8.S. NO. :>.
Hippo lyte clark't Chace
Stage I, known parentage; described as Hippolyte
califomiensis by Needier (1934); figure 1 in
Needier (1934).
Rostrum long; carapace with 4 anteroventral den-
ticles; bud of pereopod 1 present; small postero-
lateral spines on abdominal somite 5. Length: 1.9
mm. Range: Sheep Bay, AK. to Puget Sound, WA;
Santa Catalina Island, CA; depth, intertidal to 30.5
m (Butler 1980).
Cape Cod, MA; Bering and Okhotsk Seas; Aleutian
Islands, AK; depth, 0-930 m (Holthuis 1947).
Genus Spirontocaris Bate
In all described stages, rostrum absent to long;
posterolateral spines on abdominal somites 4 and 5,
or 5 only; no minute spines on posterior margins of
abdominal somites. In Stage I, supraorbital spine
present or absent; all pereopods present luit undevel-
oped. Exopodites only on pereopods 1 and 2 in later
stages (usually by Stage IV or V).
Genus Lebbeus White
In all described stages, posterolateral spines on
abdominal somites 4 and 5 (Fig. 2). In Stage I, larvae
relatively long (> 5.0 mm); rostrum long, slightly
sinuate (Fig. 2), with no supraorbital spine. Abbre-
viated development.
Lebbeus groenlandicus (Fabricius)
Three larval stages.
Stages I-III from both known parentage and plank-
ton; figures 1-3 in Haynes (1978b).
Stage I. known parentage; figure 5 in Ivanov
(1971).
Not "SpironfocarisAarva. No. lA." as described by
Stephensen (1935) (see Haynes 1978b).
Somewhat more developed in each stage than lar-
vae of L. polaris. In Stage II, no vestigial exopodites
f)n pereopods. Telson with about 20 setae in Stages I
and II, and 3 -(- 3 spines in Stage III (megalopa).
Length: 6.4-7.6 mm. Range: Sea of Japan to
Chukchi Sea to Puget Sound, WA; arctic coast of
Canada; Greenland to Cape Cod, MA; depth, 11-518
m (Butler 1980).
Lebbeus polaris (Sabine)
Probably 4 larval stages.
Stages I and II, known parentage; figures 1 and 2
in Haynes (1981).
Neither Spirontocaris polaris (= L. polaris) as
described by Stephensen (1916) nor "Spironto-
mnls-larva No. 1" as described by Stephensen
(1935) (see Haynes 1981).
In Stages I and II, telson with 9 -i- 9 setae. In
Stage II, vestigial exopodite on peropod 1. Length:
Stage I, 5.2 mm; Stage II, 5.8 mm. Range: circum-
polar, southward to the Skagerrak and Hebrides;
Spirontocaris arcuata Rathbun
Only Stage I described, known parentage; figiuv 6
in Haynes (1981).
Rostrum short (about 1/7 carapace length), pro-
jects downward following contour of eyes; 2 or 3
minute denticles on anteroventral margin of cara-
pace; supraorbital spine absent; posterolateral spines
on abdominal somites 4 and 5. Length: 4.1-4.4 mm.
Range: Sea of Japan to Chukchi Sea to Juan de Fuca
Strait, WA; Canadian Arctic; depth, 5-641 m (Butler
1980).
Spirontocaris lilljehoriiii (Danielssen)
Larvae described from Atlantic Ocean.
Six larval stages.
Stages I and II, known parentage; Stages I-\'.
from plankton; Stages VI (megaloi:)a) and \1I
(first juvenile), reared in laboratory from Stage
V; figure 1 in Pike and Williamson (1961).
Stage I. known parentage; described as>). sjii)ii(s
var. lilljehorgi by Lebour (1937); figure 1 in
Lebour (1937).
Stage I; figures 14-16 iti Williamson (1957a). De-
scription and figures from Lebour (1937).
In all described stages, posteroanterior margins of
carapace smooth; abdominal somite 4 with a dorsal
tuft of short setae, without posterolateral spines.
Rostrum long (about 3/4 length of antennular pedun-
cle), deepens slightly in later stages but does not
develop teeth until megalopa. Supraorbital spine
rudimentary in Stiige I, clearly defined in later
stages. F\)sterolateral spines on abdominal somite 5
becoming smaller in later stages and may be absent
in Stages V and VI. Megalopa and first juvenile
stage without dorsal tooth on posterior margin of
abdominal somite 3. Length: Stages I-VI, 4.8-8.5
mm. Range: From Spitsbergen and southwestern
278
IIAVNES: I'ANDAI.IDAK. IIIl'rol.VI'IDAK, AMKKANCOMDAK I.AKNAK
Barents Sea south to south coast of England; Ice-
land; (ireenland; east coast of North America from
Nova Scotia to Massachusetts Bay; arctic Alaska;
depth, 20-1,200 m (Holthuis 1947).
Spirontocaris murdochi Rathbun
Only Stages I-III described, known parentage;
figures 1-3 in Haynes (in press).
Rostrum about 1/4 carapace length, supraorbital
spine in Stage III; posterolateral spine on abdominal
somite 5 longer than posterolateral spine on abdo-
minal somite 4; dorsal surface of abdominal somite 4
without tuft of setae. Length: Stages I-III, 3.2-4.3
nun. Range: Arctic to southeastern Alaska, Kam-
chatka, Sea of Okhotsk, Patience Bay (Sakhalin);
depth, 18-50 m (Holthuis 1947; Haynes in press).
Spirontocaris ochotetisis (Brandt)
Only Stage I described, known parentage; figure 7
in Haynes (1981).
No rostrum; carapace usually with only 1 denticle
along anteroventral margin; supraorbital spine
minute; posterolateral spines on abdominal somites 4
and 5. Length: 2.8 mm. Range: Sea of Japan to
Bering Sea and western coast of Vancouver Island,
British Columbia; depth, intertidal to 247 m (Butler
1980).
Spirontocaris phippsii (Kr0yer)
Larvae known from Atlantic Ocean.
Stage II, from plankton; Pike and Williamson
(1961). No figure. Identity assumed from distri-
bution of adults.
Stage III, from plankton; described as "Sprionto-
cam-larva Nr. 2," ("Sp. turgidaT); figure 6 in
Stephensen (1916). Not figure 7 in Stephensen
(1916), "last stage"; probably Eualus macilentus
(see Pike and Williamson 1961) (Pike and
Williamson identified figure 7 as E. macilentus
based on identity of S. spinus and S. lilljehorgii
and distribution of Eualus spp. in Greenland
waters).
Stage V, from plankton; described as "Spironto-
caris-larva No. 2 (? Sp. turgida (Kr0yer))" and
''Spirontocaris-\a.r\'s. No. 2B" in Stephensen
(1935) (see Pike and Williamson 1961 for identi-
fication).
Spines on abdominal somites 4 and 5; abdominal
somite 4 without dorsal tuft of setae. Length:
Stage II, 6.0 mm. Range: circumpolar, southward
to northern Norway; Cape Cod, MA; Shumagin
Islands, AK; and Plover Bay, Siberia; depth, 11-225
m (Holthuis 1947).
Spirontocaris spinus (Sowerby)
Larvae described from Atlantic Ocean only.
Six larval stages.
Stages I and II, known parentage; Stages III-VII
(Stage VII, first juvenile), from plankton; figure
1 in Pike and Williamson (1961).
Stage IV, from plankton; described as "Spironto-
caris A" by Frost (1936); figure 3 in Frost (1936)
(see Pike and Williamson 1961 for identifica-
tion).
Stage I, probably from known parentage; Stage V,
probably from plankton (see Pike and William-
son 1961); figures 17-20 in Williamson (1957a).
Larvae and juvenile stages very similar to those of
S. lilljeborgii. In all described stages, abdominal
somite 4 with a dorsal tuft of short setae; abdominal
somites 4 and 5 with posterolateral spines; postero-
lateral spines on abdominal somite 5 remain same
size in all zoeal stages. Posterior margin of abdo-
minal .somite 3 with distinct dorsal tooth in megalopa
and first juvenile stage. Length: Stages I-VI,
4.3-8.0 mm. Range: Circumpolar, southward to the
northern North Sea, Massachusetts Bay (eastern
United States), Alaska Peninsula, and eastern coast
of Siberia; depth, 16-400 m (Holthuis 1947).
Spirontocaris spinns var. intermedia Makarov*
Only Stage I described, known parentage; figure 4
in Ivanov (1971).
Not S. spimis intermedia as described by Makarov
(1967) (see Ivanov 1971).
Rostrum long (> 1/3 carapace length); no supra-
orbital spine; abdominal somite 4 with dorsal tuft of
setae; posterolateral spines on abdominal somites 4
and 5. Length: Stage I, 5.0 mm. Range: (see S.
spinus); depth, 9-1,380 m (Hayashi 1977).
^According to Ivanov (1971), V. V. Makarov, rather than Z. I.
Kobjakova, is the author of the subspecies 5. spimis var. intervriedia
based on Article .51(c) of Chapter XI of the International Code of
Zoological Nomenclature (International Commission on Zoological
Nomenclature 1964). The subspecies S. spinus var. intermedia.
however, may be identical toS. spiv^is. Hayashi (1977) believed that
the morphological criteria used by Kobjakova (1937) to distinguish
5. spinus var. intermedia from S. spimis were too small and
variable to be valid.
279
FISHERY BULLETIN: VOL. 83, NO. 3
CRANGONIDAE
(Genera Argis, Crangon, Mesocrangon,
Paracrangon, Sabinea, and Sclero crangon)
Rostrum nearly always present and long (at least
1/4 length of carapace), spiniform, and always with-
out teeth (rostrum spinulose in Stage I larvae of
Paracrangon echinata); supraorbital spine absent; in-
ner flagellum of antennule a setose spine or oblong
projection rather than a plumose seta; tip of antennal
scale never segmented; exopodite usually only on
pereopod 1 (rarely on pereopod 2); maxillule without
subterminal seta on basipodite; dorsal spine may be
on abdominal somite 3 or keels on both abdominal
somites 2 and 3; usually posterolateral spines on
abdominal somite 5; endopodite of pleopods undevel-
oped; usually telson widens posteriorly, never with
more than 1 pair of lateral spines. Pereopods 1 sub-
chelate at about Stage V. Anal spine absent until
about Stage IV.
The principal morphological characters and
number of larval stages of known larvae of
crangonid shrimp of the northern North Pacific
Ocean are summarized in Table 6.
Genus Argis Kr^yer
In Stage I, rostrum styliform; pereopods and pleo-
pods developed but not functional; exopodite on
pereopod 1 rudimentary or absent; abdominal somite
3 without dorsal spine; abdominal somite 5 with
posterolateral spine (posterolateral spine absent in
megalopa of A. dentata).
Argis crassa'' (Rathbun)
Only Stage I described, known parentage; figure 2
in Ivanov (1968).
Not Stage I A. crassa as described by Makarov
(1967) in figure 21.
Antennal scale without distal spine on outer
margin; endopodite of maxillule with 5 setae; sca-
phognathite of maxilla with 9 setae; abdominal
somites 2-5 fringed dorsally with small spinules;
telson and abdominal somite 6 jointed; telson with 8
+ 8 setae. Length: 7.5 mm. Range: Sea of Japan
to Bering Sea to San Juan Islands, WA; depth, 4-125
m (Butler 1980).
Argis dentata (Rathbun)
Three larval stages. Stage I described, known
parentage from Pacific Ocean; Stage I-III de-
scribed, from plankton from Atlantic Ocean.
Stages I-III, from plankton; figures 1-6 in Squires
(1965).
Stage I, known parentage; figure 3 in Ivanov
(1968).
Megalopa, from plankton; described as "Necto-
'Makarov (1967) described a crangonid larva from plankton that
has a short rostrum flattened dorsoventrally. He assumed it was
Argis (= Nectocrangon) crassa. According to Ivanov (1968), who
reared Stage I A. crassa from known parentage, the larva described
by Makarov is neither Argis crassa nor a later stage of Argis
crassa. The short flattened rostrum, however, is typically a post-
larval (juvenile) characteristic of crangonid shrimp. The specimen
described by Makarov, therefore, is probably a juvenile rather than
a larva.
Table 6. — Principal morphological characteristics and number of larval stages of known larvae of crangonid shrimp
of the northern North Pacific Ocean, -i- = yes; - = no; ? = unknown.
Pereopods
Postero-
bearing
lateral
Pereopods
an exopodite
spines on
Dorsal spine
Telsonic
No. of
in
in later
abdominal
on abdominal
spines in
larval
Species
Rostrum
Stage 1
zoeal stages
somite
somite
Stage 1
stages
Argis crassa
+
5
5
8 +
8
'2 or 3
A. dentata
+
5
5
—
8 -1-
8
3
A. lar
+
5
—
5
—
7 -1-
7
'3
Crangon alaskensis
+
—
5
3
7 +
7
5
C. communis
+
M
5
—
7 +
7
'5
C. dalli
+
^5
5
—
7 +
7
5
C. franciscorum angustimana
+
M
1,2
5
3
7 +
7
'5
C. septemspinosa
+
—
5
3
7 +
7
5-6
Mesocrangon intermedia
+
'5
5
—
8 -1-
8
5
Paracrangon echinata
+
?
1.2
1-5
1-5
7
7-1-
Sabinea septemcarinata
+
?
5
—
16 +
16
'4
Sclerocrangon boreas
—
5
—
—
—
12 +
12
2
S. salebrosa
-»-
5
5
22 -1-
22
1
S. zenkevitchi
—
5
—
—
—
—
'2
'Estimated.
'Undeveloped pereopods.
280
HAYNES: PANDALIDAK, HIPPOLYTIDAE, ANDCRANCONIDAE LARVAE
crangon larl, young stage" by Stephensen
(1916); figure 3 in Stephensen (1916).
In Stage I, antennal scale with distal spine on
outer margin; endopodite of maxillule and scaphog-
nathite of maxilla with 6 setae each; abdominal
somites 3-5 fringed dorsally with small spinules
(spinules not mentioned for Atlantic specimens);
telson and abdominal somite 6 jointed; telson with 8
+ 8 setae. In megalopa, short, pointed rostrum ex-
tends to middle of eye; carapace with 2 dorsal teeth,
ventral edge fringed with short plumose setae; ab-
dominal somite 5 without posterolateral spines.
Length: Stages I-III, 8.0-12.0 mm. Range: Sea of
Japan to Anadyr Gulf, Gulf of Georgia, and San Juan
Islands, WA; arctic Canada to Nova Scotia, Canada;
depth, intertidal to 2,090 m (Butler 1980).
Argis la I (Owen)
Probably 3 larval stages.
Stages I and II, from plankton; described cisNecto-
crangon lar by Makarov (1967); figure 22 in
Makarov (1967).
Not Crangonidae "Species F" (described by Kurata
1964b). as assumed by Makarov (1967). i"
In Stage I, telson and abdominal somite 6 not
jointed; telson with 7 -i- 7 setae. In Stage II, telson
with 8-1-8 setae. Abdominal somites without
spinules. Length: Stages I and II, 6.2-7.5 mm.
Range: Sea of Japan to Chukchi Sea to Strait
of Georgia, WA; depth, 10-280 m (Butler
1980).
Genus Crangon Fabricius
(= Crago Lamarck)
Five or six zoeal stages. Anteroventral margin of
carapace denticulate in most if not all larval stages.
In all described stages, rostrum about 1/3 carapace
length, spiniform, without teeth; posterolateral
spines on abdominal somite 5; exopodites develop
on either pereopod 1 or pereopods 1 and 2; ab-
dominal somite 3 usually with dorsal spine; telson
always widens posteriorly, with setae and < 8 + 8
spines.
Crangon alaskensis Lockington
Five larval stages.
Stages I-VII (Stage VI, first juvenile), known
parentage; illustrations 1-79 in Loveland (1968).
In all described stages, rostrum barely reaches
beyond eyes; dorsal spine on abdominal somite 3.
Length: Stages I-V, 2.0-3.3 mm. Range: Kuril
Islands; Bering Sea to Puget Sound, WA; depth,
intertidal to 275 m (Butler 1980).
Crangon communis Rathbun"
Only Stage I described, known parentage; de-
scribed as Sclerocrangon communis by Ivanov
(1968); figure 1 in Ivanov (1968).
Not Stages I I-V C. communis from plankton; de-
scribed by Makarov (1967) as Sclerocrangon
communis.^^
Antennal flagellum about 3/4 length of antennal
scale; antennal scale with 14 setae; abdominal
somites without keels; spinules on posterior margins
of abdominal somites 3-5. Length: Stage I, 4.8 mm.
Range: Sea of Japan to Chukchi Sea to San Diego,
CA; depth, 16-1,537 m (Butler 1980).
Crangon da Hi Rathbun
Five larval stages.
Stage I, known parentage; Stages II-V and VI
(first juvenile, "postlarval"), from plankton;
figure 18 in Makarov (1967). Larvae figured in
part but not described. Larvae thought to be
identical morphologically to C. allmani larvae
from the Atlantic Ocean (Makarov 1967).
Stage I from plankton; figures 7-9 in Birshteyn
(1938).
Not "last (?) stage" as described by Birshteyn
(1938) (see Makarov 1967).
Typical unabbreviated crangonid development. In
all described stages, carapace without dorsal, lateral,
or supraorbital spines; anterior margin of carapace
denticulate; rostrum spiniform, without teeth;
'"Morphological differences are too great for Makarov'.s Necto-
rrnngon lar larvae and Kurata's "Species F" larvae to be identical.
Makarov's larvae lack exopodites on pereopods in all stages and, in
Stages I and II, have posterolateral spines on abdominal somite 5.
Kurata's "Species F" larvae, known only in Stage II, have an exo-
podite on pereopod 1 and posterolateral spines on abdominal
somites 5 and 6.
•'Zarenkov (1965) proposed placing C. commuvis in a new
subgenus, Neocrangov. Butler (1980) has shown that Zarenkov's
diagnosis for Neon-angon is invalid, at least for British Columbia
species. Based on Butler's findings, I have retained C. mmmuni.^ in
the genus CraJigcn).
12 It is unlikely that Makarov's (1967) larvae and Ivanov's (1968)
larvae are the same species because Makarov's larvae have keels on
abdominal somites 2 and 3, whereas Ivanov's larvae do not.
281
FISHERY BULLETIN: VOL. 88. NO. 3
posterolateral spines on abdominal somite 5; abdo-
minal somites without spinules or keels; telson
always widens posteriorly, never with > 1 pair of
lateral spines. In Stage V, pleopods uniramous, with
buds of endopodites. Length: Stages I-V, 2.8-7.0
mm. Range: Sea of Japan to Chukchi Sea, to Puget
Sound. WA; depth, 3-630 m (Butler 1980).
Crangon franciscorum angustiwana Rathbun
Only Stage I described, known parentage; figure 1
in Haynes (1980b).
Rostrum extends beyond eyes; carapace without
shallow transverse groove; antennal scale with 10
plumose setae including subterminal seta along outer
margin; endopodite with 4 segments on maxilliped 1,
and 5 segments on maxilliped 3; exopodites of maxil-
lipeds not jointed; pereopods 1-4 present but un-
developed; buds of exopodites on perepods 1 and 2;
median dorsal spine on abdominal somite 3; postero-
lateral spines on abdominal somite 5; fifth pair of
telsonic spines about equal in length to fourth and
fifth pairs. Length: Stage I, 2.8-3.3 mm. Range:
Kachemak Bay, AK, to Tillamook Rock, OR; depth,
18-183 m (Butler 1980).
Crangon septemspinosa Say
Described from specimens from both Atlantic and
Pacific Oceans.
Five or six larval stages.
Stages I and II, known parentage; Stages III-VI,
from plankton; described as C. affinis by Kurata
(1964b); Pacific specimens; figures 1-29 in
Kurata (1964b).
Stage I, known parentage; Stages II-V, from
plankton; Atlantic specimens; described as
Crago septemspinosufi Say by Needier (1941);
figures 1 and 2 in Needier (1941).
Stages I-X (Stage X, first juvenile stage), known
parentage (larval series likely includes extra
stages); Atlantic specimens; figures 1-51 in
Tesmer and Broad (1964).
Stages I-V, from plankton; Pacific specimens;
figure 20 in Makarov (1967).
Discrepancies among descriptions may result, at
least in part, from geographical variations in mor-
phology. The following synopsis is based on speci-
mens from off Hokkaido, Japan (Kurata 1964b). In
all described stages, shallow transverse groove in
carapace; dorsal spine on abdominal somite 3,
posterolateral spines on abdominal somite 5. Exo-
podite only on pereopod 1. In Stage I, antennal scale
with 11 setae, including 2 subterminal setae along
outer margin; endopodites of maxillipeds 1-3 with 4
segments; exopodites of maxillipeds jointed; fifth
pair of telsonic spines distinctly shorter than fourth
or sixth pairs. Length: Stages I-V, 1.9-5.0 mm.
Range: Prince Edward Island, Canada (Needier
1941); Beaufort, NC (Tesmer and Broad 1964);
an estuarine, subarctic boreal species, Sea of
Okhotsk (Makarov 1967); Hokkaido, Japan (Kurata
1964b); depth, 0-90 m, rarely to 440 m (Holthuis
1980).
Genus Mesocrangon Zarenkov
Largest larvae of Crangonidae with unabbreviated
development. From Stage III on, posterior margin of
telson straight or slightly concave.
Mesocrangon intermedia (Stimpson)
Five larval stages.
Stages I-V, from plankton; described as Sclero-
crangon intermedia by Makarov (1967); figure
24 in Makarov (1967).
In Stage I, antennal flagellum about half as long as
antennal scale; antennal scale with 11 setae; abdo-
minal somites 2-3 with keels; abdomen apparently
without spinules. Length: Stages I-V, 4.5-9.0 mm.
Range: Sea of Okhotsk to St. Lawrence Island (Ber-
ing Sea); depth, 18-180 m (Makarov 1967).
Genus Paracrangon Dana
In all described stages, rostrum long, spiniform,
spinulose, directed upwards about 45°; carapace
with denticulate anteroventral margin; basipodite of
maxilliped without subterminal seta; exopodites on
pereopods 1 and 2; exopodites of pereopods 1 and 2
with ^ 6 natatory setae; protopodite of antenna with
2 spines- one at base of flagellum, other a long spine
at base of scale.
Paracrangon echinata*^ Dana
At least 7 larval stages.
"A diagnostic character of adult Paracrangon is the absence of
pereopods 2 (Rathbun 1904). Kurata's (19fi4b) description of Pnni-
rrangon erhiriala shows pereopixi 2 fully (levelof)ed as late tLs the
seventh larval stage. Either Makarov's(19t>7) identification of these
larvae as P. fchmata is incorrect, or P. echimitu must have at least '.i
or 4 more larval stages before pereopod 2 becomes reduced or
absent.
282
HAYNES:PANI)A1,11)AK. HIl'I'OI.VTIDAE.ANDCRANCONIDAKLAKVAE
Stapes II, IV-VII, from plankton; tentatively iden-
tified as GlyphocrangoH sp. by Kuratii (19641));
figures 103-130 in Kurata (1964b).
Stages II and IV; Makarov (1967) based identity
on known distribution of adults and morphology
of embryo of Glyphocrangon granulofsLs (see
Bate 1888); figure 28 in Makarov (1967).
Most spinose of crangonid larvae known from
northern North Pacific Ocean (Fig. 10). Length:
Stage II, 5 mm; Stage VII, 13.8 mm. Range: Sea of
Japan; Okhotsk Sea; Port Etches, AK, to La Jolla,
CA; depth, 7-201 m (Butler 1980).
Genus Sabinea J. C. Ross
Probably 4 larval stages. In all described stages,
telson relatively wide, with shallow indentation;
pereopods 2-5 without exopodites.
Sahinea septemcarinata (Sabine)
Probably 4 larval stages.
Prezoeal telson and Stages I and III, probably
known parentage; Atlantic specimens: plate V,
figures 1-23, and plate VI, figures 1-13, in Sars
(1890).
Stages I and III, probably known parentage; de-
scribed as Crangon septemcarinatus by William-
son (1915); figures 167-172 in Williamson
(1915). Williamson's figures from Sars (1890).
Stages I and III, from plankton; figure 12, "last
stage" (= Stage III), in Birshteyn (1938).
Stage I (whole larva) and Stage III (telson); origin
of specimens not given; figures 1 and 2 in
Williamson (1960).
Stages and origin of specimens not given, de-
scribed as Myto gaimnrdi by Birshteyn (1938);
plate 7, figure 1 (Kr0yer 1846 in Birshteyn
1938).
In all described stages, anteroventral margin of
carapace with about 7 denticles. Abdominal somites
1-4 with 1, 2, 1, and 1 ventral spines, respectively;
abdominal somite 5 with posterolateral spine. Telson
with 16-1-16 setae in Stage 1, 13 -i- 13 setae in Stage
III. Length: Stages I-III, 7.7-11.5 mm. Range
area of Iceland and Faroe Islands (Williamson 1960)
Barents and Norwegian Seas (Williamson 1960)
Chukchi Sea (Birshteyn 1938); eastern coast of
North America from mouth of St. Lawrence River to
Massachusetts Bay; Arctic Ocean to Point Barrow
(Alaska), White Sea, and northern Europe (Williams
1974); depth, 10-240 m (Williams 1974).
0. 5 mm
Figure 10. -Dorsal view of body, Stage I zoea of
Para era ngon echinata.
Genus Sclerocrangon G. O. Sars
Not more than 2 larval stages. Appendages resem-
ble adult except uropods enclosed and pleopods not
fully setose. Pereopods without exopodites;
pereopods 4 and 5 have characteristic sickle-shaped
dactyli(Fig. 11).
Sclerocrangon horeas (Phipps)
Two larval stages.
Late embryo extracted from egg; plate VI, figures
14-28, in Sars (1890, as cited in Williamson
1960).
Stage not specified, known parentage (Makarov
1967). No figures.
Stage I and Stage II ("postlarval"), known parent-
age; figures 1-3 in Makarov (1968).
283
FISHERY BULLETIN: VOL. 83. NO. 3
1 , 0 mm
Figure ll.-Pereopod 4 or 5 of Sclerocrangan
larva with characteristic sickle-shaped daot\'l.
Larvae not free living but cling to pleopods of
female. In all described stages, carapace without
anteroventral denticles; flagellum of antennule
segmented; basal portion of antennule shaped as in
adult; maxillipeds with undeveloped exopodites; exo-
y)odites with a few feeble natatory setae; pereopods
segmented, without exopodites. In Stage I, rostrum
absent; carapace covers sessile eyes; telson and abdo-
minal somite 6 jointed. In Stage II, rostrum short,
triangular, flattened dorsoventrally. Length: Stage
I, 9.0 mm; Stage II, 11.5 mm. Range: Sea of Japan
to Chukchi Sea to Bare Island, WA; arctic Canada to
Cape Cod, MA; North Atlantic Ocean and arctic
Europe; Spitsbergen to Faroe Islands; depth, 0-366
m (Butler 1980).
Sclerocrangon salebrosa (Owen)
One larval stage.
Stage I, from plankton; figure 27 in Makarov
(1967).
Embryos, from female; Stage I and Stage II ("post-
larval"), from plankton; figures 1 and 2 in
Makarov (1968). Larvae from plankton identi-
fied by comparison with embryos dissected from
eggs.
Larvae free living. In Stage I, rostrum spiniform;
carapace with anteroventral denticles; exopodites of
maxillipeds fully developed, each exopodite with 5
natatory setae; telson exceptionally wide with 22 -t-
22 setae. Length: Stage I, 10.3-10.5 mm. Range:
Okhotsk Sea; Hokkaido; no depth range (Kurata
1964b; Makarov 1967).
Sclerocrangon zenkevitch't Birstein and Vinogradov
Only Stage I described, known parentage; figure 5
in Birshteyn and Vinogradov (1953).
Carapace nearly circular laterally, without ros-
trum; cephalothorax and abdomen without spines or
denticles; telson ovoid. Length: Stage I, 7.2 mm.
Range: Bering Sea; depth, 2,995-3,940 m (Birshteyn
and Vinogradov 1953).
BIOLOGY
Although pandalid, hippolytid, and crangonid lar-
vae are common inhabitants of the neritic mero
plankton of temperate and arctic waters of the North
Pacific Ocean, only a few studies on their biology
have been published. The most complete studies are
those of Haynes(1983), Makarov (1967), and Rothlis-
berg (1975). Haynes described the relative abun-
dance and distribution of pandalid shrimp larvae in
the lower Cook Inlet-Kachemak Bay area, Alaska;
Makarov (1967) described the distribution of decapod
shrimp larvae of the West Kamchatkan shelf; and
Rothlisberg (1975) discussed larval ecology oiPan-
dalus jordani off the Oregon coast. In this section, I
review the findings of these authors and supplement
their findings with information from the literature.
To avoid redundancy of citation, only information in
addition to that given by Haynes, Makarov, and
Rothlisberg is cited by author and date. This section
does not include every known facet of the biolog>' of
decapod shrimp larvae of the northern North Pacific
Ocean; however, more information can be acquired
from the papers of Haynes, Makarov, and Rothlis-
berg and from their bibliographies.
Areas of high abundance of Stage I larvae ap-
parently indicate areas where females are releasing
larvae. For example, in Kachemak Bay in 1972,
Stage I larvae of Pandalus borealis, P. goniunts, P.
hypsinotixs, and Pandaiopsis dispar were most abun-
dant in plankton samples collected in the same area
284
IIAVNKS. I'ANDAMDAl-:. llll'l'OLVTIDAK. AN1)CKAN(;()NIIIAK I.AKVAK
where females were releasing larvae (for these 4
species, females were releasing larvae at depths of
about 85, 35, 50, and 100 m, respectively, based on a
trawling survey).
Time of release of pandalid larvae varies with
species. In Kachemak Bay in 1972, Stage I larvae of
Panda Ins boreal i-x were not caught until the first half
of April; Stage I larvae of P. goniurus and P. hyp-
sinotus were caught later, in the latter half of April.
In British Columbia waters, P. borealis larvae are
also released earlier than larvae of either P. goni-
urus or P. hypsinotus (Berkeley 1930; Butler
1964).
Time of lar\'al release is also related to water
temperature. F^or example, a residual layer of
relatively cold (sometimes subzero) water remains on
the central West Kamchatkan shelf at a depth of
50-150 m throughout the summer. Decapods living in
this layer of cold water release their larvae later than
decapods living in warmer waters to the north and
south. In the western North Atlantic Ocean, pan-
dalid shrimp also release their larvae later in colder
waters than in warmer waters (Haynes and Wigley
1969).
Depth distributions of larvae of P. borealis and P.
goniurus in Kachemak Bay, 1972, were usually
similar. Few larvae were in the 0-10 m stratum; most
were between about 10 and 40 m. The abundance of
larvae remained relatively constant below about 50
m. Numbers of Stage I P. borealis larvae, however,
increased below about 70 m, possibly reflecting their
recent release. These depth distributions differ from
the depth distribution of P. jordani off the Oregon
coast. Younger (Stages V-X) P. jordani larvae were
found closer to the surface (0-10 m stratum) than
older (Stages XI-XV) larvae (to 160 m).
Water temperature has profound effects on larval
survival, growth, and size at metamorphosis. For ex-
ample, survival of P. jordani larvae (Stages I-III) is
markedly less at 17° than at 5°C. For the oldest
stage (Stages IX-XIII), the relation between survival
and temperature is reversed, and survival is lowest
at 5°C (Rothlisberg 1979). For larvae of P. platy-
ceros, survival is reduced by sudden changes in
temperature, particularly about 20 °C and below 9°C
(Wickins 1972). At a given temperature (range
5°-14°C), growth increments for all larval stages of
P. jordani decrease with increasing size; however,
the higher the temperature, the more rapid the
molting frequency (Rothlisberg 1979).
Shrimp larvae can probably influence the direction
and extent of their dispersal. For instance, in Kache-
mak Bay, 1972 and 1976, pandalid shrimp larvae
were released in the central portion of the outer bay.
Some of these larvae were carried northward out of
the bay in the direction of the current, but others
were dispersed southwestward in a direction op-
posite the current. In the southern area of the
western Kamchatka shelf, Crangon larvae released
close to shore with larvae of other species, such as
king crab, Paralithodes camtschatica, remained close
to shore. Larvae of the other species, however, were
carried seaward. In the northern area of the western
Kamchatka shelf, where currents are faster than in
the southern area, Crangon larvae were carried
seaward (Makarov 1967). The causes for dispersal of
larvae against known water currents are unknown,
but dispersal may be dependent, at least in part, on
the swimming capability of the larvae.
Some pandalid shrimp larvae migrate vertically in
a diel cycle. In Kachemak Bay in 1972, Stages I and
II larvae of P. borealis and P. goniurus were most
abundant between the surface and 15 m during low
light levels (1800-0800 h); however, during high light
levels (1000 and 1600 h), they were most abundant
between 30 and 60 m. Although present, a pro-
nounced thermocline did not prevent larvae from
moving vertically. Whether later stages of P.
borealis and P. goniurus migrate similarly is
unknown; however, in waters off Oregon, only
Stages XII-XVI larvae of P. jordani migrate ver-
tically in a diel cycle. During the day, these P. jor-
dani larvae are distributed from the surface to 1 50 m
by age: the deeper the water, the older the lar\'ae. At
night, P. jordani larvae migrate upwards in the
water column, and the stages remain somewhat
uniformly distributed with depth.
Foods of pandalid larvae have been determined
during attempts to rear the larvae in the laboratory
and from examination of shrimp stomachs. Larvae of
P. jordani and P. platyceros have been reared on
brine shrimp, A rtemia salina nauplii (Modin and Cox
1967; Lee 1969; Price and Chew 1972), P. hypsino-
tus larvae have been reared on brine shrimp nauplii
and algae (Haynes 1976), and P. kessleri larvae have
been reared on small pieces of crab, shrimp, and
mussel tissue (Kurata 1955). In 1976, I made a
preliminary study (unpublished) on foods eaten by
pandalid shrimp larvae in Kachemak Bay by examin-
ing their gut contents. The larvae mostly ate
diatoms, especially Coscinodisais types, and larval
crustaceans. Many of the guts also contained black
pigment and ommatidia. The assumption that pan-
dalid larvae feed on eyes of other decapod larvae was
subsequently confirmed when I observed a P.
borealis zoea ingesting the eye of a live king crab
zoea. Calcareous fragments (probably molluscs),
coccolithophores, spines of larval echinoderms, and
285
FISHERY BULLETIN: VOL. 83, NO. :i
bits of diatoms have been found in guts of Pandalus
larvae from European waters (Lebour 1922).
Some species of pandalid larvae are sustained by
their internal yolk for several days after hatching
without feeding; others must feed immediately after
hatching or die. Pandalus platyceros larvae can live
11-13 d on stored yolk with no food (Price and Chew
1972); however, when food is offered, they feed
immediately after hatching. In Price and Chew's
(1972) study, the starved larvae ate their dead rela-
tives, but did not actively prey on them. Larvae of P.
jordani, however, if not fed soon after hatching,
starve and die regardless of later increases in prey
concentrations (Modin and Cox 1967). In another
study, 40% of Stage I zoeae of P. borealis without
prey died in 5 d, and 100% died in 13 d (Paul et al.
1979).
The relationship between food and survival in cap-
tivity has been determined for some North Pacific
Ocean larvae; however, little is known about this
relationship in nature. For instance, year-class
strength may be influenced or even largely deter-
mined by the quality and quantity of food available
during the larval period. Unfortunately, there is vir-
tually no information on the t\T3es and quantities of
food needed for survival of shrimp larvae in nature.
Until this information is available, the relation be-
tween food and survival of shrimp larvae at sea will
remain unknown.
ACKNOWLEDGMENTS
Donald I. Williamson of the University of Liver-
pool, England, and T. H. Butler of the Pacific
Biological Station, Nanaimo, British Columbia, read
an earlier version of this paper and offered valuable
suggestions for improvement.
LITERATURED CITED
Bate, C. S.
1888. Report on the Crustacea Marrura dredged by H.M.S.
Challenger during the years 1873-1876. Rep. Sci. Results
Voyage H.M.S. Challenger, Zool. 24, 942 p.
Berkeley, A. A.
1 930. The post-embryonic development of the common panda-
lids of British Columbia. Contrib. Can. Biol. Fish., New Ser.
6(6):79-163.
BlR-SHTEYN, YA. A.
1938. Zemetka o Decapoda iz Planktona, Sobrannogo vo
Vremya Plavaniya Ledokolov Sadko i Litke v Arktike.
(Decapoda from plankton collected during voyages of the ice-
breakers Sadko and Litke in the Arctic.) |In Russ.J Byull.
M. 0-Va Isp. Frirody Otd. Biol. 47(3): 199-209. (Translated
by A. L. Peabody, agency unknown, available from author,
15 p.)
BiRSHTEYN, Ya. A. AND L. G. VINOGRADOV.
1953. Novyye Dannyye po Faune Desyatinogikh Rakoobraz-
286
nykh (Decapoda) Beringova Morya. [New data on the Deca-
poda of the Bering Sea.] [In Russ., Engl. Summ.) Zool. Zh.
32:215-228. (Translated by Lang. Serv. Div., Natl. Mar.
Fish. Serv., NOAA. Wash., D.C., 20 p.)
Bull, H. 0.
1939 The newly-hatched larva of Spirnvtocarif: iniswla
(Kroyer). Rep. Dove Mar. Lab. (3). 6:43-44.
Butler. T. H.
1964. Growth, reproduction, and distribution of pandalid
shrimps in British Columbia. J. Fish. Res. Board Can. 21:
1403-1452.
1980. Shrimps of the Pacific Coast of Canada. Can. Bull.
Fish. Aquat. Sci. 202, 280 p.
Frost, N.
1936. Decapod larvae from Newfoundland waters. Div. Fish.
Res., Newfoundland, Rep. Faun. Ser. 1:11-24.
GURNEY, R.
1942. Larvae of decapod Crustacea. Ray Soc. (Lond.) Publ.
129, 306 p.
Hayashi, K.-L
1977. Studies on the hippolytid shrimps from Japan- VI. The
genus Spirontocaris BATE. J. Shimonoseki Univ. Fish. 25:
155-186.
Haynes, E.
1976. Description of zoeae of coonstripe shrimp, Fnndalns
hypainotus, reared in the laboratory. Fish. Bull., I'.S. 74:
323-342.
1978a. Description of larvae of the humpy shrimp, PaxdaluK
goniurus, reared in situ in Kachemak Bay. Alaska. Fish.
Bull., U.S. 76:235-248.
1978b. Description of larvae of a hippolytid shrimp, Lrbbms
groevlnndicus, reared in situ in Kachemak Bay. Alaska.
Fish. Bull.. U.S. 76:457-465.
1979. Description of larvae of the northern shrimp, Pandalu-n
borealis, reared in situ in Kachemak Bay, Alaska. Fish.
Bull.. U.S. 77:157-173.
1980a. Larval morphology of Pnndalu,^ trideri.f and a sum-
mary of the principal morphological characteristics of North
Pacific pandalid shrimp larvae. Fish. Bull., U.S. 77:625-640.
1980b. Stage I zoeae of a crangonid shrimp, Crangon fnni-
riscorum anguj-ttimann, hatched from ox'igerous females
collected in Kachemak Bay, Ala.ska. Fish. Bull., U.S. 77:
991-995.
1981. Early zoeal stages ai Lehhe^is polaris, Eunhts surklei/i.
E. fahricii, Spirontocaris arruatn. S. (trhotensis. and Heptn-
carpus camtschaticus (Crustacea, Decapoda, Caridea, Hippo
lytidae) and morphological characterization of zoeae of
Spirontocaris and related genera. Fish. Bull., U.S. 79:
421-440.
1983. Distribution and abundance of larvae of king crab,
Paralithodes camtschatica, and pandalid shrimp in Kachemak
Bay, Alaska, 1972 and 1976. U.S. Dep. Commer., NOAA
Tech. Rep. NMFS SSRF-765. 64 p.
In press. Description of early stage zoeae of Spirontocaiis
wurdochi (Decapoda, Hippolytidae) reared in the laboratory.
Fish. Bull., U.S. 82:523-527.
Haynes, E. B., and R. L. Wigley.
1969. Biology of the northern shrimp, Pandalus borealis, in
the (kilf of Maine. Trans. Am. Fish. Soc. 98:60-76.
HOLTHUIS, L. B.
1947. The Decapoda of the Siboga Expedition. Part IX. The
Hippolytidae and Rhynchcx;inetidae collected by the Siboga
and Snellius Expeditions with remarks on other species.
Siboga Exped. 140, Monogr. 39a'*, 100 p.
1976. The identities of Pandalus gracilis Slimpson, 1860, and
Pandalus prensor Stimpson, 1860 (Decapoda, Pandalidae).
«
HAVNLS: I'ANDALIDAE. Hll'l'OI.Y'l'lliAK. ANDCKANCOMDAK l.AKVAK
Cnistaceaiia .S():4[491-r)4 .
1980. Shrimps and prawns of thf world, an annotated cata-
lo^e of species of interest to fisheries. Vol. 1 , FAO species
cataloKiio. FAO Fish. Syn. 125, FIR/SI 25 Vol. 1, 271 p.
Internationai, Commission on Zooiak;ic:ai, Nomknclaturk.
1964. International ccxle of zoological nomenclature, adopted
at the XV International Congress of Zoology. Int. Tnist
Zool. Nomen., Lond., 176 p.
IVANOV, B. G.
196,5. A description of the first larvae of the far-eastern
shrimp (Piiiid(du,s i^otiiurn-t). [In Riiss., Kngl. summ.| Zool.
Zh. 44:1255-1257. (Translated by U.S. Dep. Commer.,
NOAA. Natl. Mar. Fish. Serv., Off Int. Fish. Aff., Code No.
F44.)
1968. Lichinki Nekotorykh Dal'nevstochnykh Krevetok
Semeystva Crangonidae (Crustacea, Decajioda). (Larvae of
certain far eastern shrimps of the family Crangonidae (Crus-
tacea, Decapoda).] |In Russ., Engl, summ.] Zool. Zh. 47:
534-540. (Translated by A.L. Peabody, agency unknown,
available from author, 8 p.)
1971. The larvae of some eastern shrimps in relation to their
taxonomic status. |In Russ., Engl. summ.]. Zool. Zh. 50:
657-665. (Translated by U.S. Dep. Commer., NOAA, Natl.
Mar. Fish. Serv., Off Int. Fish. Aff, Code No. F44.)
KOBJAKOVA, Z. I.
1937. Systematisch Uebersicht der Dekapoden aus dem Ocho-
tskischen und Japanischen Meere. Uchenie Zapiski Leningr.
Univ.. (15). (). 93-154. [Not seen by author, cited in Hayashi
1977.1
KR0YER, H.
1846. Karcinologiske Bidrag. Naturhist. Tidsskrift. (Kroyer
et Schiodte), Ser. 2, Bd. 1. [Not seen by author, cited in
Birshteyn 1938.|
1861. Pp. 63-69 in Naturhist. Tidsskrift., Ser. 3, Vol. 1.,
Copenhagen. [Not seen by author, cited in Stephensen
1935.)
Kl'RATA, H.
1955. The post-embryonic development of the prawn, Pnnda-
liix kesslen. Bull. Hokkaido Reg. Fish. Res. Lab. 12:1-15.
1964a. Larvae of decapod Crustacea of Hokkaido. 3. Panda-
lidae. Bull. Hokkaido Reg. Fish. Res. Lab. 28:23-34.
(Translated by Fish. Res. Board Can., 1966, Transl. 693.)
1964b. Larvae of decapod Crustacea of Hokkaido. 4. Crango
nidae and Glyphocrangonidae. Bull. Hokkaido Reg. Fish.
Res. Lab. 28:35-50.
Ki!Ris, A. M., AND J. T. Carlton.
1977. Description of a new species, Crarigor^ hatidi. and new
genus Lissorrnruion, of crangonid shrimps (Crustacea:
Caridea) from the California coast, with notes on adaptation
in body shape and coloration. Biol. Bull. (Woods Hole) 153:
540-559.
Lebohr, M. V.
1922. The food of planktonic organisms. J. Mar. Biol. Assoc.
U. K. 12:644-677.
1930. The larval stages of Caridimi, with a description of a
new species. C. utevetii. Proc. Zool. Soc. Lond., p. 181-194.
1931 . The larvae of the Plymouth Caridea. I. The larvae of the
Cragonidae. II. The larvae of the Hippolytidae. Proc. Zool.
Soc. Lond., [). 1-9.
1936. 6. Notes on the Plymouth species of Spircmtocaris
(Crustacea). Proc. Zool. Soc. Lond., p. 89-104.
1937. The newly hatched larva of Spirontocari-t; spinus
(Sowerby) var. lilljeborgi Danielssen. J. Mar. Biol. Assoc.
U. K. 22:101-104.
1940. The larvae of the British sf)ecies oi Spirontocarix and
their relation to Thor (Crustacea Decapoda). J. Mar. Biol.
Assoc. U. K. 24:50.5-514.
Lee, Y. J.
1969. Larval development <if pink shrimp, Pandalius jordani
Rathbun, reared in laboratory. M.S. Thesis, Univ. Washing-
ton, Seattle, 62 p.
LovELAND, H. A., Jr.
1968. Larval development under laboratory conditions of
Crangon aUuikeri.vus Rathbun, (Crustacea: Decap(Kia). M.A.
Thesis, Walla Walla Coll., Washington, 22 p.
Makarov, R. R.
1967. Larvae of the shrimps and crabs of the West Kamchat-
kan shelf and their distribution (Lichinki krevetok, rakov-
otshel'nikov i krabov zapadnokamchatskogo shel'fa i ikh
respredelenie). Translated from Russian by B. Haigh, Natl.
Lending Libr. Sci. Technol., Boston Spa, Yorkshire, Engl.,
199 p.
1968. On the larval development of the genus Sckrocrangon
G. 0. Sars (Caridea, Crangonidae). Crustaceana Suppl.
2:27-37.
MiKULiCH, L. v., and B. G. Ivanov.
1983. The far-eastern shrimp Pandalus prensor Stimpson
(Decapoda, Pandalidae): description of laboratory reared
larvae. Crustaceana 44:61-75.
MoDiN, J. C, and K. W. Cox.
1967. Post-embryonic development of laboratory-reared ocean
shrimp, Pandalm jordani Rathbun. Crustaceana 13:197-
219.
Needler, a. B.
1934. Larvae of some British Columbian Hippolytidae.
Contrib. Can. Biol. Fish., New Ser. 8:237-242.
1938. The larval development of Pandahis stenolepis. J.
Fish. Res. Board Can. 4:88-95.
1941. Larval stages oiCrago septemspinosus Say. Trans. R.
Can. Inst 23:193-199.
Paul, A. J., J. M. Paul, P. A. Shoemaker, and H. M. Feder.
1979. Prey concentrations and feeding response in laboratory-
reared stage-one zoeae of king crab, snow crab, and pink
shrimp. Trans. Am. Fish. Soc. 108:440-443.
Pike, R. B., and D. I. Williamson.
1961. The larvae oi Spirontocaris and related genera (Deca-
poda, Hippolytidae). Crustaceana 2:187-208.
1964. The larvae of some species of Pandalidae (Decapoda).
Crustaceana 6:265-284.
Price, V. A., and K. K. Chew.
1972. Laboratory rearing of spot shrimp larvae (Pandalus
platyceros) and descriptions of stages. J. Fish. Res. Board
Can. 29:413-422.
Rathbun, M. J.
1902. Descriptions of new decapod crustaceans from the west
coast of North America. Proc. U.S. Nat. Mus. 24:885-905.
1904. Decapod crustaceans of the northwest coast of North
America. In C. H. Merriam (editor), Alaska: the Harriman
Expedition, Vol. 10, Crustaceans, p. 1-210. Doubleday. N.V.
(Also published in 1910 as a Smithson. Inst., Harriman
Alaska Ser. 10 (Publ. 1897).)
Rothlisberg, p. C.
1975. Larval ecology of Pandalus jordani Rathbun. Ph.D.
Thesis, Oregon State Univ.. Corvallis, 104 p.
1979. Combined effects of temperature and salinity on the
survival and growth of the larvae of Pandalus jordani (Deca-
poda: Par\da.Mae). Mar. Biol. (Berl.) 54:125-134.
1980. A complete larval description of Paiuialus jordani
Rathbun (Decapoda, Pandalidae) and its relation to other
members of the genus Pandalus. Crustaceana 38:19-48.
Sars, G. 0.
1890. Bidrag til kundskaben om Decapodernes Forvandlinger.
287
FISHERY BULLETIN: VOL. 83. NO. 8
in. Crangonidae. Arch. Math. Naturv. 104:132-195.
1900. Account of the postembryonal development of Pandalus
horealia Kr?iyer with remarks on the development of other
Pandali. and description of the adult Pandaluii borealia.
Rep. Norw. Fish. Mar. Invest. 1:1-45.
Squires. H. J.
1965. Larvae and megalopa of Arffiti dentata (Crustacea:
Decapoda) from Ungava Bay. J. P'ish. Res. Board Can. 22:
69-82.
Stephensen. K.
1912. Report on the Malacostraca collected by the "Tjalfe"-
Expedition, under the direction of cand. mag. Ad. S. Jensen,
especially at W. Greenland. Viden.sk. Medd. Dan. Naturhist.
Foren. Kbh. 64:57-134.
1916. Zoogeographical investigation of certain fjords in
southern Greenland, with special reference to Crustacea,
Pycnogonida and Echimxlermata including a list of Alcyo-
naria and Pisces. Medd. Gr0nl. 53:230-378.
1935. Crustacea Decapoda. The Godthaab Expedition 1928.
Medd. Gr(>nl. 80:1-94.
Tesmer. C. a., and a. C. Broad.
1964. The larval development of Crangon septemspinosa
(Say). Ohio J. Sci. 64:239-250.
WlCKINS, J. F.
1972. Experiments on the culture of the spot prawn Pandahis
platyreros Brandt and the giant freshwater prawn Mncro-
brackium rosenbergii (de Man). Fish. Invest., Minist.
Agric. Fish. Food (G.B.) Ser. 2, 27(5), 23 p.
Williams, A. B.
1974. Marine flora and fauna of the northeastern United
States. Crustacea: Decapcxia. U.S. Dep. Commer., NOAA
Tech. Rep. NMFS Circ.-389, 50 p.
Williamson, D. I.
1957a. Crustacea, Decapoda: Larvae V. Caridea, Family
Hippolytidae. Fiches Identif Zooplancton 68. 5 p.
1957b. Crustacea. Decapixia: Larvae I. tleneral. Fiches
Identif. Zooplancton 67, 7 p.
1960. Crustacea, Decapoda: Larvae VII. Caridea. Family
Crangonidae, Stenopodidea. F"iches Identif Zooplancton 90,
5 p.
1969. Names of larvae in the Decapoda and Euphausiacea.
Crustaceana 16:210-213.
1982. Larval morphology and diversity. In L. (i. Abel
(editor). The biology of Cnistacea. Vol. 2. Embryology,
niorpholog>', and genetics. |i. 4.'M10. Acad. Press. N.V.
Williamson, H. C.
1915. Decapoden. I. Teil (Larven). Nordisches plankton IS:
315-588. (Also published in Nordisches plankton, Zoolo-
gischer teil, Dritter Band: Crustacea, p. 315-588. Verlag von
Lipsius and Tischer, Lepzig 1927, and by Neudruck A.
Asher Co., Amsterdam 1964.)
Zarenkov, N. a.
1965. Revision of genera Cramjon fiihrinns and Sclrnirnn/-
gon G. (). Sars (Decapoda. Crustacea). |In Russ.. Engl.
summ.] Zool. Zh. 44:1761-1775. (Translated from Russian.
Fish. Res. Board Can. Transl. Ser. 1465. 43 p.)
288
WITHIN-SEASON DIFFERENCES IN GROWTH OF
LARVAL ATLANTIC HERRING, CLUPEA HARENGUS HARENGUS
Cynthia Jones'
ABSTRACT
Data (il)laitic'il from two previous studies of larval Atlantic herrinj^ Kff'Wth were compared, based on otolith
intremeiU estimated age. These data, from the Gulf of Maine in 1976-77 and 1978-79, supported the
hypothesis that larvae hatched early in the spawning season grew faster than larvae hatched late. Differ-
ences were siffnificant under assumptions that increments were deposited in the otolith either daily or at 0.5
increments per day. Corroborative evidence indicated that otolith increments were formed daily at least dur-
in.u; the early part of the spawning season.
The otolith increment technique has been used to
estimate age and growth in field-caught larval Atlan-
tic herring, Clupea harengus harengus, in the Gulf of
Maine by Townsend and Graham (1981) and by
Lough et al. (1982). Use of the increment technique
to estimate age usually assumes daily deposition of
otolith increments. Uncertainty exists, however,
regarding increment deposition rates in the otoliths
of larval herring. Gjosaeter (1981) and 0iestad
(1982) have observed daily increment deposition. In
contrast, Geffen (1982) found that increment deposi-
tion can be variable and a function of growth rate in
larval herring, underscoring the problem in simply
assuming that increments occur daily under field
conditions. Growth calculations based on assump-
tions of daily increment deposition in populations
that experience variable increment deposition rate
would result in inaccurate estimates of growth rates.
In most cases where otolith increment deposition has
been tested under suboptimal conditions, the deposi-
tion rate has been found to be nondaily (for review
see Jones 1984). Estimates of growth rates can be
made, however, by expressing growth based on
increment counts and with the use of corroborative
evidence to determine periodicity of increment
deposition.
Das (1968) found that growth rates of larval Atlan-
tic herring, measured by following the progression of
length modes over time, were different within a
spawning season. He stated that early-spawned lar-
vae grew faster than late-spawned larvae and model-
ed growth with curvilinear functions. Townsend and
Graham (1981) also reported two different growth
'Graduate School of Oceanography, University of Rhode Island,
Kingston. RI 02882-1197; present address: Department of Natural
Resources, Fernow Hall, Cornell University, Ithaca, NY 14853.
rates for Atlantic herring, one for larvae born prior
to November 5 and one for larvae born later. Each
group was modeled by two regression lines to
emphasize that growth ceased in January and resum-
ed in February. In their study, early- and late-
hatched groups were analyzed separately and the
comparison of growth between larvae hatched early
versus late in the season was not statistically
verified.
This paper uses otolith increment data from Town-
send and Graham (1981) and from Lough et al.
(1982) to compare early-season versus late-season
larval Atlantic herring growth. The comparisons are
made using the assumptions of both daily and non-
daily otolith increment deposition.
METHODS
Raw data for otolith counts and larval fish lengths
used in these studies were obtained from Gregory
Lough of the National Marine Fisheries Service,
Northeast Fisheries Center, Woods Hole, MA, and
from Joseph Graham and David Townsend of the
Maine Department of Marine Resources, Boothbay
Harbor, ME. Both data sets were used in the detec-
tion of within-season differences in growth rates.
Although the study of Lough et al. (1982) encom-
passed a larger area, only data from the Gulf of
Maine were included in the analysis (Table 1), in
order that comparisons were made within the same
area as for Townsend and Graham (1981). Methods
employed for the collection of data were reported by
Lough et al. (1982) and by Lough and Bolz (1979) for
the 1976-77 data and by Townsend and Graham
(1981) for the 1978-79 data.
For each season (1976-77, 1978-79), data were
analyzed in three ways:
Manuscript accepted October 1984.
FISHERY BULLETIN: VOL. 83. No. 3, 1985.
289
FISHERY BULLETIN: VOL. 83. NO. 3
TABLE 1. — Station information for Atlantic fierrlng samples
from tfie Gulf of Maine area for the fall and winter of 1976-77
sampling program. (Data from Lough et al. 1982.)
Vessel
Cruise
No.
Stn.
Time
Lat. Long. (Night
N W Date or Day)
Annandale 76-01
Researcher 76-01
Mt. Mitchell 77-01
38 43°37' 69°22' 8 Oct. 0300 (N)
44 43°44' 68°50' 8 Oct. 1415(D)
59 44°25' 67°35' 9 Oct. 1515(D)
65 44°36' 67°07' 13 Oct. 0330 (N)
102 42°58' 70°00' 8 Dec. 1030 (N)
105 43°30' 69°30' 9 Dec. 1100 (N)
122 43°14' 70°01' 24 Feb. 1620(D)
123 43°00' 70°15' 24 Feb. 1933(D)
1) Hatch date was calculated on the assumption
of daily increment deposition, and all data
were considered.
2) Hatch date was calculated on the assumption
of daily increment deposition only with larvae
which had 60 or fewer increments included for
analysis. This was done to determine whether
growth differences were present in the earlier
months of life. Also, since the range of incre-
ment counts for the late-hatched larvae from
1976 to 1977 was greater than for early-hatch-
ed larvae, use of a truncated data set resulted
in more valid comparisons.
3) Hatch date was calculated on the assumption
of nondaily deposition (0.5 increment/d).
Date of hatching was calculated by subtracting the
estimated age of each larva from its date of capture.
This calculation, of course, depends on how age was
estimated. According to the Lough et al. (1982) cal-
culation, a larva with 10 otolith increments would be
29 d old: 22 d for the first 3 increments, plus 7 d to
lay down the next 7 increments. According to the
assumptions used by Townsend and Graham (1981),
a larva with 10 otolith increments would be 15 d old,
assuming that increment deposition began 5 d after
hatch, and was daily thereafter. There is a difference
of 14 d between these two estimates of age, and,
therefore, estimated day of hatch. This does not af-
fect the regression analysis, as long as the indepen-
dent variable used is increment count, not age.
The range of possible hatch dates for each in-
dividual was also calculated, based on the considera-
tion that deposition rates could vary from 0.5 to 1.0
increment/d (after Geffen 1982). Age could be equal
to the number of increments plus a constant (5 d) or
up to twice the number of increments plus a constant
(5d).
Larvae were classified as either early- or late-
hatched within the spawning season. For 1976-77
the early-late division date was placed at the discon-
tinuity in the frequency of hatching plot, which also
occurred at the midpoint in the spawning cycle. Divi-
sion date for the 1978-79 data set was placed at
approximately the division of Townsend and Graham
(1981) which they felt represented two different
groups of larvae.
For analysis of nondaily deposition, the data were
partitioned to insure that there could be no overlap
of early- and late-hatched classification of larvae,
assuming deposition ranged from daily deposition to
deposition of one increment every 2 d. Any late-
hatched larva whose possible range of hatch dates
overlapped the division date (for early-hatched vs.
late-hatched classification) was eliminated from
analysis. This resulted in a loss of data (e.g., the fish
whose possible hatch date overlapped the division
date) and decreased the ability to detect differences.
Ordinary least squares linear regressions were fit
to each data set. Bartlett's test for homogeneity of
variance (Ostle and Mensing 1975) was applied to the
data before each analysis. After regressions were fit,
the residuals of length were plotted against pre-
dicted length and examined for trends (Draper and
Smith 1981). F-tests (Ostle and Mensing 1975) were
applied to paired linear regressions, early-hatched
versus late-hatched, to determine whether the slopes
were significantly different. This test showed
whether the data were better fit by two lines, one for
early-hatched and one for late-hatched larvae, or
whether a single regression line was preferable. In
the regression plots the change in length is express-
ed in millimeters per increment.
The von Bertalanffy growth equation.
L, = L^(1
■k{t-l
0))
was also fitted to the data, using the nonlinear
regression procedure (NLIN) within SAS (Statistical
Analysis Systems, SAS Institute, Gary, NC). Esti-
mates of the parameters {K, L^, ^,) of the von Ber-
talanffy equations for early- and late-hatched larvae
were compared with a Fisher-Behrens test (Hoenig
1982) to determine whether the vector of parameter
estimates from the two classifications was signifi-
cantly different.
RESULTS
Linear regression models fitted to larval length-at-
increment count data showed significant differences
between larvae hatched early and late in the spawn-
ing season. Larvae hatched early had achieved
greater length at a given increment count than those
290
JONES: niKFKKKNCKS IN I,AK\AI, IIKKKINC CKOW'I'II
hatched later. Intercepts were not compared since
the data sets did not contain any larvae with fewer
than seven increments and inferences outside the
range of the data should not be drawn.
1976-77 Study
A frequency plot of hatching dates for the Gulf of
Maine stations is shown in Figure 1 for age esti-
mated on the assumption of daily ring deposition and
in Figure 2 for age estimated on the assumption that
deposition was daily or as little as one ring every
other day.
Differences in length-at-increment count between
early- and late-hatched larvae was striking (Table 2).
Regression plots are shown in Figure 3. Analysis of
the data confirmed that the length-at-count data
were modeled more accurately by two different
regression lines (P < 0.01) and that the slopes of
these two regressions were significantly different (P
LARVAL HERRING
1976-1977 STUDY
15-1
UJ
<
>
% 10
GC
UJ
m
z
o^
SEPT 1
1
SEPT 1
"^
OCT 1
NOV
OCT
NOV 1
DEC 1
DATE OF HATCHING
Figure 1 . - Frequency of Atlantic herring hatching during the 1976-77 study. Upper scale gives the day of hatch based on
the Lough et al. (1982) aging method, or, as discussed in the text. Lower scale gives the day of hatch based on Townsend
and Graham's (1981 ) aging method as discussed in the te.xt. Arrow indicates division point between early- and late-hatched
classification.
Table 2. — Regression analysis of 1976-77 Gulf of Maine Atlantic herring data.
et al. 1982.)
(Data from Lough
Otolith
Hatch
Slope
Standard
Probability
Probability
increment
classifi-
Sample
regression
error
intercepts
slopes
count
cation
size
Intercept
line
of slope
R'
equal
equal
All data
Early
117
9.4
0.3284
0.0172
0.76
<0.01
<0.01
Late
64
15.8
0.0948
0.0047
0.87
60 or fewer
Early
117
9.4
0.3284
0.0172
0.76
<0.01
<0.01
Late
44
14.6
0.1470
0.0274
0.41
Data were classified Into early- and late-hatched larvae. These two groups were compared
by fitting ordinary least squares regression lines to 1) all the data within the two classifications,
and 2) using only lengths from larvae with 60 or fewer increment counts. Slopes and intercepts
were compared between early versus late for each group.
291
FISHERY BfLLETIN: VOL. 83. NO. 3
LARVAL HERRING
1976- 1977
15-1
LU
<
>
DC 10
<
cc
LU
CO
INCREMENT EVERY 2 DAYS
o 0 DAILY DEPOSITION
\ I \ \ r
MAY 1 JUN 1 JUL 1 AUG 1 SEP
OCT 1
I \ \ \ f-
MAY 1 JUN I JUL 1 AUG 1 SEP
DATE OF HATCHING
NOV
OCT 1
NOV
Figure 2. -Frequency of Atlantic herring hatching during the 1976-77 study, calculated under two assumptions of
otolith increment count and age relationship.
< 0.01). The average length achieved per increment
was 0.33 mm and 0.10 mm for early- and late-hatch-
ed larvae, respectively. Bartlett's test confirmed that
variances were homogeneous. Analysis of residuals
showed that the last three residuals, corresponding
to the three largest larvae, were below the average.
The exclusion of these points did not alter the results
of the analysis.
Analysis of the subset of larvae with fewer than 60
increments (Table 2) showed that data were better
fitted with two different regression lines {P < 0.01)
and that the slopes were significantly different {P <
0.01). Regression plots are shown in Figure 4.
Change in length of early-hatched larvae was 0.33
mm/increment and 0.15 mm/increment for late-
hatched larvae. Bartlett's test showed variances to
be homogeneous and residuals showed no trends, ex-
cept for the two youngest late-hatched larvae which
fell below the regression line. Late-hatched larvae
were slightly larger than early-hatched larvae for the
lowest increment counts.
Differences in length-at-increment count were
apparent for data whose calculated hatch dates in-
cluded deposition rates of from 0.5 to 1.0 incre-
ments/d (Table 3). The change in length of early-
hatched larvae was 0.33 mm/increment compared
with 0.17 mm/increment for late-hatched larvae.
Data were again better fit with two regression lines
(P < 0.01) whose slopes were significantly different
(P < 0.01).
The von Bertalanffy growth equation fit the late-
hatch larval data well (Table 4). L^ was estimated at
29.81 mm, with a 95% confidence interval of 26.41
to 33.22 mm. Fit to the early-hatched larval data was
poor. L^ was estimated at 35.59 mm, with a con-
fidence interval of 17.76 to 53.41 mm. These data
were adequately fit with a straight line, and there is
little justification for fitting with a curvilinear func-
tion other than it has been traditionally used for
adult fish. Beverton and Holt (1954), however,
stated that the von Bertalanffy equation should not
necessarily be used during the early life stages.
Nevertheless, when the parameter estimates from
the two curves were compared, they were signifi-
FlGURE 4. -Regression plot of length-at-otolith increment count for
Atlantic herring. Only lengths for larvae with 60 or fewer otolith
increments have been included for analysis. Data from Lough et
al. (1982).
292
JONES: DIKKKRENCES IN LARVAL HKKKlNCCKOWI'll
30
25
E
E
X
I- 20H
o
z
UJ
15-
10-
LARVAL HERRING GROWTH
1976-1977 STUDY
l^m.--^
A
1 AA
A A
A A A
TIME OF HATCH
EARLY •
LATE A
0
20
40 60 80 100
INCREMENT COUNTS
-1 \ I \ 1
120 140
Figure 3. - Regression plot of length-at-otolith increment count for Atlantic herring. Complete data set represented. Data from Lough et al.
(1982).
25-1
E 20 -
E
I
I-
O
z
LU
-I 15H
10^
LARVAL HERRING GROWTH
1976-1977 STUDY
TIME OF HATCH
EARLY •
LATE A
10
n \ \ r
20 25 30 35
INCREMENT COUNTS
40
45
50
293
FISHERY BULLETIN: VOL. 83, NO. 3
Table 3. — Regression analysis of 1976-77 Gulf of Maine Atlantic herring data based on two otolith
increment deposition assumptions. (Data from Lough et al. 1982.)
Otolith
increment
count
Hatch
classifi-
cation
Sample
size
Intercept
Slope of
regression
line
Standard
error
of slope
R'
Probability
intercepts
equal
Probability
slopes
equal
All data
Early
Late
117
39
9.4
14.2
0.3284
0.1711
0.0172
0.0364
0.76
0.37
<0.01
<0.01
Legend: Data were classified into early- and late-hatched larvae. Two dates of hatch were calcu-
lated: 1) Age equalled increment count plus a constant, and 2) age equalled twice the increment
count plus a constant. This resulted in a range of potential hatching dates. Any late-hatched larva
whose range of hatch date overlapped the division date (Text Fig. 1) was eliminated from the
analysis.
Table 4.— Estimation of von Bertalanffy growth parameters for larval Atlantic her-
ring from the Gulf of Maine.
Hatch
classi-
Para-
Estimate
of
Standard
error of
95% confide
nee interval
Year
fication
meter
parameter
estimate
Low
High
1976-77
Early
K
0.01865
0.00939
0.00008
0.03723
L^
35.6
9.0
17.8
53.4
h
-12.3
S.OOj
-22.2
-2.41
Late
K
0.01530
0.00457
0.00616
0.02443
Loo
29.8
1.7
26.4
33.2
to
-38.01
12.46
- 69.92
-13.10
1978-79
Early
K
0.00262
0.00158
- 0.00050
0.00575
Loo
113.2
48.8
16.3
210.1
tn
-42.28
9.94
- 62.00
- 22.57
Late (convergence
criteria cou
Id not be me
t)
LARVAL HERRING
1978-1979 STUDY
lU
<
>
a.
<
QC
UJ
CD
SEPT 1
OCT 1
NOV 1
DEC 1
SEPT
OCT I NOV I DEC
DATE OF HATCHING
JAN
Figure 5. -Frequency of Atlantic
herring hatching during the
1978-79 study. Upper scale gives
the day of hatch based on the Lough
et al. (1982) aging method as
discussed in the text. Lower scale
gives the day of hatch based on
Townsend and Graham's (1981)
aging method as discussed in the
text Arrow indicates division point
between early- and late-hatched
classification.
294
JONES: DIFFERENCES IN LARVAL I IKRHING GROWTH
cantly different (P < 0.01)- early-hatched larvae
grew faster than late-hatched larvae.
1978-79 Study
A frequency plot of hatching dates under the
assumption of daily increment deposition for larvae
sampled in the Sheepscot estuary is shown in Figure
5.
Analysis (Table 5) showed that the data were
better fit with two lines {P < 0.01) and that the
slopes were different (P < 0.01). The change in
length was 0.21 mm/increment and 0.18 mm/incre-
ment for early- and late-hatched larvae, respectively
(Fig. 6). However, the results should be interpreted
with the knowledge that Bartletf s test showed the
variances to be heterogeneous. This could have been
caused by actual heterogeneity of variances, or by
nonnormality in the data. The F tests used in these
analyses assumed equal variances between the hatch
classifications. Cochran (1947) reported, however,
that lack of homogeneity would decrease the power
of an F test to discern true differences when they
did, in fact, occur. Since differences were statisti-
cally significant, not meeting this assumption did not
hinder analysis (the use of various transformations
Table 5.— Regression analysis of 1978-79 Gulf of Maine Atlantic herring data. (Data fro
send and Graham 1981.)
im Town-
Otolith
Hatch
Slope of
Standard
Probability
Probability
increment
classifi-
Sample
regression
error
intercepts
slopes
count
cation
size
Intercept
line
of slope
m
equal
equal
All data
Early
102
13.3
0.2134
0.0661
0.92
<0.01
<0.01
Late
198
14.2
0.1793
0.0060
0.82
60 or fewer
Early
42
9.4
0.3378
0.0189
0.89
<0.01
<0.01
Late
53
11.4
0.2434
0.0203
0.74
Data were classified into early- and late-hatched larvae. These two groups were compared
by fitting ordinary least squares regression lines to 1) all the data within the two classifications,
and 2) using only lengths from larvae with 60 or fewer increment counts. Slopes and intercepts
were compared between early vs. late for each group.
60 -n
50
E
E 40H
I
O
m
30-
20-
)0 -
LARVAL HERRING GROWTH
1978-1979
A A,
W/ :
TIME OF HATCH
EARLY •
LATE A
T
20
40
80 100
T
60 80 100 120 140 160
INCREMENT COUNTS
~1
180
Figure 6. - Regression plot of length-at-otolith increment count for Atlantic herring. Complete data set represented. Data from Townsend
and Graham (1981).
295
FISHERY BULLETIN: VOL. 83. NO. 3
did not result in homogeneity of variances). Except
for the residuals for three small larvae, analysis for
residuals showed no trends.
For larvae with 60 increments and fewer (Fig. 7),
Bartlett's test showed homogeneity of variance.
These data were better fitted by two lines (P < 0.01);
the slopes were significantly different (P < 0.01).
The change in length was 0.34 mm/increment and
0.24 mm/increment for early- and late-hatched lar-
vae, respectively.
The von Bertalanffy growth equation fit the early-
hatched larval data poorly (Table 4). L^ was esti-
mated at 113.22 mm, with a 95% confidence interval
of 16.37 to 210.06 mm. The von Bertalanffy growth
function could not be fitted (solution would not con-
verge) to the late-hatched larval data.
The 1978-79 data could not be tested under
assumptions that increment deposition could vary
from 0.5 to 1.0 increment/d. Almost all of the calcu-
lated hatch dates for late-hatched larvae, estimated
on deposition rates of 0.5 increment/d, overlapped
the classification division date. Too few points were
left for analysis.
DISCUSSION
Evidence from the Gulf of Maine supports the
hypothesis that increase in length for herring larvae
hatched early in the spawning season is greater than
for larvae hatched late in the season. These differ-
ences were evident both under assumptions of daily
otolith increment deposition and for deposition of
one increment every other day. Before these dif-
ferences are assumed to be due to differences in
growth, however, there are other hypotheses which
should be considered that could explain these obser-
vations. Differences could be the result of within-
season changes in otolith increment deposition rates,
or of differential mortality due to selective predation.
If there are within-season changes in otolith incre-
ment deposition rates, growth (change in length at
age) could actually be similar, but the calculated
growth rates would appear to be different because
they are expressed as change in length per incre-
ment count. In order for this hypothesis to explain
the above results, larvae born early in the season
would be required to put down fewer increments per
time period than would larvae born late in the
season. The data allow a test of the hypothesis that
larvae lay down fewer than 1 increment/d during the
early part of the year. When estimated hatching
dates are calculated for larvae caught early in the
season, under the assumption that one increment
was deposited every other day, some of these larvae
35 -1
LARVAL HERRING GROWTH
1978-1979
TIME OF HATCH
EARLY •
LATE A
10
20
I r \
30 40
INCREMENT COUNTS
50
60
Figure 7. - Regression plot of length-at-otolith increment count for Atlantic herring. Only lengths for larvae with 60 or fewer otolith incre-
ments have been included for analysis. Data from Townsend and Graham (1981).
296
.lONKS: DIFKKKKNCKSIN LAIUAL HKKKINC OKOWl'H
would have had to appear in the plankton in the mid-
dle of the summer (Fig. 3). However, newly hatched
larvae are not found in significant numbers in the
plankton before September (Boyar et al. 1973; Col-
ton et al. 1979). It is far more plausible that larvae
hatched early in the season, when growing condi-
tions are more nearly optimal (Sherman and Honey
1971; Cohen and Lough 1983), deposit increments
with close to daily periodicity. Hence, in order for
this hypothesis to be true, late-hatched larvae would
have to deposit increments at a rate greater than 1
increment/d. There is no evidence in the literature to
support this for larval herring.
Difference in population growth rates within a
spawning season could also result from a shift in size-
specific mortality during the season. The observed
differences in growth rate could result if early-hatch-
ed larvae have higher cumulative mortalities for
slower growing individuals, while late-hatched larvae
have higher mortalities for faster growing indivi-
duals. Progressively, fewer and fewer of the selec-
tively predated larvae would be seen in older ages.
This would result in differences in population growth
rates that are not apparent for individuals within the
population.
Although differential mortality cannot be dis-
missed with the available data, the most plausible
explanation for the differences in length-at-incre-
ment count is an actual difference in larval growth
rate over the spawning season. Such differences in
population growth rate can be important for larval
herring survival. Since greater time spent in the lar-
val stage is thought to be related to increased mor-
tality, it is interesting to note that an early-hatched
larva from the 1978 study would require, on the
average, 80 d to reach 30 mm, compared with 88 d
for a late-hatched larva. For the 1976 study, it would
take, on the average 63 d for an early-hatched larva
to reach 30 mm compared with 157 d for a late-
hatched larva to reach this size.
It has been shown that in both years, late-hatched
larvae are larger than early-hatched larvae at the
time of first increment formation. This could result
from larger eggs being produced in the winter
(Cushing 1967), or from different growth rates from
hatch to the age of larvae covered in this study.
Without further evidence of differences in egg size
or actual growth rates between hatch and the age
these studies began, neither hypothesis can be sup-
ported.
Differences in growth rate within the spawning
season can contribute to error when using an age-
length key to age larvae. For a given length, samples
containing early-hatched larvae would yield different
ages than samples containing late-hatched larvae.
For the 1978-79 study (under the assumption of daily
increment deposition), a 25 mm larva would average
60 increments for early-hatched larvae versus 56 for
late-hatched larvae. For the 1976-77 study a larva of
this length would average 47 versus 102 increments,
respectively. This additional variation should be
taken into consideration when using age-length keys
for larvae.
Differences in growth during the spawning season
might be due to changes in the environment when a
species of fish spawns over a protracted time period,
such as Atlantic herring which spawns from late
August through November (Boyar et al. 1973; Col-
ton et al. 1979). Early in the season copepods, the
main food for larval herring (Sherman and Honey
1971; Cohen and Lough 1983), are more abundant
than late in the spawning season (Sherman et al.
1983). Temperatures average 12°-16°C early in the
season and < 8°C later in the season (Colton 1968;
Colton and Stoddard 1972). Day length and
metabolic demand may also vary over the spawning
season. Alternately, differences in growth between
larvae hatched early and late in the season could be
the result of genetic differences if early and late
spawners are from different stocks.
ACKNOWLEDGEMENTS
I thank R. G. Lough, D. Townsend, and J. J.
Graham for providing their data; and B. E. Skud, R.
G. Lough, J. J. Graham, and K. R. Hinga for their
suggestions and review of this manuscript.
LITERATURE CITED
Beverton, R. J. H., AND S. J. Holt.
19.54. On the dynamics of exploited fish populations. Fish.
Invest. Minist. Agric, Fish., Food (G.B.) Ser. II, Vol. XIX,
533 p.
Boyar. H. C, R. R. Marak, F. E. Perkins, and R. A. Clifford.
1973. Seasonal distribution and growth of larval herring
{Clupea harengns L.) in the Georges Bank-Gulf of Maine area
from 1962 to 1970. J. Cons. Int. Explor. Mer 35:36-51.
Cochran, W. G.
1947. Some consequences when the assumptions for the ana-
lysis of variance are not satisfied. Biometrics 3:22-38.
Cohen, R. E., and R. G. Lough.
1983. Prey field of larval herring Clupea harengus on a Con-
tinental Shelf spawning area. Mar. Ecol. Prog. Ser. 10:211-
222.
Colton, J. B., Jr.
1968. Recent trends in subsurface temperatures in the Gulf of
Maine and contiguous waters. J. Fish. Res. Board Can. 25:
2427-2437.
Colton, J. B., Jr., and R. R. Stoddard.
1972. Average monthly sea water temperatures, Nova Scotia
to Long Island, 1940-1959. Ser. Atlas Mar. Environ., Am.
297
FISHERY BULLETIN: \()L. 83. NO. .S
Geogr. Soc. Folio 22, 10 p.
CoLTON, J. B., Jr.,"' W. G. Smith, A. K. Kendall, .Jr., P. L.
Berrien, and M. P. Fahay.
1979. Principal spawning areas and times of marine fishes,
Cape Sable to Cape Hatteras. Fish. Bull., U.S. 76:911-915.
Gushing, D. H.
1967. The grouping of herring populations. J. Mar. Biol.
Assoc. U.K. 47:193-208.
Das, N.
1968. Spawning, distribution, survival, and growth of larval
herring {Clupea harengus L.) in relation to hydrographic con-
ditions in the Bay of Fundy. Fish. Res. Board Can., Tech.
Rep. 88, 162 p.
Draper, N. R., and H. Smith.
1981. Applied regression analysis. 2d ed. John Wiley and
Sons, Inc., N.Y., 709 p.
Geffen, A. J.
1982. Otolith ring deposition in relation to growth rate in
herring (Clupea harengus) and turbot (ScaphthalmTis inaxir
WM-s) larvae. Mar. Biol. 71:317-326.
Gjosaeter, H.
1981. Dagsonelesing som metode i aldersstudier pa fisk, med
eksempler pa anvendelse pa tropiske og boreale arter. Ph.D.
Thesis, Univ. Bergen, Bergen, Norway, 172 p.
HOENIG. N. A.
1982. A study of seasonal growth models for fishes. M.S.
Thesis, Univ. Rhode Island, Kingston, 91 p.
Jones, C. M.
1984. The otolith increment technique: Application in larval
fish. Ph.D. Thesis, Univ. Rhode Island, Kingston, RI, 123 p.
Lough, R. (J., and G. R. Bolz.
1979. A description of the sampling methods, and larval her-
ring {Clupea harengus L.) data for surveys conducted from
1968-1978 in the Georges Bank and Gulf of Maine areas.
Natl. Mar. Fish. Serv., NOAA, Northeast Fish. Cent., Woods
Hole, Mass., Lab. Ref Doc. 79-60, 230 [>.
Lough, R. G., M. Pennington, G. R. Bolz, and A. A. Rosenburg.
1982. Age and growth of larval Atlantic herring, Clupea
harengus L., in the Gulf of Maine-Georges Bank region based
on otolith growth increments. Fish. Bull., U.S. 80:187-199.
0IESTAD, V.
1982. Application of enclosures to studies on the early life
history of fishes. In G. D. Grice and M. R. Reeve (editors).
Marine mesocosms, p. 49-62. Springer-Verlag, N.Y.
OSTLE, B., and R. W. Mensing.
1975. Statistics in Research: basic concepts and techniques for
research workers. Iowa State Univ. Press. Ames, Iowa, 596
P-
Sherman, K., J. R. Green, J. R. Goulet, and L. E.isymont.
1983. Coherence in zooplankton of a large northwest Atlantic
ecosystem. Fish. Bull., U.S., 81:855-862.
Sherman, K., and K. A. Honey.
1971. Seasonal variations in the food of larval herring in
coastal waters of central Maine. Rapp. P. -v. Reun. Cons. int.
Explor. Mer 160:121-124.
Townsend, D. W., and J. J. Graham.
1981. Growth and age structure of larval Atlantic herring.
Clupea harengus harengus. in the Sheepscot River Estuary,
Maine, as determined by daily growth increments in otoliths.
Fish. Bull., U.S. 79:123-130.
298
SEASONAL CYCLES OF FAT AND GONAD VOLUME IN
FIVE SPECIES OF NORTHERN CALIFORNIA ROCKFISH
(SCORPAENIDAE: SEBASTES)
Patrick J. Guillemot, ' Ralph J. Larson,^ and William H. Lenarz^
ABSTRACT
Seasonal changes in visceral fat volume and gonad volume are compared in five species of rockfish from
northern and central California: Sebastes entomelas, S. paucispinis, S. goodei, S. pinniger, and S. flairidus.
In these species, visceral fat was deposited between spring and fall, at the same time as gametogenesis.
Visceral fat declined in volume between fall and spring, coinciding with the decline in volume of testes and
preceding the release of embryos in females. We suggest that increased feeding during the summer upwell-
ing season provides the energy for simultaneous fat accumulation, gametogenesis, and perhaps somatic
growth. During subsequent seasons of presumed food storage, these rockfishes may utilize visceral fat
reserves for maintenance. This pattern of fat deposition and utilization may contribute to the long life and
repeated reproduction of rockfishes, at the expense of current fecundit\' and growth.
Our data also suggest that rockfishes which spawn only once during the reproductive season have fat
cycles of greater magnitude than those spawning more than once a year. Of the species that we studied, the
apparent single spawners S. entomelas and S. flaindus have more northerly geographic distributions and
larger fat cycles than the multiple spawners S. goodei and 5. paucispinis. It is possible that the shorter and
more pronounced productive season in the north leads to a greater need for fat reserves during winter and
makes the wintertime production of additional batches of eggs energetically difficult.
The seasonal storage and utilization of lipid (and
nonlipid) reserves are important in the metabolic
activities and overall life histories of many animals
(Love 1970; Shul'man 1974; Derickson 1976a and
associated papers). While cycles of lipid storage and
utilization are generally associated with seasonal
changes in food availability (Derickson 1976b) or
metabolic demands (Lawrence 1976), the functions
of lipid storage are varied.
In many fishes, reserves are used primarily in
reproduction, as indicated by complementary cycles
of lipid content and reproductive activity (Lasker
1970; Shchepkin 1971a, b; Schevchenko 1972;
Shul'man 1974; Tyler and Dunn 1976; Wootton and
Evans 1976; Lasker and Smith 1977; Diana and
MacKay 1979; Delahunty and de Vlaming 1980;
Patzner 1980; Hunter and Leong 1981). The
seasonal accumulation of sufficient reserves may be
a prerequisite for sexual maturity in some fishes (lies
1974), and the amount of material stored may in-
fluence fecundity (Tyler and Dunn 1976). Reserves
'Southwest Fisheries Center Tiburon Laboratory, National
Marine Fisheries Service, NOAA, Tiburon, CA; present address:
3298 Madera Avenue, Oakland, CA 94619.
^Department of Biological Sciences, San Francisco State Univer-
sity, San Francisco, CA 94132.
^Southwest Fisheries Center Tiburon Laboratory, National
Marine Fisheries Service, NOAA, 3150 Paradise Drive, Tiburon,
CA 94920.
Manuscript accepted August 1984.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
may also be used in migration (Robertson and Wex-
ler 1960; Dotson 1978; Glebe and Leggett 1981 a, b),
and, when used in spawning migrations, may con-
tribute indirectly to reproduction.
Slobodkin (1962) and Calow (1977), however,
noted that fat deposition may actually detract from
reproduction, particularly when fat deposition and
reproduction are concurrent. In such cases, reserves
are often used instead for maintenance during
periods of food scarcity (Calow and Jennings 1977),
enhancing the opportunity to reproduce in the
future. Some fishes seem to use reserves both for
reproduction and maintenance, when spawning oc-
curs during periods of food scarcity or fasting
(Wilkins 1967; MacKinnon 1972; lies 1974;
Newsome and Leduc 1975; Foltz and Norden 1977;
Dawson and Grimm 1980; Pierce et al. 1980; Glebe
and Leggett 1981 a, b). The interpretation of such
cases is complex, since reproduction and
maintenance may be competing concurrently for
reserves.
Roberts (1979) noted that fat was deposited
seasonally around the viscera of two species of
shallow-water rockfish, Sebastes mystinus and S.
melanops. He suggested that the cycle of fat deposi-
tion and utilization was related to seasonal changes
in the abundance of food and to reproduction.
In this paper we examine the seasonal relationship
299
FISHERY BULLETIN: VOL. 83, NO. 3
between visceral fat volume and gonad volume in
five offshore species of rockfish: Sebastes entomelas,
S. paucispinis, S. goodei, S. pinniger, and 5.
flavidus. Based on Roberts' suggestion and the
general literature on fat cycles in fishes, we expected
to find complementary cycles of fat and gonad
volume, indicating that reserves are used in repro-
duction. We used visceral fat volume as a convenient
index of the timing and magnitude of seasonal
changes in reserves, explicitly assuming that
reserves stored elsewhere would change coinciden-
tally (Delahunty and de Vlaming 1980). Since we did
not measure total reserves, our data on visceral fat
volume cannot be applied to quantitative studies of
energ\' budgets, but are most useful for examining
seasonal changes and making comparisons within a
group of closely related species.
The use of gonadal volume as an index of reproduc-
tive activity requires some explanation. In males,
gonadal volume is a good index of the timing of
gametogenesis. In females of this live-bearing genus,
however, gametogenesis is often reflected only in the
initial increase of gonadal volume. Following fertili-
zation (which may occur some time after copulation,
due to sperm storage [Sorokin 1961; Echeverria
1981''; Boehlert and Yoklavich 1984]), ovarian
volume continues to increase during a gestation
period that lasts a month or so (Moser 1967). There
may be some postzygotic nutrition of embryos dur-
ing this time (Boehlert and Yoklavich 1984), but
much of the increase in volume is due to the ac-
cumulation of water (Moser 1967). In some species of
Sebastes that spawn more than once a year,
gametogenesis takes place again late in the repro-
ductive season of females. Among the species con-
sidered here, S. paucispinis and 5. goodei are clearly
multiple spawners (Moser 1967; MacGregor 1970),
and Echeverria^ has presented some evidence for
multiple spawning in S. pinniger.
MATERIALS AND METHODS
Party boat and commercial rockfish catches were
sampled weekly, as a part of a large-scale study, by
personnel from the National Marine Fisheries Ser-
vice (Tiburon Laboratory) and the California Depart-
*Echeverria, T. 1981. Maturity in six species of roci<fish
(Pisces, Scorpaenidae, Seba.'<tt's). [Abstr.] Proceedinji^s of the
1981 Western (Iroundfish Conference.
^Echeverria, T. 1983. Maturity and seasonahty of the
rockfishes (Scorpaenidae: Seh(ustes) of central California. Unpulil.
manuscr., 60 p. Southwest F'isheries Center Tihuron Laboratory.
National Marine f^isheries Service, NOAA, 31.50 Paradi.se Drive,
Tiburon. CA 94920.
ment of Fish and Game, at northern California
fishing ports between Crescent City (lat. 41°N) and
Morro Bay (35° N). The species sampled depended on
the day's catch. Samplers measured the total length
of each specimen to the nearest millimeter and
removed the viscera and gonads for preservation in
10% Formalin^ in seawater.
In the laboratory, fat tissue was dissected from the
viscera and its volume estimated by water displace-
ment in graduated cylinders. In some samples, a
small amount of fat had liquified. The volume of this
liquid was estimated and added to total fat volume.
Gonads were also removed and their volume
measured as above. The state of development of
ovaries and testes was scored according to indices
based mainly on gonad morphology and coloration
(Moser 1967; Gunderson et al. 1980). Histological
preparations of small gonads were used to confirm
sex and state of maturity. Data for species, sex, total
length, stage of maturity, and fat and gonad volume
were stored using a computer.
Data on visceral fat volume were analyzed for col-
lections made between March 1980 and February
1981, inclusive. Measurements of gonad volume
were begun in June 1980 and continued until May
1981 to obtain a full year of data. For each species,
data were pooled over all ports of collection and
divided quarterly, as follows: spring (March-May),
summer (June-August), fall (September-November),
and winter (December-February). Quarterly division
of data gave good sample sizes for most seasons, yet
still allowed seasonal separation. Primary production
is relatively low off California during fall and winter,
but is greater during most of spring and summer,
when coastal upwelling occurs (Bolin and Abbott
1963).
To facilitate comparisons, visceral fat volume and
gonad volume were expressed as log-transformed
power-function regressions of volume on fish length.
The power equation is:
V = aL'\
where V is volume, L is total length, and a and h are
estimated parameters. This equation is often used to
express the relationship between volumetric
measures, such as fecundity, and linear measures,
such as length (Bagenal 1978; Glebe and Leggett
1981a; de Vlaming et al. 1982). Logarithmic trans-
formation to
In V = In 0 + 6 In L
^Reference to trade names does not imply endorsement by the Na-
tional Marine Fisheries Service, NOAA.
300
GUILLEMOT ET AL.: SEASONAL CYCLES IN CALIFORNIA ROCKFISH
allows the use of standard least-squares regression
techniques, and stiihilizes variances (Bagenal 1978).
Thus, rather than using ratios of fat or gonad volume
to fish weight or length, which can be biased by allo-
metric relationships between the measurements
(Bagenal 1978; de Vlaming et al. 1982), we employed
empirically derived regression lines. The use of
power equations also allowed us to test hypotheses
with standard statistical procedures. Regressions
were calculated for each sex during each season.
Although most of the analyses were for adults,
seasonal regressions of visceral fat volume were also
computed for juveniles when samples were large.
Differences between regressions of fat or gonad
volume were tested by analysis of covariance, using
the ratio:
F =
{N - 4) (SS,„^. - SSi - SS^)
2 (SS, + SSg)
where SS, and SSo are the residual sums of squares
about the separate regressions, SS^.^.^, is the residual
sum of squares for a common regression, and A'' is
the number of specimens (Kleinbaum and Kupper
1978). When regressions differed significantly, the
direction of differences was assessed by examining
the positions of the regression lines and of calculated
volumes at mean fish length. We chose to display
only the calculated volumes at mean length, to
simplify the presentation of data. The mean of In
(total length) was determined for all specimens of a
sex and species included in the annual analysis. For
each season and sex, the estimated value of In
(volume) at the mean of In (length) (designated Y)
was calculated from the appropriate regression. We
intend these point values to be used only for making
comparisons within our data. The regression lines
themselves best represent fat or gonad volume, and
we present the parameters for these regressions.
See Guillemot (1982) for scatter diagrams of raw
data and regression plots.
The estimated values of fat volume at mean length
were also used in an index of the relative amplitude
of fat cycles. This index was the antilog of the differ-
ence between estimated In (fat volume) in peak and
low seasons, and is equivalent to the ratio of peak
season -.low season fat volume.
We compared fat cycles of males and females
within a species by qualitatively noting differences in
the timing and amplitude of fat cycles, and by statis-
tically comparing fat regressions during peak and
low seasons of fat volume. The latter comparisons
were carried out by analysis of covariance, as above.
In comparing fat cycles among species, we noted
differences in the timing of fat cycles and differences
in the amplitude of cycles. We also assessed dif-
ferences in the absolute volume of fat stored by
applying analyses of covariance to the peak-season
fat regressions of the different species.
RESULTS
Seasonal Cycles of Fat and
Gonad Volume in Adults
In most seasons, moderate to low correlations (0.5
and below) existed between In (visceral fat volume)
and In (total length), indicating a fair amount of scat-
ter about the regressions (Table 1). Lower correla-
tions occurred mainly in seasons of low fat volume
(cf. Fig. 1). The slopes of most regressions were not
significantly different from 3.0 (Table 1), indicating a
proportionate relationship between fat volume and
fish length. Slopes significantly smaller than 3
occurred in seasons of low fat volume (winter and
spring), and in general slopes from seasons of low fat
volume were smaller than those from seasons of
higher fat volume. During seasons of low fat volume,
fish of all sizes tended to have little fat, accounting in
part for some of the lower correlations. Some slopes
were significantly greater than 3 during seasons of
high fat content (5. entamelas females, 5. paucis-
pinis males, S. pinniger females, and S. Jlavidus
females), indicating disproportionately greater fat
content in larger fish. Correlations between In
(gonad volume) and In (total length) were generally
high (Table 2), and showed no marked relation with
season (Fig. 2). Below, we first examine the fat and
gonad cycles for adults of each species separately,
and then briefly compare the cycles of different
species.
Sebastes entomelas
Visceral fat content changed significantly during
the year in both male and female S. entomelaf; (Fig.
1). In females, where all seasonal regressions of In
(visceral fat volume) on In (total length) differed
significantly from each other, fat content increased
from a low in spring to a peak in fall, and then declin-
ed in winter (Fig. 1). In males, neither the spring and
winter nor the summer and fall fat regressions dif-
fered significantly (Fig. 1). Visceral fat volume in
males increased after spring to a peak spread
through summer and fall, and then declined in winter
(Fig. 1). During the fall, when both sexes had large
volumes of visceral fat, fat content of males barely
301
FISHERY BULLETIN: VOL. 83, NO. 3
Table 1.— Seasonal regressions of In (visceral fat volume, nnl) on in (Jotal length, mm) in adults of five species of
Sefcas^es from northern and central California. Slopes significantly different from 3 are indicated (? = P<0.1;* = P<
0.05; ** = P< 0.01; *** = P< 0.001).
Species
and
Females
Males
Sample
Sample
season
size
Intercept
Slope
r
size
Intercept
Slope
r
S. entomelas
Spring
118
'21.752
3.845
0.240
88
-12.267
2.341
0.138
Summer
102
- 23.875
4.335*
0.578
58
-32.427
5.795?
0.456
Fall
81
-28.715
5.184**
0.581
57
- 20.654
3.908
0.459
Winter
163
- 18.442
3.400
0.428
84
-19.524
3.538
0.251
S. pauclspinis
Spring
117
-10.334
1 .988?
0.314
115
-17.544
3.150
0.443
Summer
116
-16.415
2.982
0.576
127
-16.120
2.978
0.553
Fall
75
- 12.957
2.500
0.462
101
- 24.053
4.259**
0.693
Winter
82
-1.269
0.633* *•
0.165
83
- 9.847
1.942*
0.389
S. goodel
Spring
193
-12.741
2.220
0.272
51
-14.555
2.671
0.281
Summer
219
-10.780
2.027
0.221
80
-11.827
2.299
0.403
Fall
140
-14.895
2.763
0.499
68
-17.686
3.228
0.334
Winter
183
0.253
0.155***
0.020
55
0.783
- 0.026?
- 0.002
S. pinniger
Spring
23
-16.134
2.980
0.400
38
-16.581
3.006
0.445
Summer
61
-28.391
4.957***
0.786
103
-17.213
3.152
0.455
Fall
32
-24.771
4.453
0.579
37
-14.859
2.825
0.593
Winter
18
-24.371
4.289
0.529
14
- 28.849
5.063
0.538
S. flavidus
Spring
73
8.221
-1.038**
- 0.099
71
-18.255
3.298
0.259
Summer
143
- 24.044
4.323**
0.605
88
- 10.960
2.152
0.240
Fall
147
-14.050
2.771
0.468
112
- 8.652
1.777
0.212
Winter
69
- 2.946
0.743*
0.092
72
-14.442
2.575
0.227
exceeded that of females. Fat recessions at the low
point in spring did not differ significantly (Table
3).
As expected, gonad volume changed significantly
during the year in both sexes of S. entomelas (Fig. 2).
In males, the volume of testes increased dramatically
from a low in spring to a peak in summer, and then
declined through fall and winter (Fig. 2). In females,
the volume of ovaries increased very slightly be-
tween spring and summer, and then increased great-
ly in fall and winter (Fig. 2).
Sebastes paucispinis
Visceral fat volume changed significantly during
the year in males and females of S. paucispinis (Fig.
1). In females, fat content did not change significant-
ly between spring and summer, but increased from
summer to a peak in fall, to decline slightly in winter
(Fig. 1). In males, visceral fat accumulated between
spring and summer, remained about constant from
summer to fall, and declined in winter (Fig. 1). Dur-
ing the nominal peak season in fall, fat content of
females was significantly greater than that of males,
while the regressions for fat content during the
nominal low points in spring did not differ signifi-
cantly (Table 3).
Ovarian volume in S. paucispinis reached its low
point during summer, increased with vitellogenesis
in fall, increased again with embryogenesis and/or
further vitellogenesis in winter, and then declined in
spring (Fig. 2). The volume of testes increased from
spring into summer, continued to increase slightly in
fall, and declined in winter (Fig. 2).
Sebastes goodei
Visceral fat volume in female S. goodei increased
from spring through summer to a peak in fall, and
declined in winter (Fig. 1). In male 5. goodei, visceral
fat volume increased from low levels in spring to a
peak in summer, declined slightly in fall, and
decreased again in winter (Fig. 1). The fat content of
females during their fall peak exceeded that of males
during their summer peak, while there was no signi-
ficant difference in fat content during the low
seasons of spring for females and winter for males
(Table 3).
Ovarian volume increased slightly between spring
and summer in females of S. goodei, and then grew
more rapidly through fall and winter (Fig. 2). The
volume of testes increased greatly between spring
and summer in males of 5. goodei, and then declined
through fall and winter (Fig. 2).
302
GUILLEMOT ETAL.: SEASONAL CYCLES IN CALIFORNIA RCX^KKISH
Females ^ entomelas
3
Males
S. paucispinis
S. goodei
S. pinniger
S. flavidus
3
-
^ ^ ^*^
2
■
--^
1
"
f\
1
' 1
„ . Summer ^ ., Winter
Sprmg Fall
Summer ^ ,, Winter
Sprmg Fall
SEASON
Figure 1 . - Seasonal variation of visceral fat volume in adults of five species of Sebastes from northern and central
California. For each species and sex, points are estimates of In (fat volume) at the overall average of In (total length)
for specimens of that species and sex examined during the year. Estimates were derived from the seasonal regres-
sions of In (visceral fat volume) on In (total length) (Table 1). A horizontal line between two seasons means that the
fat regressions for those two seasons differed significantly (P < 0.05) by analysis of covariance. The upper of the two
rows of horizontal lines are for adjacent seasons in the graph. The lower horizontal line is for winter and spring. The
absence of a horizontal line means that the regressions did not differ significantly. Annual averages of In (total
length, mm) areS. entomelas females, 6.13, and males, 6.08; S. paucispinis females, 6.31, and males, 6.20; S. goodei
females, 6.11, and males, 5.88; S. pinniger females, 6.11, and males, 6.14; diUd S.flavidus females, 6.11, and males,
6.04. Seasons: spring (March-May 1980), summer (June-August 1980), fall (September-November 1980), and
winter (December 1980-February 1981).
303
FISHERY BULLETIN; VOL. 83, NO. 3
Table 2.— Seasonal regressions of In (gonad volume, mL) on In (total length, mm) in adults of five species
of Sebastes from northern and central California.
Species
and
Females
f^ales
Sample
Sample
season
size
Intercept
Slope
r
size
Intercept
Slope
r
S. entomelas
Spring
217
- 36.259
6.226
0.787
93
- 40.725
6.738
0.709
Summer
17
-50.148
8.148
0.908
18
-42.341
7.386
0.644
Fall
65
- 58.734
10.187
0.781
33
-10.442
1.930
0.191
Winter
177
- 40.049
7.249
0.532
115
- 18.856
3.207
0.403
S. paucispinis
Spring
113
- 26.341
4.541
0.640
163
- 36.055
5.933
0.855
Summer
78
- 34.265
5.767
0.919
105
- 36.360
6.130
0.807
Fall
78
-37.533
6.386
0.833
118
- 28.802
4.935
0.845
Winter
118
- 34.058
5.946
0.647
127
-17.757
3.014
0.508
S. goodei
Spring
146
- 34.372
5.961
0.785
60
-20.612
3.552
0.332
Summer
166
-32.127
5.617
0.798
63
-12.733
2.386
0.283
Fall
176
-17.064
3.293
0.460
93
-29.433
5.095
0.772
Winter
184
-27.812
5.151
0.495
71
-17.172
2.886
0.214
S. pinniger
Spring
21
- 23.843
4.181
0.694
35
- 49.963
8.230
0.799
Summer
22
-51.129
8.611
0.902
43
-60.352
10.175
0.939
Fall
31
-50.164
8.448
0.889
40
- 45.336
7.564
0.845
Winter
21
- 34.798
6.022
0.538
14
-65.227
10.657
0.904
S. fl avid us
Spring
100
- 29.422
5.083
0.707
138
-31.837
5.228
0.499
Summer
83
-33.961
5.892
0.852
50
-54,152
9.204
0.759
Fall
162
-47.425
8.155
0.822
134
- 38.906
6.649
0.690
Winter
53
- 30.680
5.592
0.575
80
- 23.743
3.927
0.555
Table 3.— Comparisons of fat volume between males and
females during peak and low fat seasons in five species of
Sebastes. If not defined statistically, peak and low seasons
were selected on the basis of regression positions. Y, the
estimated In (fat volume) at the overall average of In (total
length), is presented as an indication of regression position
(Fig. 1). If male and female fat regressions differed
significantly (P < 0.05) by analysis of covariance, their
relative fat volumes are indicated. NS denotes regressions
that did not differ significantly.
Females
Males
Species Season
Season
Comparison
S. entomelas
Peak
Low
S. paucispinis
Peak
Low
S. goodei
Peak
Low
S. pinniger
Peak
S. flavidus
Peak
Low
Fall 3.07 Fall 3.09
Spring 1.82 Spring 1.96
Fall 2.81 Fall 2.35
Spring 2.20 Spring 1.99
Fall 1.98 Summer 1.70
Spring 0.82 Winter 0.63
Fall
2.69 Fall
2.49
Fall 2.87 Fall 2.08
Winter 1.59 Winter 1.12
o- > 9
NS
9 > o-
NS
9 > o"
NS
NS
9 > CT
NS
Sebastes pinniger
Cycles of visceral fat volume were poorly defined
in S. pinniger. In females, only the summer and fall
fat regressions differed significantly, suggesting a
peak in fat content during the fall (Fig. 1). In males.
no two consecutive seasons differed significantly in
fat content, and the only two seasons that differed
significantly at all were spring and fall (Fig. 1). Thus,
males may also have had peak fat content during fall,
but their fat cycle was not pronounced. The visceral
fat content of males and females did not differ signi-
ficantly during their apparent fall peaks (Table 3).
The ovarian cycle of S. pinniger was also poorly
defined in our data. Ovaries increased significantly in
volume between spring and summer (Fig. 2). No
other seasons differed significantly, but a peak in
winter is indicated in Figure 2. In males, gonadal
volume increased dramatically from spring to a peak
in summer, remained fairly high in fall, and declined
in winter (Fig. 2).
Sebastes flavidus
Visceral fat volume in female .S. Jlavidtis increased
from spring through fall, and then declined in winter
(Fig. 1). Ma\e S.Jlavidits exhibited a gradual increase
in fat content between spring and fall, followed by a
decline to minimal fat levels in winter (Fig. 1). Fat
content of females exceeded that of males during
their fall peaks, and the difference in fat content dur-
ing their winter lows was not significant (Table 3).
Ovarian volume in S. flavidus showed a pattern
similar to most of the rest of the species: an increase
304
CUILLEMOT ET AL.: SEASONAL CYCLES IN CALIFORNIA ROCKFISH
Females S. entomelas
Males
<
o
C5
S. paucispinis
S. goodei
S. pinniger
S. flavidus
Summer
Winter
Spring
Summer Winter
Spring Fall
Figure 2. - Seasonal variation of gonad volume in adults of five species of Sebastes from northern and central
California, as in Fi^ire 1. Averages of In (total length, mm) used in estimating gonadal volume are S. ev-
tomdas females, 6.14, and males, 6.06; S. paucispinis females, 6.24, and males, 6.17; S. goocki females, 6.09,
and males, 5.88; S. pintiiqrr females, 6.20, and males, 6.13; and S. flavidus females, 6.09, and males,
6.04. Seasons: spring (March-May 1981), summer (.lune-August 1980), fall (September-November 1980),
and winter (December 1980-Februar>' 1981).
305
FISHERY BULLETIN: VOL. 83, NO. 3
from low volume in spring to peak volume in winter
(Fig. 2). In males, the volume of testes increased
from spring to a peak in summer, declined slightly in
fall, and fell greatly in winter (Fig. 2).
Summary and Comparison of
Adult Fat Cycles
In all species studied, visceral fat volume was high,
if not at a peak, during fall. In males, fat content was
usually high during summer as well. In male S. en-
toTnelas, S. paucispinis, and S. Jlavidus, summer and
fall fat content did not differ significantly, and in
male S. goodei the fat content in summer was actual-
ly greater than in fall. Summertime fat content was
relatively high in female S. entomelas, S. goodei, and
S. flavidus, but in females of all species the fat con-
tent increased to a peak in fall. Winter and spring
were usually the seasons of low fat volume in both
sexes. Little pattern existed in S. pinniger, except
that fat volume appeared to reach a peak in fall.
Both the relative amplitude of fat cycles and peak
fat volume differed among the species and sexes. In
Table 4.— Relative amplitude of fat cycles in five spe-
cies of Sebastes. The ratio of estimated peak season :
low season fat volume is presented for eacti species
and sex, and is used as an index of cycle amplitude.
Ratios are the antilogs of the differences between
estimated In (fat volume) at the average of In (total
length) in peak and low fat seasons (Fig. 1, Table 3).
Amplitude
Species
Females
Males
S. entomelas
3.50
3.10
S. paucispinis
1.83
1.44
S. goodei
3.20
2.91
S. pinniger
1.67
1.84
S. flavidus
3.61
2.64
male and female S. entomelas, S. goodei, and S.
flavidus, the fat volume of average-sized fish
changed by about a factor of three during the year
(Table 4). The amplitude of the fat cycle was lower in
S. paucispinis and S. pinniger, where there was less
than a twofold change in fat content between peak
and low seasons (Table 4). Among females, S. en-
tomelas and S. Jlavidus generally had higher peak fat
volumes than the other species (Table 5). Among the
other three species, peak fat content of females
seemed to decrease from S. pinniger to S.
paucispinis toS. goodei (Table 5). Females of S. ento-
melas and S. Jlavidus, then, possessed high-volume,
high-amplitude fat cycles, while S. pinniger and S.
paucispinis had low-volume, low-amplitude fat
cycles, and S. goodei showed low volume and rela-
tively high amplitude. The peak fat volume in maleS.
entomelas far exceeded that of the remaining
species, most of which had relatively similar fat-
length relationships during peak seasons (Table 5).
Thus among males, only S. entomelas showed a high-
volume, high-amplitude fat cycle. Males of S. Jlavidus
and S. goodei possessed fat cycles of low volume and
moderately high amplitude, and S. paucispinis and
S. pinniger had cycles of low volume and low ampli-
tude, like the females of these species.
Fat Cycles in Juveniles
Fat cycles were examined in juveniles of male and
female S. paucispinis, and of female 5. pinniger and
iS. Jlavidus, where seasonal sample sizes were large
enough to permit analysis (Table 6). In 5. paucispi-
nis, juvenile females appeared to reach a peak in fat
content during winter, but in juvenile males there
were no significant differences among the seasonal
regressions (Fig. 3). In S. pinniger, juvenile females
Table 5.— Comparisons of the peak-season regressions of In (fat volume) on In (total
length) for different species of Sebastes. Comparisons were made by analysis of
covariance. For significantly differing regressions (P < 0.05), the comparative fat
volumes are indicated (based on the positions of the regressions, cf. Fig. 1, Table 1),
unless intersecting lines made position difficult to interpret. NS denotes regressions
that did not differ significantly.
S. paucispinis
S. goodei
S. pinniger
S. flavidus
Females
S. entomelas
S.e. > S.pa.
S.e. > S.g.
NS
NS
S. paucispinis
S.pa. > S.g.
NS
S.pa. < S.f.
S. goodei
S.g. < S.pi.
S.g. < S.f.
S. pinniger
S.pi. < S.f.
Males
S. entomelas
S.e. > Spa.
S.e. > S.g.
S.e. > S.pi.
S.e. > S.f.
S. paucispinis
intersection
S.pa. < S.pi.
intersection
S. goodei
NS
NS
S. pinniger
NS
306
GUILLEMOT ET AL.: SEASONAL CYCLES IN CALIFORNU ROCKFISH
possessed little fat in the spring, and higher levels in
summer through winter (Fig. 3). Fat content in
juveniles of female S. flavidus peaked in fall (Fig. 3).
Table 6.— Seasonal regressions of In (visceral fat volume,
mL) on In (total length, mm) in juveniles of three species of
Sebastes from northern and central California.
Species
and sex
Season
Sample
size
Intercept
Slope
r
S. paucispinis
females
Spring
140
- 19.637
3.510
0.325
Summer
138
- 26.793
4.669
0.455
Fall
55
- 23.626
4.189
0.419
Winter
67
- 29.508
5.205
0.719
males
Spring
92
-10.309
1.976
0.157
Summer
86
- 22.626
3.969
0.362
Fall
10
- 48.866
8.324
0.599
Winter
21
- 27.486
4.818
0.766
S. pinniger
females
Spring
41
-21.012
3.655
0.402
Summer
76
-21.794
3.859
0.624
Fall
37
- 36.539
6.383
0.875
Winter
20
-18.568
3.345
0.651
S. flavidus
females
Spring
21
- 22.796
4.080
0.388
Summer
70
- 8.502
1.642
0.260
Fall
53
- 36.450
6.558
0.639
Winter
19
- 9.906
1.848
0.361
Thus, in three of the four groups analyzed, fat con-
tent of juveniles varied during the year. The timing
of the apparent cycles was similar to that of adults.
The amplitude of the fat cycle in juveniles of female
S. paucispinis and S. pinniger (less than twofold
change in fat volume) was similar to adult amplitude.
In female S. Jlavidus, the amplitude of the fat cycle
in juveniles (less than twofold change) was lower
than in adults. As adults, S. flavidits showed high-
amplitude fat cycles, while 5. paucispinis and S. pin-
niger showed low-amplitude cycles.
DISCUSSION
Clear cycles of visceral fat volume and gonadal
volume occurred in both sexes of S. entomelas, S.
paucispinis, S. goodei, and S. flavidus. The fat cycles
of male and female S. pinniger were less well-
defined, as was the gonadal cycle of female S. pin-
niger. Many of the female S. pinniger we examined
were relatively small adults. This may account, at
least in part, for the small and ill-defined fat and
gonad cycles, as the fat cycles of female 5. flavidus
increased in amplitude from juveniles to adults.
Visceral fat volume generally increased propor-
S. paucispinis
Females S. paucispinis
Males
S. pinniger
Females S. flavidus
Females
<
U.
^ ^^-"
•
. 1
Summer
Spring Fal
Winter
Summer
Spring Fall
Winter
SEASON
Figure 3. -Seasonal variation of visceral fat volume in the juveniles of five species of Sebastes, as in Figure 1.
Averages of In (total length, mm) used in estimating fat volume are S. paucispinis females, 6.08, and males, 6.04; S.
pinniger females, 5.88; and S. flavidus females, 5.78. Seasons: spring (March-May 1980), summer (June-August
1980), fall (September-November 1980), and winter (December 1980-February 1981).
307
FISHERY BULLETIN: VOL. 83, NO. 3
tionately with fish volume, since most slopes of In
(fat volume) on In (length) were near 3. Slopes
smaller than 3 occurred in those seasons when fish of
all sizes had little fat. Some slopes during seasons of
high fat volume were significantly greater than 3, in-
dicating that larger fish had disproportionately
greater fat volume than smaller fish. This was parti-
cularly true of, but not limited to, the species and
sexes with high-magnitude fat cycles (males and
females of 5. entomelas and females ofS.flavidus). It
would be interesting to discover whether larger
females of 5. pinniger have high-amplitude fat
cycles, since the slopes of the fat regressions for
female S. pinniger were relatively high.
The dependence of fat volume on fish size and
season of collection, while applicable on average,
does not apply to every individual. The scatter about
the regressions of fat volume on length was large.
Some of the scatter was probably due to errors in
measurement, but a large part was real. We have
observed large differences in the amount of visceral
fat among fish of the same size and sex in the same
collection. The reasons for such variation may be dif-
ficult to resolve, since it is difficult to know the
history of individuals collected in the field.
However, our data were adequate in most species
to detect seasonal changes on average. We wanted
to compare the timing of fat cycles and gonad cycles,
and thus learn something of the function of fat
storage in rockfish. Our initial hypothesis was that
stored fat would be used in reproduction, based on
Roberts' (1979) observations.
The data for males do not support this hypothesis.
Fat and gonad cycles were nearly coincident, with
peaks in both cycles occurring in fall and/or summer
and lows in winter/spring. Thus the energy for
gonadal growth was probably derived from current
ingestion, not from material previously stored as fat.
Maximum somatic growth also coincides with the
summertime growth of testes and fat deposits (e.g..
Love and Westphal 1981), so all three processes may
be competing for energy consumed during this time.
The situation is more complicated in females.
Some fat was deposited between spring and summer
in females of S. entomelas, S. goodei, Sind S. Jlavidus,
and females of all species gained fat between sum-
mer and fall. Some gonadal growth took place be-
tween spring and summer in females of all species
except S. paucispinis. In all but 5. pinniger,
however, ovarian volume increased steadily between
summer and winter. The growth of ovaries through
fall was due largely to vitellogenesis, while the
greater growth of ovaries into winter was due
primarily to embryogenesis and hydration of ova
(Moser 1967). Additional vitellogenesis probably
occurred during winter in the multiple spawners, 5.
paucispinis and S. goodei (Moser 1967; MacGregor
1970).
In females, then, fat deposition usually began in
summer, perhaps slightly before the initiation of
vitellogenesis, but continued into the main period of
vitellogenesis between summer and fall. Thus, like
males, females of these species deposited fat more or
less concurrently with gonadal maturation and
somatic growth. The depletion of visceral fats oc-
curred between fall and spring in females of most
species, during and after gestation. It is possible that
fat reserves are used for the maturation of additional
ova in multiple spawners or are involved in the nutri-
tion of embryos (Boehlert and Yoklavich 1984), but
as in males, reserves are not used in the initial devel-
opment of gonads.
There were two main differences in the fat cycles
of males and females: females usually had larger fat
cycles than males, and the peak fat volume of
females occurred in fall, while fat volume in males
usually reached a plateau that spread through sum-
mer and fall. It is possible that courtship activity in
males (Helvey 1982) draws energy from fat deposi-
tion between summer and fall, or that this activity
draws time from feeding. As a result, females may
continue to fatten after fat deposition ceases in
males. It is also possible that females require more
reserves in winter and they somehow are able to ac-
quire these extra reserves.
The synchronous depletion of reserves in males
and females, however, indicates a common function
for such reserves. We suggest two possible func-
tions:
First, some rockfish may migrate during the
period of fat depletion. Love (1981) presented
evidence for seasonal movements in SebaMes
paucispinis and S. entomelas off southern California,
but had no data on the extent or direction of move-
ment. Females of S. alutus undertake seasonal
migrations covering as much as 300 m of depth (sum-
marized in Gunderson 1977). Lenarz (pers. obs.)
found evidence of seasonal movement in female S.
jordani. Several species of rockfish undertake little
or no seasonal migration, including ^S. ./7a rvV/M.s from
shallow waters off Alaska (Carlson and Barr 1977).
Since seasonal migrations in rockfish may not be
long and seem to occur primarily in females, we sug-
gest that other possibilities be ruled out before ac-
cepting migration as a major use of fat reserves.
Second, we suggest that fat reserves are used for
maintenance during wintertime periods of reduced
food availability. Fattening, as well as growth and
308
(;U1LLKM()TETAL.:SKAS()NAL CYCLES IN CALIFORNIA ROCKFISII
initial gametogenesis, occurs during and shortly
after the spring-summer upwelling period, and deple-
tion occurs during and after a time of lower primary
production (Bolin and Abbott 1963). Roberts (1979)
noted that several species of inshore rockfish near
Monterey consumed more food during the summer,
when macroplankton (euphausiids) and juvenile rock-
fish were abundant. During the nonupwelling
season, juvenile rockfish and macroplankton were
less abundant, and adult rockfish consumed less food.
Love and Westphal (1981) found less food in the
stomachs of S. serranoides during the nonupwelling
season near Morro Bay. Gunderson (1977) noted a
"summer feeding season" in 5. alutus. Hobson and
Chess', however, found the gelatinous prey of 5.
mystinns to be more abundant during nonupwelling
periods off northern California. There is only limited
information on the seasonal food habits of the five
species studied here. Sehastes paucispinis is largely
piscivorous (Phillips 1964), while S. entomelas, S.
goodei, S. pinniger, and S. fiavidus feed on macro-
plankton and small fish (Phillips 1964; Pereyra et al.
1969; Brodeur 1982). Brodeur (1982) examined
seasonal changes in the diets of S. fiavidus and 5.
pinniger, and found that food consumption declined
during winter in 5. pinniger, but not in S. fiavidus.
However, Carlson and Barr (1977) found a pro-
nounced decline in activity during winter in 5.
fiavidus off Alaska, suggesting seasonal changes in
feeding. This hypothesis can be examined with con-
current data on food consumption and fat volume. It
is not mutually exclusive with other functions of fat
reserves, since some fat could also be used for migra-
tion, nourishment of embryos, or maturation of addi-
tional ova in multiple spawners.
The wintertime use of reserves for maintenance,
however, is consistent with the overall pattern of
long life and repeated reproduction in rockfish (as
discussed also by Gunderson [1977]). As suggested
by Slobodkin (1962) and Calow (1977), summertime
fat deposition may exact a cost in current reproduc-
tion (if more gametes could be packed into rockfish
abdomens) or in future increases in gamete capacity
(through additional growth), but may help to ensure
survival.
An interesting result of our study was the differ-
ence in magnitude of fat cycles among species, which
was particularly evident in females. These differ-
ences are correlated with both the frequency of
spawning and geographical distributions of the
^Hobson, E. S., and J. R. Chess. 1981. Seasonal patterns in
trophic relationships of the blue rockfish, Sebaates
myatinu-ti. |Abstr.| Proceedings of the 1981 Western Groundfish
Conference.
species. Females of S. entomelas and S. Jlaviduji had
fat cycles of high amplitude and volume, probably
spawn only once a year (Westrheim 1975; Eche-
verria footnote 5), and have northerly distributions
(Phillips 1957, 1964; Gunderson and Sample 1980;
Adams 1980). On the other hand, 5. paucispinis and
S. goodei had fat cycles of low amplitude and/or
volume, spawn more than once a season, at least in
southern California, and have southerly distributions
(Phillips 1957, 1964; Gunderson and Sample 1980;
Adams 1980). The case with S. pinniger is unclear.
Females seemed to have low-amplitude fat cycles,
but the small sample and small sizes of females in the
samples make conclusions tenuous. Echeverria (foot-
note 5) has some evidence for multiple spawning in
S. pinniger. If so, its northerly distribution would be
inconsistent with the pattern seen in the other
species. We will restrict our discussion to the remain-
ing four species, although further studies of S. pin-
niger may be instrumental in evaluating the sugges-
tions we make below.
The small fat cycles of multiple spawners are prob-
ably not caused by their potentially greater repro-
ductive output, since fat deposition stops long before
the maturation of additional batches of ova. It seems
more likely that the magnitude of the fat cycle, fre-
quency of spawning, and geographical distribution
are all related. Boehlert and Kappenman (1980) sug-
gested that year-round spawning in southern popula-
tions of 5. diploproa served to increase reproductive
output in response to annual variation in the survival
of planktonic larvae. Multiple spawning in southern
populations and species may also be a response to the
more even seasonal distribution of upwelling in
southern vs. northern areas of the northeastern
Pacific (Bakun et al. 1974; Parrish et al. 1981; Smith
1978), as it affects planktonic larvae. However, the
more restricted upwelling season in northern waters
may also lead to larger and better defined seasonal
variation in the food supply of adults. A more pro-
nounced summertime pulse of food may enable
northerly species like 5. entomelas and S. fiavidus to
store large amounts of fat. Similarly, a more pro-
nounced decline in food during winter may make the
accumulation of such reserves necessary, and
preclude the maturation of additional batches of ova.
On the other hand, a more even seasonal distribution
of food in the south may enable southerly species like
S. paucispinis and S. goodei to produce additional
batches of ova during winter, and may also reduce
the need for wintertime reserves. These suggestions
are speculative, but it should be possible to compare
the seasonal variation of food consumption in species
with northern vs. southern distributions.
309
FISHERY BULLETIN: VOL. 83. NO. 3
In summary', we suggest that seasonal changes in
the availability' of food are rather important in the
life histories of rockfish. The summer storage and
winter use of fat reserves, in near synchrony with
growth and decline of gonad volume, indicate a
wintertime paucity of food that is compensated by
the use of material that was stored at the expense of
fecundity or growth. Further study of seasonal
feeding, fat deposition, and reproductive cycles,
categorized by size and sex, would be useful in
evaluating this hypothesis. Further, geographical
comparisons of these cycles may illuminate some
causes of differences in the life histories of
rockfishes.
ACKNOWLEDGMENTS
For their assistance during the course of the study,
we thank Tina Echeverria, Pete Adams, Connie
Ryan, Nancy Wiley, and many other employees of
NMFS and the California Department of Fish and
Game. Pete Adams, Tom Niesen, and George Boeh-
lert suggested improvements in the manuscript.
Diane Fenster drafted the figures. This paper is
derived from the senior author's Master's thesis at
San Francisco State University. The work took place
at the Southwest Fisheries Center Tiburon Labora-
tory, National Marine Fisheries Service, CA, under a
NMFS student appointment.
LITERATURE CITED
Ar)AM.s. p. B.
1980. Morphologj' and distribution patterns of several impor-
tant species of rockfish ({jt'nus Sehastes). Mar. Fish. Rev.
42(.3-4):8()-82.
Bagenal, T.
1978. Aspects of fish fecundity. In S. L). Gerkinjj (editor),
Ecology of freshwater fish production, p. 7.5-1(11. Biackwell
Scientific Publications, Oxford.
Bakun, a., D. R. McLain, and F. V. Mayo.
1974. The mean annual cycle of coastal upweliing off western
North America as observed from surface measurements.
Fish. Bull.. U.S. 72:843-844.
BOEHLERT, G. W., AND R. F. KaFPENMAN.
1980. Latitudinal growth variation in the ji;enus Sehnsfcs from
the northeast Pacific Ocean. Mar. Ecol. Prog. Ser. .3:1 -10.
BOEHI.ERT. G. W.. AND M. M. YoKLAVICH.
1984. RepHKiuction. embryonic energetics, and the maternal-
fetal relationship in the viviparous genus Sebastes (Pisces:
Scor{)aenidae). Biol. Bull. (Woods Hole) 167:354-370.
BoLiN. R. L., AND D. P. Abbott.
1963. Studies on the marine climate and phytoplankton of the
central coastal area of ('alifornia, 1954-1960. Calif. Coop.
Oceanic Fish. Invest. Rep. 9:2.3-45.
Brodeur, R. D.
1982. Food habits, dietary overlap and gastric evacuation
rates of rockfishes (Genus Sebn.sles). MS Thesis, Oregon
State Univ., Corvallis, 102 p.
Calovv, p.
U)77. Ecology, evolution and energetics: a study in metabolic
adaptation. Adv. Ecol. Res. 10:1-62.
Calow, p., AND J. B. Jennings.
1 977. Optimal strategies for the metabolism of reserve mater-
ials in microbes and metazoa. J. Theor. Biol. 65:601-603.
Carlson, H. R., and L. Barr.
1977. Seasonal changes in spatial distribution and activity of
two species of Pacific rockfishes, Sebn^ften flnndns and S'.
ciliatvs in Lynn Canal, southeastern Alaska. Mar. Fish.
Rev. 39(3):23-24.
Dawson, A. S., and A. S. Grimm.
1980. Quantitative seasonal changes in the proteins, lipid and
energy content of the carcass, ovaries and liver of adult
female plaice. Plfumn/'ctf's |ll^t('!<^ta L. J. Fish Biol. 16:493-
504.
Delahi'NTY, G., and V. L. de Vlaming.
1980. Seasonal relationships of ovary weight, li\er weight and
fat stores with body weight in the goldfish, ( 'a nissius iinriitiis
(L.). J. Fish Biol. 16:.5-13.
Derickson, W. K.
1976a. Introduction to the symposium: lipi<ls in animal life
histories. Am. Zool. 16:629-630.
1976b. Lipid storage and utilization in rej)liles. Am. Zool.
16:711-723.
DE Vlaming, V, L., G. Grossman, and F. Chapman.
1982. On the use of the gonosomatic index. Comp. Hiochem.
Physiol. 73A:31-39.
Diana, .J. S., and W. C. MacKay.
1979. Timing and magnitude of energy- deposition and loss in
the body, liver, and gonads of northern pike (Esax IkcIus). .1.
Fish. Res. Board Can. 36:481 487.
DOTSON, R. C.
1978. F^at deposition and utilization in albacore. In G. D.
Sharp and A. E. Dizon (editors). The physiological ecolog\- of
tunas, p. 343-355. Acad. Press, N.Y.
FoLTZ, J. W., and C. R. Norden.
1977. Seasonal changes in food consumption and energy con-
tent of smelt {OsmcnLs nidrdajc) in Lake Michigan. Trans.
Am. Fish. Soc. 106:230-234.
Glebe, B. D., and W. C. Leggett.
1981a. Temporal, intra-population difference's in energy allo-
cation and use by American shad (Alona xaiiidi^shiui) during
the spawning migration. Can. ,1. Fish. Acjuat. Sci. 38:795-
805.
19Xlb. Latitudinal differences in energy allocation and use
during the freshwater migrations of American shad (Alomi
snpidi'^xivw) and their life history con.se(]uences. Can. .1.
Fish. A(iuat. Sci. 38:806-820.
(il'Il.I.EMOT, p. .1.
1982. Seasonal cycles of fat content and gonad volume in
species of northern California rockfish (Scorpaenidae: Si-hiis-
tcs). MA Thesis, San Francisco State Univ., San Francisco,
167 [1.
Gl'NDERSON, I). R.
1977. I'opulation biology of Pacific ocean [lerch, Sf6o.s7c.s-
alutu.s, stocks in the Washington-Queen Charlotte Sound
region, and their response to the fishery. Fisli. Bull., U.S.
75:369-403.
Gunderson, D. R., p. Callahan, and B. Goiney.
1980. Maturation and fecundity of four species of Sebafstex.
Mar. Fish. Rev. 42(3-4 ):74-79.
Gunderson, D. R., and T. M. Sample.
1980. Distribution and abundance of rockfish off Washington,
Oregon, and C'alifornia during 1977. Mar. Fish. Rev. 42
(3-4):2-16.
310
GUILLKMOT KT AL.: SEASONAL CVCLKS IN CALIFORNIA R(X:KFISH
Helvey, M.
1982. First obsen'ations of courtship behavior in rockfish,
genus Sefcastes. Copeia 1982:763-770.
Hl'NTER, J. R.. AND R. LEONC.
1981. The spawning energetics of female northern anchovy,
Enffraulit vurrdax. Fish. Bull., U.S. 79:215-230.
Iles. T. D.
1974. The tactics and strategy' of growth in fishes. In F. R.
Harden-Jones (editor), Sea fisheries research, p. 331-345.
Wiley. N.Y.
Kleinbai'm, D., and L. Kitpek.
1978. Applied regression analysis and other multivariable
meth(Mis. Duxbury Pre.'^s, North Scituate, Mass., 556 p.
Lasker, R.
1970. Utilization of zooplankton energy by a Pacific sardine
population in the California Current. In J. H. Steele (editor).
Marine focnl chains, p. 265-284. Oliver and Boyd. Edinb.
Lasker, R.. and P. K. Smith.
1977. Kstimation of the effects of environmental variations on
the eggs and larvae of the northern anchovy. Calif. Coop.
Oceanic Fish. Invest. Rep. 19:128-137.
Lawrence, J. M.
1976. Patterns of lipid storage in post-metamorphic marine
invertebrates. Am. Zool. 16:747-762.
Love. M. S.
1981. Evidence of movements of some deepwater rockfishes
(Scorpaenidae: genus Sebnttfes) off southern California.
Calif. Fish C.ame 67:246-249.
Love, M. S.. and W. V. Westphal.
1981. (Jniwth, repnwiuction. and food habits of olive rockfish,
Srhds/t's sirnniiiidi's. off central California. Fish. Bull, LI.S.
79:533-545.
Lo\K. R. M.
1970. The chemical biology of fishes: with a key to the chemi-
cal literature. Acad. Press, Lond., 547 p.
MacCrecor. .1. S.
1970. Fecundity, multiple spawning, and description of the
gonads in St'h(ist(i<lfn. U.S. Fish Wildl. Serv., Spec. Sci. Rep.
Fish. .596. 12 p.
M.m-Kinnon, J. C.
1972. Summer storage of energy and its use for winter meta-
l)olism and gonad maturation in American plaice {Hippoglos-
s„i,h-s i,lnlr^x,ii(h'!<). .]. Fish. Res. Board Can. 29:1749-1759.
MdSER. H. C..
1967. Reproduction and development oi' Seba.itodes pauciftpi-
ins and comparison with other rockfishes off southern Califor-
nia. Copeia 1967:773-797.
Newsome. C. F.. and (;. Leduc.
1975. Seasonal changes of fat content in the yellow perch
(Perm jhiirsct'iis) of two Laurentian lakes. .J. Fish. Res.
Board Can. 32:2214-2221.
Parrish. R. H., C. S. Nelson, and A. Bakin.
1981. T'ransport mechanisms and reproductive success of
fishes in the California current. Biol. Oceanogr. 1:175-203.
Patzner, R. a.
1980. Cyclical changes in weight and fat condition of the liver
and their relationship to reproduction in the hagfish Eptatre-
fiis hiirgeri (Cyclostomata). Acta Zool. 61:157-160.
Pereyra, W. T., W. G. Pearcy, and F. E. Carvey, Jr.
1969. Sebasl(Hles Jloriduii, a shelf rockfish feeding on meso
pelagic fauna, with consideration of the ecological implica-
te .ns. ,1. Fish. Res. Board Can. 26:2211-2215.
Phillips, J. B.
1957. A review of the rockfishes of California (family Sror-
paenidae). Calif Dep. F'ish Came, Fish Bull. 104. 158 p.
1964. Life history studies on ten species of nK'kfish (Genus
Sebastodes). Calif Dep. Fish Game, Fish Bull. 126, 70 p.
Pierce, R. J., T. E. Wissinc;, .J. G. .Jaworski, R. N. Givens, and
B. A. Megrey.
1980. Energy storage and utilization patterns of gizzard shad
in Acton Lake, Ohio. Trans. Am. Fish. Sfx;. 109:611-616.
Roberts, D. A.
1979. Food habits as an ecological partitioning mechanism in
the nearshore rockfishes (Sebastes) of Carmel Bay, California.
MA Thesis, San Francisco State L'niv., San Francisco, 74 p.
Robertson, 0. H., and B. C. Wexler.
1960. Histological changes in the organs and tissues of migra-
ting and spawning Pacific salmon (Genus Oncorhynchua).
Endocrinology 66:222-239.
Shchepkin, V. Ya.
1971a. The dynamics of lipid composition in the Black Sea
horsemackerel [Trachmrus mediterraneus ponticus (Aleev))
in relation to maturation of the gonads and spawning. J.
Ichthyol. 11:587-.591.
1971b. Dynamics of lipid composition of the scorpionfish
[Sro'r'paena pwrva (L.)] in connection with maturation and
spaw'ning. J. Ichthyol. 11:262-267.
Shevchenko, V. V.
1972. Dynamics of the content of dr\- fat-free residue and of
lipid content in the body and organs of the North Sea haddock
[Melanogrammus aeglefinus (L.)] in the course of growth and
gonad maturation. J. Ichthyol. 12:830-837.
Shul'man, G. E.
1974. Life cycles of fishes: Physiology and biochemistry.
Wiley. N.Y., 258 p.
Slobodkin, L. B.
1962. Energy in animal ecology. Adv. Ecol. Res. 1:69-101.
Smith, P. E.
1978. Biological effects of ocean variability: time and space
scales of biological response. Rapp. P.-v Reun. Cons. int.
Explor. Mer 173:117-127.
Sorokin, V. P.
1961. The redfish; gametogenesis and migrations oi Sebastes
mannus (L.) and Sehnates mentnlla Travin. Rapp. P.-v.
Reun. Cons. int. Explor. Mer 150:245-250.
Tyler, A. V., and R. S. Di'nn.
1976. Ration, growth, and measures of somatic and organ
condition in relation to meal frecjuency in winter flounder,
Paeiidopleuronectes omericanus. with hypotheses regarding
population homeostasis. J. Fish. Res. Board Can. 33:63-75.
Westrheim, S. J.
1975. Reproduction, maturation, and identification of lar\ae of
?,ome Sebastes (Scorpaenidae) species in the northeast Pacific
Ocean. J. Fish. Res. Board Can. 32:2399-2411.
WlLKlNS, N. P.
1967. Starvation of the herring, Clupeo harengus L.: Survival
and some gross biochemical changes. Comp. Biochem.
Physiol. 23:.503-518.
WOOTTON, R. J., AND G. W. EVANS.
1976. Cost of egg production in the three-spined stickleback
(Gasterosteus acukatus L.). J. Fish Biol. 8:385-395.
311
THE POSSIBLE INFLUENCE OF WARM CORE GULF STREAM RINGS
UPON SHELF WATER LARVAL FISH DISTRIBUTION
G. R. Flierl' and J. S. Wkoblewski=*
ABSTRACT
We propose a simple one-dimensional mixlel for examining the impact of warm core riiij^s upon the larval
fish distribution and abundance over the continental shelf off the northeastern United States. The model in-
cludes (in a cross-shelf averaged sense) the loss of larvae due to biological causes of mortalit^t', the advective
transport of larvae due to the mean down-shelf currents, and the changes in larval density pnxiuced by the
on-shelf or off-shelf flow s t)ccurring when a ring approaches the shelf-slope front. The results of this highly
idealized mt)del indicate that the decreases in larval abundance caused by cross-shelf flows may be as large
as those caused by biological factors and, furthermore, the effects are strongly dependent upon the rate of
motion of the ring. A stationary ring may cause a 20 to 50% drop in abundance, depending on the strength
and size of the ring and on the longshore velocity in the shelf water. When the ring is slowly moving, the im-
pact can be even greater: a patch of larvae being advected downshelf by the longshore current could, when
catching up to the back side of an eddy, essentially be swept off the shelf, decimating the patch.
Model predictions are compared with historical MARMAP data of larval cod and haddock density in the
Georges Bank area. There does appear to be a relationship between the frequency of ring interactic)n with
Georges Bank and the subsequent year-class strength of cod and haddock stocks. Thus we suggest that fur-
ther investigation of the impacts of rings is warranted, both from the observational and the theoretical view-
points. These studies should include detailed measurements in entrainment features, further analysis of
ring-Bank interactions factoring in the closeness of the ring, the strength of its currents and its translation
rate, and more detailed modelling of entrainment events and larval fish ecology.
Warm core rings form in the Slope Water region be-
tween the North American continental shelf and the
Gulf Stream. These rings are eddies 100 to 200 km in
diameter which result when a Gulf Stream meander
separates from the main current. The potential im-
pact of warm core rings upon the continental shelf
ecosystem has become more apparent with routine
satellite infrared images of the sea surface. Charts of
sea surface temperature prepared from these im-
ages, e.g., Figure 1, (Halliwell and Mooers 1979;
Chamberlin 1981) frequently show rings entraining
cold water from the continental shelf. This interpre-
tation is supported by ship observations and current
meter records of water transport onto and off the
continental shelf induced by warm core rings
(Morgan and Bishop 1977; Smith 1978; Smith and
Petrie 1982). Physical and biological oceanographers
have long been aware of occasional intrusions of
anomalously warm water onto Georges Bank (for a
review, see Bolz and Lough 1981), which are now
likely to be attributable to warm core ring activity.
In 1961 Colton and Temple hypothesized that large
'Department of Earth, Atmospheric and Planetary Sciences,
Massachusetts Institute of Technology, Cambridge, MA 02139.
^Department of Oceanography, Dalhousie University, Halifax,
Nova Scotia, B3H 4J1, Canada; present address: Bigelow
Laboratory for Ocean Sciences, West Boothbay Harbor, ME 04575.
numbers of larval fish of shelf species can be drawn
off Georges Bank into warmer Slope Water where
they succumb to unfavorable environmental condi-
tions (c.f. Laurence and Rogers 1976).
The purpose of this paper is to examine theoreti-
cally the possible influence of warm core rings on the
abundance and distribution of larval fish in continen-
tal shelf waters off the northeastern United States,
in particular the shelf region associated with cod and
haddock spawning on Georges Bank. Our study
makes estimates of the advective losses of larvae
because of the entrainment of shelf water by an eddy
and predicts changes in larval density (the observ-
able quantity in ichthyoplankton surveys) because of
the onshore and offshore flows induced by a ring. We
also consider the possible biological causes of mortali-
ty (e.g., predation, physiological death). In other
words we wish to estimate the relative importance of
the physical and biological losses via a mathematical
model. While our model does not describe either in
great detail, we feel that it does indicate the impor-
tance of ring-induced entrainment and the
dependence of this effect upon the speed of transla-
tion of the ring, the width over which it interacts
with the shelf, and the strength of its currents at the
shelf break. We compare our model predictions of
the spatial and temporal distributions of larval fish
Manuscript accepted October 1984.
FISHERY BULLETIN: VOL. 83. NO. 3, 1985.
313' Jd
with the historical MARMAP (Maritime Resources
Monitoring, Assessment and Prediction) data of lar-
val cod and haddock distributions in the Georges
FISHERY BULLETIN: VOL. 83, NO. 3
Bank area (Smith et al. 1979). We also present an ap-
parent relationship between years of low warm core
ring activity and strong year classes in the fishery.
Fh.vrk 1 . - Distribution of warm core rinps off the I'.S. northeast foiist durin};; the weei< of 1 1 May 1977.
The chart was pnxluced by the U.S. Naval Oceanographic Office from infrared satellite images.
314
P'l.lFRI. AXinVRORI.FWSKI: WARM CORK (H'I.K STKKAM RINCS
Finally, we make recommendations for further
investigations of the influence of warm core rings on
the northeast coast marine ecosystem.
Our very simplified modelling approach to the
problem of resolving biological distributions in a
variable oceanic tlow regime could, with proper
reparameterizations, be applied to estimating the im-
pact of rings on chemical distributions as well -an
example would be determining the distribution of
pollutants dumped in deepwater dumpsite 106. For
variables which do not behave as passive particles in
the flow, the model has limitations. Vertical migra-
tion behavior by fish larvae may play an important
role in their distribution which is not resolved by our
preliminary modelling. Other potentially important
details, such as the mechanism for mixing on the
shelf, have also not been included in this first,
simplified calculation. Nevertheless, we feel that the
results are extremely suggestive, indicating ways to
examine existing data sets and hypotheses to be
tested in future field studies.
THE MODEL
There are many possible approaches to modelling
the effects of rings upon fish larvae, ranging from
simple order-of-magnitude estimates to complex
physical models which predict the mean and varying
currents from winds, heating, topography, and coast-
lines. The water motions could then be coupled with
complex biological models of spawning, predation,
growth, and mortality. However, we are not yet at
the stage where such a full-scale calculation is really
justifiable; we do not understand enough about the
physics of the shelf-slope region and the rings or
enough about larval fish biology to ensure that only
important processes are included and that these are
being properly represented in our numerical model.
In addition, the questions we wish to address are
fairly simple ones: How large could the impact of
rings upon larval fish populations be and how do
these impacts depend upon the flow structure and
translational speed of the rings? We, therefore, shall
take the simplest approach to the problem of esti-
mating our primary variable, the larval fish density
(or abundance). The various processes which affect
the population distribution will be represented in the
model in an almost schematic form. The actual popu-
lations vary in all three dimensions and in time, but
we shall include only the downstream and time vari-
ations in the model. Likewise, the actual current pat-
terns are quite complicated and we choose only to
represent the impact of the ring-induced currents by
a specification of the flow at the outer edge of the
shelf, with onshore flow ahead of the ring and off-
shore flow behind the eddy. The mean downshelf
drift currents will also be included. The biological
processes of predation, physiological mortality, and
metamorphosis out of the planktonic larval stage will
be represented simply as a loss rate f^ which will be
assumed to be independent of space or time. With
these simplifications, the general equation governing
the density n{x,y,z,t) of the planktonic larvae can be
reduced to a manageable form
d d d d
— n + — un + — im + — wn = - [xn.
dt dx dy dz
(1)
We shall use the geometry shown in Figure 2 with x
the downshelf coordinate, y the offshore coordinate.
/SOURCE
OF 5
X . ■ . M-ARVAE J
Figure 2. -Schematic diagram of the geometry
assumed in the mathematical model. Y is the shelf
width, h is the average depth, and U is the average
longshore velocity of the shelf w^ater.
315
FISHERY BULLETIN: VOL. 83, NO. 3
and z positive upwards. We shall assume that there is
a source of larvae somewhere upstream of x = 0,
e.g., the spawning grounds on Georges Bank,
leading to a specified flux of organisms into the
domain at the x = 0 boundary. Alternatively, and
more conveniently, the upstream spawning can be
thought of as leading to a specified abundance of
organisms A^q (^) ^^ ^ = ^•
Although we could, in principle, specify the three-
dimensional currents and the source function Aq
from either measurements or models, the available
data and models are not really adequate for this to be
possible. We have chosen, therefore, to simplify the
model further by averaging the larval fish density
vertically and across the shelf
A(x,0 =
hY 3„ 3_
nix,y,z,t)dzdy.
(2)
Here Y is the width of the shelf and h is the depth
(both assumed independent of x). We can find the
equation governing this N by averaging Equation (1)
over the shelf width and depth, applying boundary
conditions of zero flux through the upper and lower
surfaces and the continent side of the domain. This
gives
— A +
dt
— \ I w^ dz dy I
hY 3„ 3_, J
hY 3-
+ _ I v(x,Y,z,t)n{x,Y,z,t)dz= -t^N. (S)
hY y,
The downstream variation of Y and h has been
neglected although it is not too difficult to include it.
The term representing downstream advection of lar-
vae will be simplified by assuming that the cross-
shelf mixing of larvae is sufficiently intense that n is
uniform in y. The along-shelf advection term then
becomes
d 1
dz hY
n -a
un dz dy = — UN;
, dx
U{x,t) = —
hY
— \ \ u{x,y,z,
^Y 3o ) k
t) dz dy.
(4)
Similarly, we shall ignore vertical variations in n at
the shelf edge so that the flux off the shelf becomes
hY ) ,
— \ v(x,Y,z,t) n(x,F,z,0 dz =
hY y . Y
V,{x,t) =
h:
v{x,Y,z,t) dz.
(5)
Here VQ{x,t) is the depth-averaged onshore-offshore
flow (positive offshore) and A, is the depth-averaged
larval fish density in the water which is moving onto
or off of the shelf. (Vertical migratory behavior
which is somehow correlated with vertical shears
would alter this parameterization of the outflowing
flux of larvae.)
When there is onshore or offshore flow, the aver-
aged velocity along the shelf cannot be constant. The
variations in U can be calculated from the conserva-
tion of fluid volume integrated across the shelf
dx
— I I u dz dy\
hY 3o 3_, J
^0
u dz dy\ + — =0
which implies —
dx
V,
(6)
Finally we must introduce a parameterization for
the density of larvae carried on or off the shelf at the
edge A, in terms of the average density N{x,t). It is
assumed that the Slope Water pushed onto the shelf
by the ring is devoid of shelf fish larvae. If we
presume that this Slope Water mixes completely
with the shelf water, then the water leaving the shelf
carries larvae with density A, as sketched in Figure
2. These considerations suggest that the entrain-
ment term can be modelled by
N.=
0 for Vn < 0
A for Fn > 0
(7)
(Again, we must remark upon the limitations of the
present calculation; certainly the shelf water is not
thoroughly mixed and the density of the outflowing
larvae is much more complicated and perhaps
smaller on the whole than this formula would sug-
gest. We hope that our results will spur further
modelling and observational efforts to assess the pro-
cesses we have been forced to represent so crudely.)
When all of these simplifications are gathered
together, the approximate equations for the average
density of larvae N{x,t) become
10 for Fo < 0
VoN ] = -1^
for Fo > 0
316
Fl.lKRLAN'U\VKOKLh;\VSKl:\VAKiVU'OKK(;ri.FSIKKAMKlN(;s
dU _ ^0
dx Y
with the boundary condition
iV(0,0 = iVo(0.
STATIONARY EDDIES
(8)
(9)
In nature, there are pulses of larvae entering the
domain as the fish spawn. In addition, the shelf-edge
velocities V^){x,t) are changing as mesoscale eddies
and Gulf Stream warm core rings impinge upon the
shelf. We shall present in the section on moving ed-
dies several numerical solutions of Equations (8) and
(9), simulating this complex situation. However, in
order to fully understand the importance of the rings
and eddies in determining the fish larvae's spatial
distribution, it is first useful to consider some
simpler, analytically tractable cases. We shall begin
by discussing the distributions which occur when the
shelf-edge flows are not changing with time, i.e., the
eddies are stationary. This problem also has bearing
on the real situation south of Long Island, where
rings may often stop for considerable lengths of
time.
As a first example, consider the larval fish distribu-
tion which would occur in the absence of any biolo-
gical loss processes (f^ = 0) and when the source term
A^Q is independent of time. The resulting equations
dx
iUN) =
N
Fo — foryo>0|
Y
for F„ < 0
au
dx
Y
(10)
can be solved readily
where f/,, is the longshore velocity and N,, is the
(time-independent) population density at the
upstream boundary x = 0. We can now see explicitly
the effects of the physics alone upon the larval fish
distribution. In the regions where the flow is onto the
shelf (Equation (11a)), the shelf break boundary con-
tribution to Equation (10) is zero. But the effects of
the tlow field are still felt in that the along-shelf flow
is divergent. U increases downstream as water
comes onto the shelf, spreading out the larvae and
reducing their average density. In contrast, when
the flow is offshore (Equations (lib) or (lie)), there
are direct loss terms due to larvae being carried off
the shelf. Some of the water flowing into a section
are diverted offshore while some continues down the
shelf, with the larvae separating in the same propor-
tions. Thus, although there is a decreased flux down
the shelf, this does not affect the density since there
are no biological losses which need to be balanced by
this flux. The net effect is that the physics by itself
does not change the population density in regions of
offshore flow (Equation (lib)). The only exception
would occur when the offshore transport (/ F,, dx) is
sufficiently strong so that all of the normal
alongshore flow (f/,, Y) is diverted off the shelf. In
this case (Equation (lie)), the flow in regions farther
down the shelf is reversed and the water moves up
the shelf. Since this water is from regions without
. sources of larvae, the population density is zero.
By putting together these two results, we can con-
struct a picture of the density of larvae in continental
shelf water flowing past a stationary ring centered
a.tx = D. This is shown in Figure 3. For these calcu-
lations we have used
n =
,x- D
■A exp
[2 2 L' ]
(12)
with A = 20 cm/s the peak offshore velocity) and L
= 20 km (so that roughly 80 km along the shelf is
strongly influenced by the ring currents). This figure
A^ =
'A^o
Nn
U
N,a
o"-^o
C/n
S
Va
0 Y
if Fo < 0
if Fo > 0 and U^ >
if F„ > 0 and Uo <
Va
Y
(11a)
(lib)
(lie)
317
FISHERY BULLETIN: VOL. 83, NO. 3
^1
No
<
>
<
O
z
<
o
z
m
<
0)
H.;
DISTANCE -
DOWNSTREAM
X (KM)
500
20
OFFSHORE
cm/s
ONSHORE
-20
Figure 3. -The steady state abundance of fish larvae with
distance aion^ the shelf. This abundance is expressed as a frac-
tion of the number of larvae continuously being produced at the
spawning site, Nq. There is a 80 km wide, stationary eddy at the
shelf edge, inducing onshore and offshore flows of 20 cm/s. The
longshore velocity Uq of the shelf water is 5 cm/s. Biological
losses (f.() are set equal to zero. The dotted line shows the steady
abundance of fish larvae with distance down the shelf when
there is no eddy present.
shows only the spatial distribution of larval density in
the water moving down the shelf, as affected by flow
convergences or divergences associated with the
physics of the ring. The flux of larvae off the shelf
(not shown) is given by V',, hN,^ in the regions where
Vo is greater than zero and amounts in total to
i
Vq h N^^ dx ^ A hL N^e
}k
66% of the flux into the domain (L^,, A^,, hY) at x = 0.
Next, we shall see that the physics and biology ac-
tually interact to produce a greater net impact than
when either is considered separately.
For this second model problem, we shall still use a
steady onshore and offshore flow pattern, but now
include the biological loss term and the time-depen-
dence in the source function Nq. When the flow is off-
shore or zero, the population distribution is given by
N{x,t) = NS- T)e'
(13a)
whej-e the variable t measures the length of time
necessary to reach the point x from the upstream
edge of the domain. In general r is given by
T =
s
' rfo:'
., U{x)
(13b)
where U{x) can be found by integrating the mass
conservation equation
U{x) = f/o- \ dx —.
i
(13c)
In the absence of ring-induced onshore-offshore
flows (V,) = 0), however, t is just equal to xlU^^ and
N{x,t) = iVo [t
1 ilL\
(13d)
The population at any downstream point lags that at
the origin by the travel time xIUq and has also
decayed exponentially during its travel. This solution
is an important base case for understanding the
distributions in a spawned patch which has not been
impacted by rings.
When water is being drawn off the shelf, the along-
shelf decay in concentration is again purely due to
travel time, since the effect of losses off the shelf on
the density is compensated for by the convergence.
However the spatial density of the larvae is still
noticeably altered by the offshore flow because the
travel time necessary to reach any point is increased.
This occurs because U is decreasing with i- as a result
of the advection of water off the shelf (as shown in
Equation (13c)). Since U is less than Uq, the travel
time T in Equation (13b) is necessarily greater than
that in the absence of the ring (xlU^^). We have
sketched t(x) for the three possible signs of F,, in
Figure 4a. These results suggest that there will be an
enhanced spatial decay rate of larval density in the
regions where the flow is offshore.
318
KLIKKL AND V\ KOBLliW SKI: WARM ('(IKK ( ;r 1 ,K STKKAM KINGS
100
o
OL
2 T
2 (days)
cr
t-
<n
z
$
g 501-
o
H
UJ
2
5
EC
»-
a
Vo • 20CM/S
Vo -q,^
Vq .-20CM/S
LONGSHORE DISTANCE X (K M )
500
Figure 4. -a) The travel time t necessar\' for lanae to
reach the point x down the shelf from the spawning site at x
= 0. The values of t are computed in the absence of an eddy
(Vq = 0) and when an eddy induces onshore ( Vq = - 20
cnVs) and offshore (Vq = 20 cm/s) flows, b) The rate of
change in numbers of larvae N with distance down the shelf
X, plotted against longshore position for the three values of
LONGSHORE DISTANCE (KM)
500
When the flow is onshore (y,, < 0) we can also solve
Equations (8) and (9) and find
N{x,t) = N,it - t)
U{x)
(14)
In this case, the timelike variable t increases less
rapidly with x than in the base case. This alone would
lead to a slower spatial decay; however, the dilution
effect (the UJU factor) counters this. In most cases,
the dilution will be stronger than the effects of
decreased transit time.
Perhaps the simplest way to see this is to consider
the downstream decay rates when the source of lar-
vae is constant in time and the onshore or offshore
flows are spatially uniform. The spatial decay rates
- ( dN/dx)/N for the three flow cases are
I c/„
for Fo = 0
1 dN
N dx
u
for Fo > 0
\
+
1
dU
for Vq < 0.
(15)
U U dx
We have plotted these as functions of x in Figure 4b
using /^ = 10""^ s""', U^) = 5 cm/s, Vq = ±20 cm/s, and
Y = 200 km. With this value for fu, two-thirds of the
larvae disappear from the population because of the
various biological causes within 4 mo from hatching.
Most values of ^x in the literature (e.g., Sissenwine et
al. 1983) tend to be higher (see, however, Peterson
319
FISHERY BULLETIN: VOL. 83. NO. 3
and Wroblewski 1984), but it is important to
remember that these also include the advective
losses. We have therefore chosen a smaller value of ^u
to reflect only biological processes; alternate values
N
of /i will be considered shortly. The graph shows the
extreme situation where the inflow or outflow is
uniform over the whole downstream distance. The
decay rate with distance travelled is always increas-
ed for offshore flow. For onshore flow, the decay rate
can be reduced below the "no-ring" case but only
very far downstream (x > 500 km) where the flow
rate down the shelf is huge {U = 30 cm/s). Since on-
shore flows of 20 cm/s over a 500 km stretch of shelf
are not likely to occur, we can conclude that the
spatial decay rate will be enhanced in both the
regions of onshore flow and the areas with offshore
flow.
The net result, when a stream of larvae moving
down the shelf and declining in density due to biolog-
ical losses encounters a stationary eddy, can be calcu-
lated by combining the result for offshore flow in the
region 0 < x < Z> with the one for onshore flow in x >
D where the ring is centered at the point x = D.ln
Figure 5 we compare the solution without the eddy
N
exp
-fXX
(16)
to that with the eddy
exp(-MT)
UiD)
forO<x<D
Uix)
exp {-^AT)forD < x<W
, T =
s
' dx'
0 U{x')
(17)
where W is the length of the shelf domain, taken to
be 500 km. Most of the decrease in population den-
sity occurs in the onshore flow regime; the final den-
sity is only half of that which would occur in the
absence of the eddy. In assessing the causes of the
population decrease, it is clear that the physics and
the biology play comparable roles: the decrease in
density when there is no eddy is a factor of two dur-
ing the transit down the shelf (Fig. 5). The changes
in density which occur predominantly in the region
of onshore flow when the currents are present, give
another factor of 2.5 decrease. Note that recruit-
ment cannot be inferred directly from these density
patterns; we will address the implications for recruit-
ment in the section on Moving Eddies below.
We summarize the impact of stationary rings for
various values of the onshore-offshore flow rates and
the scale length along the shelf impacted in Figure 6.
Here we plot contours of the ratio of the population
density far downstream of the eddy (N ) to that
N_(Vo • 0)
No
Figure 5. - Same as Figure 3 except biological lo.sses {^/ = 10
s" ) are included.
-7
320
Kl.IKKl. AMI WKOUl.KWSKI: WAKMCORE GULF STKKAM KINGS
which would be present without any cross-shelf cur-
rents (A^^, y,i = 0). This figure shows clearly the in-
creasing impact with stronger transports onto or off
of the shelf edge. There are slight differences in this
ratio if the biological decay is ignored and if the
cross-shelf flows occur over large distances, since the
longshore flow slows down significantly. We should
note that the decrease in larval fish density com-
pared with the no-ring case depends on two nondi-
mensional parameters Pq = ALIUqY and Pj =
\jiLIU(t. Thus for values of ^, L^o. or Y other than 10""^
s"\ 5 cm/s, and 200 km, the graph can be read with
suitable values of A and L to give the desired values
for these two nondimensional numbers:
^graph = -Pi X 500 km = "— X 500 km
region influenced by the ring's cross-shelf flows while
the longshore current speed is maintained. P^igure 6
shows clearly that such an increase in L will cause a
greater reduction in larval density downstream of
the eddy. As the eddy translation rate becomes
closer and closer to the flow rate on the shelf (effec-
tively increasing L in Figure 6), the effect upon the
population becomes larger and larger, until even-
tually the eddy is drawing all of the larvae off the
shelf as it passes. This occurs when the ring's speed is
great enough so that the longshore transport of
water relative to the ring is smaller than the offshore
transport induced by the currents at the shelf edge:
C/n
C<
Uo
s:
Y
dx
(18)
P A
A , = — X 2 cm/s = — X 2 cm/s.
^gjaph
Pi \^y
MOVING EDDIES
In the previous examples, we have considered the
changes in fish larvae distributions which occur when
the shelf water flows by a stationary eddy. But rings
frequently translate to the southwest, following a
track between the continental slope and the Gulf
Stream. The translational speeds vary considerably,
ranging from a few cm/s to perhaps 10 cm/s. This
along-shelf ring movement has a profound influence
on the ring's contribution to decreasing the concen-
tration of larvae- in some cases, they may be swept
offshore in the entrainment flow of a slowly trans-
lating ring; in other cases the ring may catch up to,
dilute, and pass the organisms. Finally, if the ring
and shelf water are moving at the same rate, the lar-
vae may never experience the impact of the ring, or
alternatively may be in a region under constant
influence.
The physical effects of a moving ring upon the lar-
val fish population can be estimated readily from the
previous results; it is only necessarj' to remember
that the important quantity is the rate at which the
shelf water moves relative to the eddy. If the ring is
propagating westward more slowly than the west-
ward drift of the shelf water, the organisms are in
contact with the ring for longer periods of time, cor-
responding to a decreased value for the effective cur-
rent [/q- But decreasing the effective downstream
flow rate while keeping the eddy size constant is
equivalent to increasing the length scale of the shelf
where c is the speed of translation of the ring.
If the ring is moving faster than the shelf currents,
the situation is somewhat different; now the eddy
catches up to the larvae and they are first influenced
by a region of onshore flows and then by offshore
currents. We can calculate the impact upon the
population using the same methods as were
employed in deriving Equation (10). For simplicity,
we consider a domain which is infinite in x and com-
pare the population density in regions which have
not felt the ring with that in regions which have pass-
ed through the ring. For a ring moving at speed c,
the equations describing the effects of the currents
upon the population are
10
o
o
o
-i
u
>
u
X
(/)
I
w
o
cc
o
50
40-
30
20
O
H- •
10-^ S-'
Uo =
5 cm/s
Y ■
200km
^-^N.
(Vo-
■ 0)
0.75
0 10 20 30 40 50
L
LENGTH SCALE IMPACT (KM)
Figure 6. -The ratio of the number of larvae present far down-
stream of the eddy N^ to the number present if there were no eddy,
N^( Vq = 0). Contours of the ratio are plotted for different values of
eddy size (L) and cross-shelf velocity A.
321
FISHERY BULLETIN: VOL. 83, NO. 3
dx
[(U-c)N] =
dU _
dx
-Fn
V,
N
for Vo > 0
for V. < 0
(19)
and the population change caused by the eddy when
the downstream flow is sufficiently faster than the
ring's translation rate is
N(-oo)
-;i
V,{x,0)
y„>o ^0 - c
v.. dx
dx,
c<a
0
(20)
>o
When the flow stagnates relative to the ring at some
point, we have
N(oo) = 0 U,
Y
i
V,,dx<c<Uo (21)
X)
and when the ring is moving faster than the shelf
waters
Ni-°o) - N(oo)
N{oo)
il
Vo dx
^ Jv„>o
c - [/,, + -
^ Jv.r->o
OUa.
\i
Vq dx
These are plotted in Figure 7. Notice that the ring
may cause substantial losses in the population,
especially when its speed is roughly matched to the
mean flow on the shelf.
In principle, one could write down an analytical
solution to the full problem (Equations (8) and (i))),
including a translating ring and a time-dependent
source at the upstream edge of the domain.
However, this is a rather cumbersome calculation,
and we have chosen instead to solve these equations
numerically and simply present representative pic-
tures here of the ring induced effects when a cohort
-a single patch of larvae spawned roughly simul-
taneously - moves down the shelf and is disturbed by
a ring. Some care is necessary in selecting a
numerical scheme, since centered differencing is
100
\ loss ol
population
^a--b\ Vo di
X,>0
PHASE SPEED C
Figure 7. -Percent of the total number of larvae produced at the
spawning site which are ultimately lost when a moving eddy is pres-
ent at the shelf edge. When the speed c of the eddy is greater than
Uq - 1/Y /" Vq, all the larvae advected along the shelf are drawn
offshore. When the ring is moving faster than the down-shelf cur-
rent Uq, the ring catches up to the larvae, which are then diluted
before being drawn offshore.
unstable while upstream differencing introduces a
numerical diffusivity (Roache 1972). This may not be
undesirable, since in reality one would expect some
mixing to occur along the shelf; but unfortunately
the diffusivity is spatially variable, being lowest in
the vicinity of the eddy, and this we do not want in
the model. We compromised by choosing a very
small grid scale (5 km) so that the effective diffu-
sivity is only 1.2 x 10*^ cm^/s. This is not completely
negligible, as shown in Figure 8a which plots suc-
cessive snapshots of the larval fish density at 15-d in-
tervals in the absence of any rings (the time step was
one-half day). The population at the beginning of the
domain is assumed to enter in a pulse
(22) A^o(0 = exp
(23)
The gradual decrease in the peak abundance and the
spread in width is caused by the numerical diffusion.
Also included in this figure are the simple cases add-
ing biological decay (Fig. 8b), a stationary ring (Fig.
8c), or both simultaneously (Fig. 8d). Note the large
decreases in density induced as the population passes
the ring and also the slower advection of the popula-
tion down the shelf so that the organisms down-
stream are half a month older than they would other-
wise have been (compare Figure 8b and 8d).
Finally, we show in Figure 9 two cases when a
moving ring interacts with a patch of larvae. In the
first case, the eddy is moving at 7 cm/s (faster than
the 5 cm/s drift rate of the shelf water), so that the
eddy catches up to the population and passes by it.
322
FI.IKRI. ANinVROBI.KVVSKI: WARM ('(^KK CUl.F STKKAM KINCS
Q DIFFUSION
r20
3 monlht
DOWNSTREAM
DISTANCE X
DIFFUSION
AND RING INTERACTION
500 Km
r\
• I
I
I
X (KM)
500
BIOLOGICAL DECAY AND
DIFFUSION
X (KM)
RING. BIOLOGICAL DECAY AND
DIFFUSION
500
500
'--20
Figure 8. - Time-dependent solution of the numerical model which includes a) the diffusion of a spawning group or cohort of larvae
as the patch is advected down the shelf. Snapshots are at 15-d intervals. Parameters u = 0, U,) = 5 cm/s, Ax = 5 km, and At = 0.5
d. b) Same as (a) except M = lO'^s"'. c) Same as (a) except a stationary ring is present at the shelf edge, with parameters A = 20
— 1 — 1
cm/s and L = 20 km. d) Same as (c) except jj = 10 s .
As the ring passes by, the patch of larvae is spread
out and distorted. Some losses do occur, but because
of the rapidity of the interaction, these are slight.
Comparison of this picture with Figure 8d shows
that the larval density at 4 mo is higher than that for
the stationary ring case. On the other hand, in the
case when the shelf flow is faster than the speed of
the ring (Fig. 9b), the impact of the ring is tremen-
323
FISHERY Bl'LLETIN: VOL. 83, NO. 3
RAPIDLY MOVING RING
(C • 7 cm/s)
SLOWLY MOVING RING
(C • 3 cm/s)
b
X (KM)
500
X (KM)
500
P'igure 9. -a) Same as Figure 8d except a moving ring is present at the shelf edge, with parameters A = 20 cm/s, L = 20 km, and c = 7
cm/s. b) Same as (a) except c = 3 cm/s.
dous. When the population catches up to the back
side of the eddy, the relative speed is so slight that all
of the organisms are diverted off the shelf and lost
from the system.
In addition to the plots of density versus time and
along-shelf distance, it is extremely useful to con-
sider the net balances for larvae within the domain.
By integrating Equation (8) over x and t, using Equa-
tion (9) to evaluate the starting point contribution at
X = 0. we can calculate the percentages of the total
incoming population which are removed from the do-
main by three processes. First, there are biological
decreases of the net population (due to the integra-
ted \jiN term). It is important at this point to recall
that we consider this as representing both larval
death and metamorphosis. Therefore the recruit-
ment should be roughly proportional to this term.
(We do not consider the development time history of
the larvae here; clearly this model could be combined
with more detailed and complex larval development
models to attempt more sophisticated recruitment
predictions.) Secondly, there are losses due to advec-
tion off the shelf by the ring currents, and thirdly,
larvae can be lost out the downstream end of the do-
main. The 500 km length of the domain puts the end
of the model region near Cape May; exiting larvae
may be swept offshore into the Gulf Stream and, like
those drawn off by ring currents, presumably be lost.
The magnitude of each of these terms is sum-
marized in Table 1 for the cases plotted in Figures
8b, d and 9a, b. Table 1 shows that the ring-induced
advective losses from the population can be as large
as or larger than the biological (mortality and meta-
morphosis) losses. This is most dramatic when the
ring is moving slightly slower than the shelf water
currents. The recruitment should vary in a fashion
similar to the integrated biological causes term in
Table 1; thus we expect a strong year class when
rings are not interacting with the shelf waters, a
reduction when stationary or rapidly moving rings
are present, and a very sharp decrease in recruit-
ment if a slowly moving ring is near the edge of the
shelf at the time of spawning and larval develop-
ment.
DISCUSSION
Theoretically, the passage of warm core rings close
Table 1.— Percent of total larval fish population entering the
domain. WCR = warnn core ring.
Advection
Advection
off the shelf
out of the
in
flows
downstream
In the
Biologi
cal
in
duced
end of
presence of
causes
by
a WCR
the domain
No ring
62
38
M = 10-^ s-''
Stationary ring
42
46
12
A = 20 cm/s
L = 20 km
Rapidly moving ring
54
29
17
c = 7 cm/s
Slowly moving ring
18
82
0
0 = 3 cnn/s
324
FLIERL AND WROBLEWSKl: WARM CORK CILF STRfc:AM RINCS
to the continental shelf should have considerable in-
fluence on the abundance and distribution of shelf-
water larval fish and consequently on their recruit-
ment to the fishery. Our simple mathematical model
suggests a major effect of the ring-induced cross-
shelf flows is to cause decreases in the larval density
ahead of the ring where there is onshore flow. In
addition, water being drawn off the shelf in an
entrainment feature behind the eddy can carry lar-
vae away, constituting a significant loss to the shelf
population.
Research scientists of the National Marine
Fisheries Service are currently investigating the fre-
quency of entrainment events and their impact upon
the fisheries (A. Friedlander^). Here we shall briefly
examine the published literature on ring distribu-
tions and larval fish surveys. We have used the
schematic charts of sea surface temperature pro-
duced by NOAA and ONR (Office of Naval
Research). All of these records are necessarily in-
complete due to cloudiness in the imagery and the
difficulties in inferring water motions from the sur-
face features. We therefore will make a somewhat
subjective estimate of ring importance by consider-
ing the persistence of various eddies and their close-
ness to the shelf.
Figure 10 is a composite of the observed
MARMAP distributions of cod Gadus morhua, lar-
vae in the shelf region near Georges Rank during the
late winter and spring of 1977 (Smith et al. 1979).
We have placed on this figure the approximate loca-
tions of the warm core rings shown on the Experi-
mental Ocean Frontal Analysis Chart produced by
the U.S. Naval Oceanographic Office for this period.
Figure 11 shows the corresponding MARMAP distri-
butions for haddock, Melanogrammus aeglefiniis,
larvae.
Four warm core rings had trajectory paths near
enough to Georges Bank during the spring spawning
period in early 1977 to have had significant impact
upon the larval fish distributions according to the
predictions of our model. In front of each ring shown
on Figures 10 and 11, the concentration of larvae
over the shelf appears to be relatively low, much as
our model suggests would occur in areas of ring-
induced onshore flow. There even appear to be
indications of entrainment of larvae off the shelf
behind rings 77E (Figs. 10c, lie) and 77 A (Fig. lid).
Unfortimately the MARMAP station grid does not
extend beyond the 200 m contour, so that this cannot
be confirmed from the historical data. Extending the
MARMAP grid further offshore would be of great
benefit in assessing losses of larvae both by rings and
by other offshore transports. It is also not possible to
differentiate between patchiness from concentrated
spawning upon Georges Bank or other biological
causes and ring-induced variations. Again this makes
the relationship between theory and data difficult to
assess.
Warm core ring 77 A (Figs. 10, 1 1) is an example of
a nearly stationary eddy, remaining adjacent to
Georges Bank from 30 March to 25 May 1977. But
according to our theory, ring 77E is potentially even
more dangerous, since it slowly sweeps down the en-
tire Georges Bank edge between 18 May and 6 July,
moving at 3-5 cm/s. Drifting groups of larvae could
have caught up to the back side of ring 77E and been
drawn off the shelf.
The survival of larvae in 1977 was low, and the
year class was weak for both cod and haddock (Ser-
chuk and Wood 1981; Clark et al. 1982). In other
years also, there appears to be a relationship be-
tween the frequency of ring interaction with
Georges Bank during the winter and spring spawn-
ing season and subsequent year-class strength for
both cod and haddock stocks (Table 2). Cod spawn on
Georges Bank from December into May and haddock
spawn from February into June (Smith et al. 1979).
Therefore we have examined the 6-mo period from
January to June each year from 1975 to 1979 for
ring activity using the charts of Bisagni (1976),
Mizenko and Chamberlin (1979a, b), Celone and
Chamberlin (1980), and Fitzgerald and Chamberlin
Table 2. — Apparent relationship between years of less fre-
quent WCR (warnn core ring) interaction withi Georges Bank
during the winter and spring spawning season and strong
recruitment of cod and haddock stocks.
'A. Friedlander, Northwest Fisheries Center Narragansett
Laboratory, National Marine Fisheries Service, NOAA, R.R. 7A,
Box .522A, Narragansett, RI 02882, pers. commun. January 1983.
No. of WCR's
interacting
Recruitment
during spawn-
Sti
-ength
ing season
(Jan.-June)
Year
Cod
Haddock
Comments
1975
Very
Very
1
Eddy 6 present
good
good
February-April
1976
Weak
Weak
3
WCR 751, 76A, and
76C detrimental:
76D too far
offshore
1977
Weak
Weak
4
WCR76F, 76G,77A,
and 77E all
detrimental
1978
Good
Very
good
1
WCR 78A present
in May; 78B too far
offshore
1979
Weak
Average
3
WCR 781, 79A, and
798 detrimental
325
FISHERY BILLETIN: VOL. 83, NO. 3
^ 7 7A,
- MARCH
'';'7 7'A
MARCH- APR IL
L- MAY
Figure 10. -Distribution and abundance of Atlantic cod, Gadus
nwrhua, larvae off the eastern United States during the latter part
of the 1976-77 spawning season (redrawn from Smith et al. 1979).
The solid outline of the bottom topography is the 200 m contour.
The positions of warm core rings 76G, 77A, 77E. and 77H are
replotted from Experimental Ocean Frontal Analysis Charts pro-
duced by the U.S. Naval Oceanographie Office on 25 February' (a),
23 March (b), 27 April (c), and 25 May (d) in 1977. The dots on (10a)
show the sampling locations.
MAY - JUNE
larva* / 10 m surface area
I- 10 \
1 1 - 10 0 \\\
10 1-500 :v.vV.
5 0 1-10 0 0 ■■■
326
FLIF,RI.AND\VR(1BLFVVSKI;\VAKM('()KK(;ri,FSTKKAM RINGS
<;7 7A'.
FEB- MARCH
MARCH - APRI L
JUNE
FlGi-RE 11. -Distribution and abundance of Atlantic haddock, Mdanogrammuf. aegkfinus, larvae off the
eastern United States durinjj the latter part of the 1976-77 spawning season (redrawn from Smith et al.
1979). The positions of the warm core rings are the same as in f^igure 10.
327
FISHERY BULLETIN: VOL. 83, NO. :i
(1981). The number of rings present in the Slope
Water is less important than the trajectories of the
rings. If they pass too far offshore or appear too
early or too late in the spawning season, they may
have little impact. It is difficult to measure the
magnitude of the onshore-offshore flows from the
remote sensing data, but we have tried to consider
the size of the shelf edge affected and the longshore
speed of the eddy when judging the strength of a par-
ticular interaction. Unfortunately, we have no infor-
mation for the years considered on the timing or
location of spawning which undoubtably is important
in determining the impact of individual rings.
The spring of 1975 was a time of low warm core
ring activity (Table 2), and both cod and haddock pro-
duced good year classes, essentially the best since
the 1960's (Smith et al. 1979). This high recruitment
was not due to large numbers of larvae being spawn-
ed; indeed, the abundance of cod and haddock larvae
was at a 5-yr low (Smith et al. 1979). Apparently, the
few larvae present on Georges Bank experienced
exceptionally high survival. There was only one ring
(designated eddy 6 by Bisagni 1976) which by our
model predictions could have influenced recruitment.
Eddy 6 was in the vicinity of Georges Bank from
February- through April but did not seem to be en-
training shelf water for this entire period.
During the spring of 1976 there were three,
possibly four, warm core rings interacting with
Georges Bank between January and May. Mizenko
and Chamberlin (1979a) presented the track lines for
eddies 751 (which later possibly became 76B), 76A,
and 76C. Rings with these trajectories had the poten-
tial to affect recruitment. The 1976 year class
strength for both cod and haddock stocks was weak
(Smith et al. 1979).
The spring of 1977 was a year of unusually high
ring activity. Figure 1 shows five rings (77A, 77C,
77E, 77G, and 77H) simultaneously present in the
Slope Water region on 11 May 1977. Mizenko and
Chamberlin (1979b) presented trajectories for all the
eddies observed in 1977. Of these rings, 76F, 76G,
77A, and 77E appear to be most detrimental. The
1977 year-class strength for both cod and haddock
stocks was again weak (Serchuk and Wood 1981;
Clark et al. 1982).
The relationship of low ring activity and high
recruitment observed in 1975 holds true again for
1978. This was a good year for cod and a very good
year for haddock recruitment (Serchuk and Wood
1981; Clark et al. 1982). Examining the trajectories
of warm core rings present during 1978 (Celone and
Chamberlin 1980), we find no rings interacting with
Georges Bank until late May or June. During the
60-d period from mid-February to mid-April, no anti-
cyclonic eddies were apparent off the northeast
coast. In late April and May, there were two rings
(78A and 78B), but they occurred too far south or too
far offshore to affect the Bank.
Finally in 1979, the most recent year for which
there are both fisheries recruitment data and trajec-
tory records, we find three potentially dangerous
rings: 781, impinging upon Georges Bank from
March to July (Fitzgerald and Chamberlin 1981) and
two eddies, 79A and 79B, lingering southwest of the
Bank from February through May. The 1979 year
class was weak for cod and only average for haddock
(Serchuk and Wood 1981; Clark et al. 1982).
CRITIQUE
According to our calculations, warm core rings
may have considerable influence on the distribution
and ultimate survival of cod and haddock larvae
spawned on Georges Bank. Our simple mathematical
model demonstrates the possible effects of cross-
shelf flows induced by a ring upon larval fish distri-
butions and abundance. The ring's size, strength, and
translation speed are critical in determining its
potential impact. A stationary ring may cause a 20 to
50% loss of larvae by inducing advective transport
off the shelf. If a ring is moving, the impact can be
even greater, especially for an eddy travelling long-
shore at a slightly slower speed than the shelf water.
In this most catastrophic case, a group of larvae can
catch up to the back side of the eddy and be entirely
swept off the shelf.
In briefly examining the published literature on
ring trajectories and fisheries recruitment statistics,
we have found what appears to be a relationship be-
tween years of frequent ring interaction with
Georges Bank during the late winter and early
spring spawning season and weak year classes of cod
and haddock. Our analysis can be criticized as cur-
sory and incomplete since we had no detailed infor-
mation on entrainment features or on many impor-
tant biological factors such as the timing and location
of spawning. Future studies may show this relation-
ship was fortuitous; however, our results certainly in-
dicate that future study is warranted.
An implicit assumption in our analysis of ring
events and fisheries recruitment data is that advec-
tive losses can affect year-class success. This has not
yet been demonstrated for the Northwest Atlantic;
however, Parrish et al. (1981) presented convincing
arguments that the dominant exploitable fishes off
the west coast have adopted spawning behaviors
which minimize losses due to offshore transport.
328
Fl.lKKI.ANDWKOHl.KWSKI; WARM Ci iKK CCLK S'I'KKAM kINCS
They suggested that deviations from normal trans-
port conditions may be a cause of the very large
recruitment variations observed in the fisheries for
sardine and anchovy. Whether warm core rings
represent anomalous conditions or whether the shelf
fishes of the Northwest Atlantic have adopted
spawning patterns which minimize the losses by en-
trainment is yet to be discovered.
G. Laurence-* has suggested that in some instances
vertical migratory behavior may prevent significant
numbers of larvae from being advected offshore. If
the entrainment feature is shallow and the fish lar-
vae avoid the surface layer, then the offshore trans-
port could be much less than predicted by our model.
The National Marine Fisheries Service is currently
surveying entrainment features associated with
warm core rings to assess the losses occurring off the
shelf. Recently, Wroblewski and Cheney (1984)
reported finding significant numbers of the white
hake, Urophycis tenuis, larvae 140 km seaward of
the Scotian Shelf break in Slope Water which had
been entrained by a warm core ring. Urophycis
tenuis spawm on the Scotian Shelf and upper con-
tinental slope. Wroblewski and Cheney concluded
that the ring altered the usual larval drift pattern
along the shelf edge. Curiously, no larvae of cod or
haddock, which also spawn on the shelf during spring
and summer, were found in the ichthyoplankton net
tows. It remains to be demonstrated whether suffi-
cient numbers of shelf-spawned larvae are trans-
ported offshore by rings to affect recruitment of
shelf stocks.
The advective losses predicted by our model may
be overestimates if only larvae present near the shelf
edge are susceptible to entrainment and if their den-
sity is much lower than that further inshore. The
influence of the ring may not reach the shallower
regions where many larvae are found. Also, biologi-
cal losses may be larger than assumed in the model,
so that the relative importance of ring-induced losses
may be less.
Warm core ring entrainments are not the sole
mechanism by which fish larvae can be transported
off the shelf. In 1955, Chase found a relationship be-
tween haddock recruitment and the strength of the
wind-driven current normal to the southern side of
Georges Bank. We also recognize that there could
even be beneficial effects to the Georges Bank eco-
system if the ring-induced cross-shelf flows push
nutrient-rich Slope Water onto the Bank and fertilize
the system (G. A. Riley^). Rather than exploring all
mechanisms, we have chosen to assess one particular
source of variability which may contribute to fluctua-
tions in year-class strength for the fish stocks spawn-
ing on Georges Bank.
We have also assumed that the fish larvae are well
mixed across the shelf, although we know that they
are generally distributed in patches. Thus our model
solutions may be comparable with field data only if
one integrates the field data over x and z as we have
done in our simplified model. Fisheries recruitment
data naturally reflects this integration over large
spatial scales and we are encouraged by the apparent
relationships in Table 2. However, loss during the
larval period is only one factor affecting recruitment.
Events during the postlarval stages are also signifi-
cant; Sissenwine et al. (1983) showed that predation
in these later stages is an important factor in year
class success.
Our model has given quantitative but crude esti-
mates of the importance of ring events for larval sur-
vival and suggested that the impact of the ring
depends strongly upon its motion; investigations
with more highly resolved and more complex models
and further survey work for assessing both ring and
mesoscale eddy influences on larval fish distributions
and subsequent recruitment are the next steps.
ACKNOWLEDGMENTS
This research was supported by U.S. National
Science Foundation grant number OCE-8019260
to G. R. Flierl and J. S. Wroblewski and by Na-
tional Sciences and Engineering Research Council of
Canada grant number A 0593 to J. S. Wroblew-
ski.
LITERATURE CITED
BiSAGNI, J. J.
1976. Passage of anticyclonic Gulf Stream eddies through
deepwater dumpsite 106 during 1974 and 1975. NOAA
Dumpsite Eval. Rep. 76-1, 39 p.
BoLZ, G. R., AND R. G. Lough.
1981. Ichthyoplankton abundance, diversity and spatial pat-
tern in the Georges Bank - Nantucket Shoals area, autumn
and winter season 1971-1977. NAFO SCR Doc. 81/IX/136,
23 p.
CELONE, p. J., AND J. L. Chamberlin.
1980. Anticyclonic warm-core Gulf Stream eddies off the
northeastern United States in 1978. Ann. Biol. (Copenh.)
35:50-55.
^G. Laurence, Northwest Fisheries Center Narragansett Labora-
tory, National Marine Fisheries Service, NOAA, R.R. 7 A, Box
522 A, Narragansett, RI 02882, pers. commun. June 1983.
^G. Riley, Department of Oceanography, Dalhousie University,
Halifax, Nova Scotia, Canada B3H 4J1, pers. commun. January
1983.
329
FISHERY BULLETIN: VOL. 88. NO. 3
Chamberlin. J. L.
1981. Application of satellite infrared data to analysis of
o<'ean frontal movements and water mass interactions off the
northeast coast. NAFO SCR D(X:. 81/IX/123. 15 p.
Chase. J.
1955. Winds and temperatures in relation to the brood-
strength of Georges Bank hadd(x;k. J. Cons. Perm. Int.
Explor. Mer 21:17-24.
Clark, S. H., W. J. Overholtz, and K. C. Hennemith.
1982. Review and assessment of the Georges Bank and Gulf of
Maine haddock fisherv'. J. Northwest Atl. Fish. Sci. 3:1-27.
CoLTON, J. B., Jr., and R. F. Temple.
1961. The enigma of Georges Bank spawning. Limnol.
Oceanogr. 6:280-291.
Fitzgerald, J. L., and J. L. Chamberlin.
1981. Anticyclonic warm-core Gulf Stream eddies off the
northeastern I'nited States in 1979. Ann. Biol. (Copenh.)
36:44-51.
Halliwell, G. R.. Jr.. and C. N. K. Mooers.
1979. The space-time structure and variability of the shelf
water-slope water and (iulf Stream surface temperature
fronts and associated warm-core eddies. J. Geophys. Res.
84:7707-7725.
Laurence, G. C, and C. A. Rogers.
1976. Effects of temperature and salinity on comparative
embrj'o development and mortality of Atlantic cod (Gadtis
morhuu L.) and haddock {MelatiDgrnmniua aeglefinuK (L.)).
J. Cons. Perm. Int. Explor. Mer 36:220-228.
.MiZENKO, D., AND J. L. CHAMBERLIN.
1979a. Anticyclonic Gulf Stream eddies off the northeastern
United States during 1976. In J. R. Goulet, Jr. and E. D.
Haynes (editors). Ocean variability in the U.S. Fishery Con-
servation Zone. 1976, p. 259-280. U.S. Dep. Commer..
NOAA Tech. Rep. NMFS Circ. 427.
1979b. Gulf Stream anticyclonic eddies (warm core rings) off
the northeastern United States in 1977. Ann. Biol.
(Copenh.) 34:39-44.
Morgan, C. W.. and J. M. Bishop.
1977. An example of Gulf Stream eddy-induced water ex-
change in the Mid-Atlantic Bight. J. Phys. Oceanogr. 7:472-
479.
Parrish. R. H.. C. S. Nelson, and A. Bakun.
1981. Transport mechanisms and the reproductive success of
fishes in the California Current. Biol. Oceanogr. 1:175-203.
Peterson, I., and J. S. Wroblewski.
In press. Mortality' rate of fishes in the Pelagic ecosystem.
Can. J. Fish. Aquatic Sci.
ROACHE, P. J.
1972. Computational fluid dynamics. Hermosa Publishers,
Albuquerque, N.M., 434 p.
Serchuk, F. M., and P. W. Wood, Jr.
1981. Assessment and status of the Georges Bank and Gulf
of Maine Atlantic cod stocks - 1981. Woods Hole Lab. Ref
Doc. No. 81-06, 67 p. Natl. Mar. Fish. Serv., Woods Hole.
Mass.
Sissenwine, M. p., E. B. Cohen, and M. D. Grosslein.
In press. Structure of the Georges Bank ecosystem. Rapp.
P. -v. Reun. Cons. Perm. int. Explor. Mer.
Smith, P. C.
1978. Low-frequency tluxes of momentum, heat, salt, and
nutrients at the edge of the Scotian Shelf. J. Geophys. Res.
83:4079-4096.
Smith, P. C, and B. D. Petrie.
1982. Low-frequency circulation at the edge of the Scotian
Shelf. J. Phys. Oceanogr. 12:28-46.
Smith, W. G., M. Pennington, P. Berrien, J. Sibi'nka. M.
Konieczna, M. Baranowski, and E. Mellek.
1979. Annual changes in the distribution and abundance of
Atlantic cod and haddock larvae off the Northeastern United
States between 1973-74 and 1977-78. LC.E.S. CM. 1979/
G:47, 19 p.
Wroblewski, J. S., and J. Cheney.
1984. Ichthyoplankton associated with a warm core ring off
the Scotian Shelf Can. J. Fish. Aquatic Sci. 41:294-303.
330
FIELD AND LABORATORY ASSESSMENT OF PATTERNS IN
FECUNDITY OF A MULTIPLE SPAWNING FISH: THE
ATLANTIC SILVERSIDE MENIDIA MENIDIA'
David 0. Conover^
ABSTRACT
Patterns in fecunditj' (i.e., spawning frequency, batch fecunditj', annual egg production) of a multiple
spawning fish, the Atlantic silverside, Menidia menidia, were assessed by 1) gonadal analysis of field
specimens, 2) visual observations of spawning periodicity in the field, and 3) laboratory experiments. The
gonadal analysis assumed that the difference between total number of eggs (recruitment + mature) per
female just prior to the beginning of spawning, and recruitment egg retention per female at the end of the
spawning season, represented annual egg production. Annual egg production estimated in this manner was
893 ±197 eggs/g ovary- free body weight (±95% C.L.). Batch fecundity (no. eggs in the most advanced size
class/g ovar\'-free body weight, ±95% C.L.) varied significantly during the breeding season, being lowest
near the beginning (179 ± 21) and end (181 ± 28), and highest during the middle (266 ± 34 and 267 ± 23) of
the breeding season. Batch fecunditj' averaged over the entire breeding season, was about 225 eggs/g
ovary-free body weight, indicating that each female must spawn about four times. The gonadal estimate was
tested by inferring the actual spawning frequency from daily, visual observations of spawning in the field.
These observations showed that spawning occurred on a fortnightly cycle coincidental with new and full
moons, and that each female spawned at most once per semilunar period. There were about four semilunar
spawning phases during the breeding season, indicating close correspondence with the results of gonadal
analysis.
Laboratory observations demonstrated that female Af. menidia are physiologically capable of spawning
more frequently than in nature. Total egg output in the laboratory was about twice that in the field.
Accurate estimates of fecundity are important in
describing the dynamics of fish populations. In some
fishes, all eggs mature synchronously and are shed in
a single batch over a relatively brief period of time
each year (Bagenal 1967). Estimating fecundity in
such species is a simple process of enumerating the
number of ripening eggs per female. However, in
many other fishes, ova mature in multiple batches
that are spawned successively within one spawning
season. These species have been termed multiple
spawners, batch spawners, serial spawners, or frac-
tional spawners by various authors (Bagenal and
Braum 1971; Hempel 1979; DeMartini and Fountain
1981; Gale 1983; Snyder 1983). Little is known
about the patterns in fecundity of multiple spawners,
even though many marine and freshwater fishes
from diverse taxonomic groups in both temperate
and tropical regions produce eggs in this manner.
Determination of annual egg production in multiple
spawners is difficult and recent studies have in-
Contribution No. 89 of the Massachusetts Cooperative Fishery
Research Unit, University of Massachusetts, Amherst, MA, and
Contribution No. 437 of the Marine Sciences Research Center,
State Universitj' of New York, Stony Brook, NY.
^Marine Sciences Research Center, State University of New
York, Stony Brook, Long Island, NY 1 1794.
dicated that in some species, previous assessments
may be in error by as much as an order of magnitude
(Hunter and Goldberg 1980; Hunter and Leong
1981; DeMartini and Fountain 1981).
Frequency distributions of egg size (diameter)
within ovaries of multiple spawning fishes are
characteristically multimodal (Hempel 1979). In
most multiple spawners, a synchronously maturing
batch of eggs that is accumulating yolk sequentially
arises from a much larger group of previtellogenic
immature eggs, termed "recruitment" ova (Clark
1925; Bagenal and Braum 1971; Jones 1978; Hunter
and Leong 1981). The problem in estimating fecun-
dity has been to determine how many modes or
batches of eggs are spawned annually. The conven-
tional approach has been to count only the largest
eggs or those above an arbitrary size (e.g., all yolked
eggs) under the assumption that smaller eggs would
be resorbed or spawned in later years. Whenever
this assumption is incorrect, fecundity can be grossly
underestimated. A second approach has been to infer
the spawning frequency of adults from the propor-
tion of field-collected females in ready- to- spawn con-
dition (i.e., those containing hydrated eggs, e.g.,
Demartini and Fountain 1981) or from females
showing evidence of having just spawned (i.e..
Manuscript accepted October 1984.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
331
FISHERY BULLETIN: VOL. 83, NO. 3
presence of 1-d-old postovulatory follicles, observed
histologically, Hunter and Goldberg 1980). Spawn-
ing frequency is then multiplied by batch fecundity
(number of eggs in the largest size class) to arrive at
annual fecundity. Excellent examples of this method-
ology can be found in DeMartini and Fountain
(1981), Hunter and Goldberg (1980), and Hunter and
Macewicz (1980). A third technique for estimating
fecundity in multiple spawners has been laboratory
experiments where females are confined and allowed
to spawn repeatedly (Gale and Gale 1977; Gale and
Buynack 1978, 1982; Hislop et al. 1978; Gale 1983).
The problem here is that spawning frequency and
fecundity are dependent on the food supply (Wootton
1973, 1977, 1979; Townshend and Wootton 1984), so
that it may be difficult to interpret laboratory data
unless detailed studies of feeding rate and/or fecun-
dity of fish in nature have been previously conducted
(e.g.. Hunter and Leong 1981).
The ovarian cycle of many fishes that breed during
a restricted season involves two major, alternating
phases of oocyte production and growth: 1) a pre-
vitellogenic phase during which new oocytes are pro-
duced, cell organelles form, and cytoplasmic growth
occurs; and 2) a vitellogenic phase during which
growth is faster and yolk accumulates in the ovum
(Ball 1960; Jones 1978; Tokarz 1978; Baggerman
1980). The greatest production of new oocytes and
phase one growth occurs during the postspawning
season, with vitellogenic growth and maturation of
eggs occurring just prior to and during the spawning
season (this may not be true in tropical or other
fishes that breed throughout most of the year, see
reviews by Ball 1960; Jones 1978; Baggerman 1980).
Hence, in multiple spawners having a restricted
breeding season, the reservoir of recruitment eggs
may be largely formed prior to the breeding season.
If true, then the number of recruitment eggs per
female should consistently decline as the breeding
season progresses. The rate of decline in number of
eggs per female would provide an estimate of
seasonal egg production, and spawning frequency
per female could be estimated from the total number
of eggs shed divided by batch fecundity. The method
could be tested by comparing the estimated spawn-
ing frequency with the actual spawning frequency
determined independently in some other manner.
The purpose of this paper is to describe patterns of
batch fecundity and annual egg production in the
Atlantic silverside, Menidia menidia. The analysis
employs the method described above: I show how the
total number of eggs per female (recruitment -i-
maturing) present at the beginning of the spawning
season minus recruitment eggs per female retained
at the end of breeding can be used as an estimate of
total egg production. The method is tested by show-
ing that predicted spawning frequency is identical to
the spawning frequency inferred from direct visual
observations of spawning periodicity in a field popu-
lation. Observations of spawning frequency and egg
production under laboratory conditions are used to
demonstrate that individual females are physiolo-
gically capable of maintaining the egg production
rates and spawning frequency estimated from field
populations.
The Atlantic silverside, Menidia menidia, (Pisces:
Atherinidae) is a multiple spawning marine fish that
inhabits coastal waters of eastern North America
(Middaugh 1981; Conover and Kynard 1984).
Menidia menidia is an annual fish: all individuals
mature at age 1 and < 1% of breeding populations
are 2 yr old. The ecological importance of M. ynenidia
in terms of biomass transport from salt marsh to off-
shore communities and as forage for piscivorous
fishes has been previously documented (Bayliff 1950;
Conover and Ross 1982; Conover and Murawski
1982). The Atlantic silverside is an excellent species
for studying patterns in fecundity because it is
numerous and can be easily collected, spawning is
easy to visually observe in the field, and it readily
breeds in the laboratory.
METHODS
Gonadal Analysis
Field Sampling
Fish were sampled from the salt marsh region of
Essex Bay, MA, with beach seines. Specimens were
collected every 2 wk during 1977 as part of a general
study of the population ecology of M. Tnenidia. Addi-
tional specimens were collected intermittently in the
spring during the breeding season. All collections
were made in daylight within 1-2 h of low tide, and
all specimens were immediately preserved in 10%
buffered Formalin^. Detailed descriptions of Essex
Bay and sampling methodology are available in Con-
over and Ross (1982).
Fecundity
Gonads were excised and weighed (nearest 0.01 g)
from fish captured on 1 1 dates from October 1976 to
July 1977. All fish were measured for total length
'Reference to trade names does not imply endorsement by the Na-
tional Marine Fisheries Service, NOAA.
332
(H)N()VKR: I'ATrFRNS IN FFCrNDITY ( iK All.AN'I'K ' SILVKKSIDK
(nearest millimeter) and gonad-free body weight
(nearest 0.1 g). The gonadosomatic index (GSI) was
calculated by expressing gonad weight as a percent-
age of total weight (Snyder 1983).
Preliminary microscopic examination of ripe
ovaries from collections during the breeding season
revealed three general egg types that corresponded
with modes found in frequency distributions of egg
diameters from ripe females (see Figure 1 below).
The three egg classifications were defined by both
size and appearance of the ova as follows:
Immature ova: spherical, 0.05-0.60 mm in diameter.
The smaller ova in this group (0.05-0.15 mm) were
primary oocytes with a clear cytoplasm and large
nucleus. The larger ova (0.15-0.60 mm) were opa-
que and white. These ova formed one continuous
mode in the frequency distribution so they were
considered as one group (Fig. lA, B).
Maturing ova: spherical, 0.6-1.0 mm in diameter,
yellowish, and translucent.
Ripe ova: spherical, hydrated, 1.0-1.2 mm in dia-
meter, hyaline and golden, with visible gelatinous
threads coiled around the egg.
To confirm that these classifications represented
distinct groups of synchronously maturing ova, I
measured the diameter (random axis) of about 150
eggs, randomly subsampled from each of several
females. In females captured during the breeding
season, there were two distinct modes: the most ad-
vanced mode represented maturing eggs, and the
other mode represented immature eggs (Fig. 1 A). In
females with ripe eggs, three modes in egg fre-
quency were apparent: the most advanced group
represented ripe eggs, the intermediate mode
represented the next batch of maturing eggs, and
the remaining mode consisted of immature eggs
(Fig. IB).
"Batch fecundity" was defined as the number of
mature eggs in the most advanced size class, and
presumably represented the number of eggs spawn-
ed at one time. As illustrated in Figure 1, the most
advanced size class of maturing or ripe eggs was
clearly distinguishable from, and did not overlap in
size with, the immature ova. In ripe females, batch
fecundity represented the number of hydrated eggs
(e.g., the most advanced mode in Figure IB). In
nonripe females, batch fecundity represented the
number of maturing eggs (e.g., the most advanced
mode in Figure lA). "Recruitment fecundity" was
defined as the number of eggs smaller than the most
advanced egg batch. Recruitment fecundity presum-
ably represented the number of ova from which addi-
Immature
Maturing
n=l45
.3 .5 .7 .9 1.1
EGG DIAMETER(mm)
Figure 1.- Frequency vs. egg size (diameter in 0.1 mm interN-als)
for ova randomly sampled from two female Menidia menidia col-
lected 6 June in Essex Bay, MA. A) A nonripe female in which
there is a large number of immature eggs and a clearly definable
mode of maturing eggs. B) A ripe female in which there is a large
mode representing immature eggs, an intermediate mode of eggs
beginning to mature, and an advanced mode of ripe eggs.
tional batches of mature eggs could potentially arise.
In ripe fish containing three modes (e.g.. Fig. IB),
the intermediate mode of eggs in early maturation
was included with the immature eggs as part of the
recruitment egg group because these overlapped in
size with, and were difficult to separate from, im-
mature ova. The minimum size of recruitment eggs
was 0.05 mm in diameter. "Total fecundity" was de-
fined as the sum of recruitment and batch fecun-
dity.
Batch, recruitment, and total fecundity of indivi-
dual females were estimated gravimetrically in the
following manner. A cross section comprising
10-20% of the total ovarian weight was cut from a
randomly chosen portion of one ovary. Both the sub-
333
FISHERY BULLETIN: VOL. 83. NO. 3
sample and the remaining ovarian material were
blotted on absorbent paper and weighed to the
nearest milligram. The subsample was then placed in
modified Gilson's fluid (Bagenal and Braum 1971),
teased apart and vigorously shaken to separate ova,
and stored for several weeks. All eggs in a subsample
were counted and classified as belonging to either
the recruitment pool or the mature batch of eggs.
Batch and recruitment fecundities were then esti-
mated for each female by multiplying the number of
eggs in the subsample by an expansion factor (total
ovarian weight/subsample weight). The mean
diameter of the largest size class of eggs was also
determined by measuring a random sample of about
20 mature eggs from each female. Shrinkage of eggs
during preservation appeared to be minimal, so no
correction for shrinkage was made. Fecundity was
estimated for females collected on four occasions,
from just before the beginning of the spawning
season to its end. These dates were 6 May, 6 June, 22
June, and a pooled sample captured over the period
6-13 July.
To demonstrate whether estimates of fecundity
were dependent on the location of the ovarian sub-
sample, I compared these among replicate subsam-
ples taken from the anterior and posterior sections of
the right and left ovaries of six different females (i.e.,
four subsamples per female). Two-way ANOVA in-
dicated that estimated fecundity was independent of
subsample location (F > 0.10) and the coefficient of
variation was low (CV = 4.2%). The ratio of the
number of batch eggs to recruitment eggs was also
independent of subsample location (P > 0.5). More-
over, I also directly counted the total number of
batch eggs in four of the females used in the above
analysis; in each case estimated batch fecundity was
within 10% of the true value.
Field Observations of
Spawning Frequency
The frequency of spawning in a natural population
of Menidia menidia was inferred from daily, direct
field observations of mating. The Atlantic silverside
spawns in large groups of fish that broadcast milt
and eggs amongst vegetation in the upper intertidal
zone of salt marshes within 1 or 2 h of the daylight
high tide (Middaugh 1981; Middaugh et al. 1981;
Conover and Kynard 1984). At such times, spawning
can be easily observed. My observations were con-
ducted at a major spawning site in Salem Harbor,
MA. Daily assessments of spawning intensity were
conducted throughout the spawning season by count-
ing the number of aggregations of spawning fish
sighted during high tide. Methodological details are
provided in Conover and Kynard (1984).
Laboratory Observations of
Spawning Frequency and Egg Production
Spawning frequency and egg production were also
assessed by confining fish in laboratory tanks. A
summary of the experimental procedure, described
fully in Conover and Kynard (1984), follows. A large
group of M. menidia were captured at Salem Harbor
on 5 May 1979 and transported to the University of
Massachusetts marine laboratory at Gloucester, MA.
One female and two male fish were placed into each
of the four 74 L tanks at room temperature on a
natural photoperiod. Four males and four females
were also placed into each of two circular plastic
pools (diameter 1.5 m, depth 0.3 m). These pools
were located outdoors. All fish were fed fresh, chop-
ped seaworms (Nereis) and amphipods in excess of
daily consumption. Spawning substrates consisted of
a small tuft of synthetic aquarium filter floss, an-
chored to the bottom of each tank or pool. The floss
was checked several times daily for the presence of
eggs. When eggs were discovered, the floss was
replaced. All eggs were preserved and enumerated
later. Eggs from each female were usually deposited
in a distinct clump on the floss, providing a means for
determining the number of females that had spawn-
ed in the previous interval. The experiment was
allowed to continue until spawning ceased (27 July).
Length and weight of spawners was measured at the
conclusion of testing.
RESULTS AND DISCUSSION
Gonadal Analyses
In late fall, just prior to the offshore winter migra-
tion (Conover and Murawski 1982), ovaries repre-
sented about 1% of total body weight (Fig. 2) and
contained only small (< 0.1 mm), clear, transparent
eggs. Upon return of fish to the shore zone the
following April, the ovarian GSI was about 4% and
many opaque, white, immature ova (< 0.5 mm) were
present. Of the 25 females captured on 6 May, 92%
contained numerous immature ova and a clearly
definable batch of maturing ova. The first female
carrying ripe egges was collected on 12 May. The
GSI peaked in both sexes on 25 May and declined
thereafter until the end of July. The first fish in spent
condition (no maturing egg class, recruitment eggs,
if present, degenerating, GSI < 5%) was captured on
22 June. The proportion of spent fish was 23% on
334
CdXinKK: I'ATTKKXSIX KKCI Nni'I'V ( >K ATI.ANTH ' SIIAKKSIDK
O
<
z
o
28-
13
A. FEMALE
24-
43 32
20-
14
25
-
16
16-
12-
8-
1
10
>
-
-
-
i
4-
10 1
r 4< . —
1 -
8
1 =t^
28-
24-
20-
16
12
8-
4-
27
18
10
+
>. " I -f
B. MALE
18 8
12
^ >* I 111 I I I I >
17 16 29 A 12 25 6 22 6 13 26
OCT APR MAY JUN
1976 1977
JUL
Figure 2.-Gonadosomatic index (gonad weight expressed as a
percentage of total weight) for Menidia menidia collected during
1976-77 in Essex Bay, MA. The horizontal lines represent means,
the vertical lines represent one standard deviation, and the sample
size is given above the datum for each collection.
6-13 July and 100% on 26 July. Hence, the breeding
season in Essex Bay began sometime after 6 May
and was over by 26 July during 1977.
The potential annual fecundity of M. menidia may
be represented by the total number of eggs (recruit-
ment + maturing ova) within females just prior to
the breeding season (i.e., 6 May), if additional im-
mature eggs are not continually added to the recruit-
ment pool as the spawning season progresses. If this
premise is true, then there should be a continuous
decline in recruitment fecundity and total fecundity
during the breeding season (although not necessarily
in batch fecundity).
Comparison of fecundities between sample dates
was facilitated by the following observations. Total
number of eggs per female was linearly related to
ovary-free body weight (Fig. 3). Batch fecundity was
also a simple linear function of ovary-free body
weight (Fig. 4) and the rates of increase in batch
fecundity, recruitment fecundity, and total fecundity
with increase in female weight were generally
similar among sample dates (i.e., regression slopes
O
CO
o
o
UJ
q:
LiJ
CD
14
12
10
8
6
4
MAY 6
• •
Y = III3.4(X)-H25I9.5
n = 23 r = .78
<
o
tv^
3456789 10
OVARY- FREE FEMALE WEIGHT(g)
Figure 3. -Relation between total number of eggs (recruitment
plus mature) and ovary-free female body weight for Atlantic silver-
sides captured just prior to the beginning of the spawning season (ti
May 1977) in Essex Bay, MA.
differed little, t-test, P > 0.05). Correspondingly,
relative batch fecundity, relative recruitment fecun-
dity, and relative total fecundity (relative fecundity
= no. eggs/g ovary-free body weight) were each in-
dependent of body weight in nearly all tests (linear
correlation, P > 0.05), suggesting that females of all
sizes allocated about the same proportion of energy
to reproduction. Hence, fecundity was adequately
described and compared between dates if expressed
as a proportion of ovary-free body weight, rather
than as a function of weight.
Batch fecundity, recruitment fecundity, and total
fecundity (no. eggs/g ovary- free body weight) during
the spawning season are presented in Figure 5.
Three patterns are evident. First, total fecundity and
recruitment fecundity monotonically declined (Fig.
5 A, B). Total fecundity was 1,609 ± 126 (95% C.L.)
on 6 May and declined to 876 ± 177 by the second
week of July (Fig. 5A) while recruitment fecundity
was initially 1,430 ± 128 on 6 May and declined to
716 ± 164 in July (Fig. 5B). Second, batch fecundity
differed significantly between sample dates, being
maximal during the middle of the breeding season
(266 ± 34 and 267 ± 23 on 6 and 22 June, respective-
ly) and minimal at the beginning and end of the
breeding season (179 ± 21 and 181 ± 28 on 6 May
and 6-13 July, respectively; Fig. 5C). Third, many
recruitment eggs remained in ovaries near the end of
the spawning season (Fig. 5B) and most of these
were probably resorbed soon thereafter because all
females captured on 26 July contained only small (<
0.10 mm), transparent oocytes. Two females from
the 6-13 July collection contained only immature
eggs that appeared to be in a state of resorption and
had no maturing egg group.
335
FISHF:RV BILLETIN: VOL. Ki. NO. .S
, Y = 244 40{X)-33I.57
n-23 r = .83
iiJ
E
3
Q
Z)
o
UJ
o
<
CD
2000 r
^ 1000
y^» • Y = 329.44(X)-3I4.36
n = 23 r=.83
i_/^M I 1 1 1 1 1 1-
3000
_ JUNE 22
•
2000
•
• "^^
• -'^
^»
1000
^y^ •
•
^ Y
= 238 37(X) + I57 46
-U 1 1
n = 29 r = .65
1 1 1 1 1
2000
1000
JULY 6-13
i/-
Y = l44.42{X) + 249.65
n=l4 r = .6l
I I I I I
3456789 10
OVARY- FREE FEMALE WEIGHT(g)
FiGi'RE 4. -Relation between batch fecunditv' (no. of eggs in the
most advanced size class) and ovary-free female body weight for
Atlantic silversides captured on four occasions during the 1977
breeding season in Essex Bay, MA.
UJ x:
"2 jQ
< 3
I-
o
o
UJ
000
500
0
^ 1500
1000
5 5
q: _
q: ct 500
UJ ^
0
CO
o
o
_
300
UJ
£L
liJ
cn
q:
<i>
1)
^
<
>>
200
5
X)
o
a:
J3
g IS" 100
D
" E3 i
B
k23) (23) (29) (17)
1 1
MAY
JUNE
JULY
Batch fecundity as estimated above assumes that
the number of eggs in the most advanced mode is not
reduced by atresia as they grow and are eventually
shed. I noted few eggs which appeared to be atretic
or in a process of resorption (except near the very
end of the breeding season) and females which had
recently spawned usually contained few. if any,
residual ripe eggs. Similar observations were
reported by Clark (1925) for the atherinid Leuresthes
t£nuis. Moreover, if some eggs cease growing and
are resorbed before reaching maturity, there should
Figure 5. -Relative fecundity (no. eggs/g ovary-free female body
weight) for Atlantic silversides captured on four (x-casions during
the 1977 breeding season in Essex Bay. MA. The horizontal lines
represent means, the vertical lines represent one standard devia-
tion, and the rectangles represent 95% C.L. Sample sizes are in
parentheses. All fish were spent on 26 July. A) ToUil number of
eggs. B) Number of recruitment eggs (recruitment fecundity)- C)
Number of mature eggs (batch fecundity).
be a negative correlation between batch size and the
mean diameter of eggs in the batch (i.e., no. batch
eggs/g ovary-free body weight should generally be
336
CONOVER: PATTERNS IN FECUNDITY OF ATLANTIC SILVERSIDE
lower in fish nearly ready to spawn than in fish
where batch eggs are still maturing). Linear correla-
tions of batch size and mean diameter of the
maturing egg batch for each of the four dates on
which fecundity was measured were nonsignificant
(P > 0.05), suggesting that the number of eggs in a
batch does not decline much as the oocytes grow to
maturity.
Assuming that the recruitment pool of immature
eggs is fully formed prior to the breeding season, an
estimate of the actual number of eggs produced an-
nually can be derived from the above data. Because
recruitment eggs remain at the season's end, actual
egg production is best represented by the total
number of eggs present just prior to the beginning of
the spawning season minus the number of recruit-
ment eggs retained when the spawning season ends.
For the above data, this provides a value of (1,609 ±
126) - (716 ± 164) = 893 ± 197 eggs/g ovary-free
body weight (±95% C.L.). The mean body weight of
females during the breeding season was 5.6 g so that
the average female would have spawned about 5,001
eggs in a season. The mean batch fecundity over the
spawning season was 223 eggs/g ovary-free body
weight or about 1,249 eggs/ female. Hence, if the ini-
tial assumption is correct, the average female must
spawn about four times during the breeding season.
phic variation in M. menidia also support this conten-
tion (Johnson 1975).
Daily observations of the number of spawning ag-
gregations sighted during high tide at Salem Harbor
in 1979 showed that populations of Atlantic silver-
sides breed on a semilunar periodicity coinciding
with new and full moons (see figure 2 in Conover and
Kynard 1984). Middaugh (1981) has reported similar
observations based on a 3-yr study of populations in
South Carolina. Within each semilunar spawning
period of 1979 in Salem Harbor, the majority of
spawning (40-90%) occurred on a single day, sug-
gesting that females spawn, at most, once per semi-
lunar cycle. This conclusion is further supported by
the observation that sex ratios in spawning aggrega-
tions were highly male biased, whereas during non-
spawning intervals, the sex ratio was near unity
(Conover 1984). The sex ratio data is explained if
females spawn, at most, once per cycle, while males
spawn each day of a spawning period.
During 1979 in Salem Harbor, there were five
semilunar spawning periods, although the first in
late April was very light. In Essex Bay during 1977,
there were four semilunar phases during the period
defined as the breeding season. Hence, estimated
spawning frequency based on gonadal analysis and
direct observations of spawning fish agreed closely.
Frequency of Spawning in Nature
To test the prediction of spawning frequency
derived above, spawning periodicity was determined
from direct, visual observation of breeding events in
the field. In 1978, 1 discovered a large spawning site
in Salem Harbor, MA, where numerous eggs of M.
menidia were deposited amongst mats of filamen-
tous algae in the upper intertidal zone. Salem Harbor
is located 20 km southwest of Essex Bay; however,
individuals in each area are likely members of the
same population because extensive mixing occurs
during the offshore winter migration (Conover and
Murawski 1982). Electrophoretic studies of geogra-
Spawning Frequency and Egg Production
in the Laboratory
Females held in laboratory tanks, whether housed
individually indoors or outdoors in groups where
natural day and night illumination was present, did
not maintain a fortnightly spawning periodicity. In-
stead, spawning occurred much more frequently: the
interval between spawnings averaged about 4
d/female (Table 1; see also figure 4 in Conover and
Kynard 1984). Batch fecundity averaged 99-187
eggs/g ovary-free body weight among different
tanks. Total egg production averaged 1,425-3,375
eggs/g ovary-free body weight. Hence, the experi-
Table 1. — Egg production by Menidia menidia on unlimited food rations in the laboratory. Field data are
also provided for connparison.
Mean 9
Days from
No. of
Days
No. eggs/g
Total
Total eggs/g
body
1st to
egg
between
9 body
eggs
9 body
No. of
weight
last
batches
spawn
weight per
per 9
weight
females
(g)
spawning
per 9
per 9
egg batch
(no.)
(no.)
Pool 1
4
6.32
63
15.25
3.9
99.0
9,551
1,511
Pool 2
4
5.82
51
11.75
3.7
121.2
8,299
1,426
9 A
1
3.9
72
20.0
3.6
169.5
13,218
3,389
9C
1
3.6
'28
'7.0
4.0
187.0
'4,710
'1,308
Field
—
—
60-75
4.0
14-15
180-266
5,000
893 ±197
'Low values reflect the fact that 9 C died before the conclusion of the experiment.
337
FlSHKKVBrLLF.TI\;V()l., h:1N().3
mental fish responded to laboratory conditions by
reducing batch fecundity somewhat, but spawning
more frequently, and thereby producing about twice
the number of eggs as in nature (Table 1). The daily
rate of egg production was 24-47 eggs/g female body
weight per d in the laboratory, but averaged about
14 eggs/g female body weight per d in the field.
At the termination of the experiment, four of the
eight females in the outdoor pools were spent, three
contained only recruitment eggs, and one had both
recruitment and maturing eggs. Female A died of
unknown causes after its last spawning on 22 July.
Female C also died (9 June) before cessation of
spawning by jumping out of the tank.
The total weight specific egg production for the
experimental fish was generally within the range of
total eggs available prior to the beginning of the
breeding season. The one exception was female A
which produced about twice the total number of eggs
that a fish of its size should have had available at the
beginning of the spawning season (see Figure 3).
Hence, under certain laboratory conditions, females
may be capable of producing new oocytes from
oogonia during the breeding season, as recruitment
eggs become depleted. These laboratory observa-
tions show that the reproductive patterns of egg
maturation and spawning which are highly synchro-
nized with and influenced by environmental factors
in the field, easily become disrupted when individuals
are removed from their natural habitat.
CONCLUSIONS
This study indicates that annual fecundity in
Menidia menidia, and perhaps certain other fishes,
can be estimated from the difference between total
number of eggs (recruitment plus maturing) prior to
the breeding season and recruitment egg retention
near the end of the breeding season. Dividing the
estimated total number of eggs shed per female by
mean batch fecundity provided an estimate of
spawning frequency. The accuracy of this value for
spawning frequency was tested and found to agree
closely with the spawning fre(]uency inferred from
direct field observations of breeding fish. Previous
estimates of the fecundity of M menidia were about
3-10 times less than that rejwrted here because
spawning frequency was not determined (Bayliff
1950; Jessop 1983). The studies of Hunter and his
coworkers on northern anchovy, Engraulis mordax
(Hunter and Goldberg 1980; Hunter and Macewicz
1980; Hunter and Leong 1981), and DeMartini and
Fountain (1981) on queenfish, Seriphus politus, have
amply demonstrated that estimates of annual fecun-
dity can be in error by over an order of magnitude
when multiple spawning is ignored.
The estimation of fecundity from the difference be-
tween total prespawning fecundity and recruitment
egg retention is dependent on the assumption that
new oocytes are not simultaneously produced from
oogonia and added to the reservoir of recruitment
eggs as mature eggs are spawned. Agreement be-
tween predicted and observed spawning frequency
suggests that this may be true in M. menidia. Many
more recruitment eggs were present in ovaries at
the beginning of the spawning season than were ac-
tually spawned in nature. Evidently, the recruitment
egg pool is largely formed before the breeding
season in Menidia, as is believed for some other
seasonal spawners (Tokarz 1978; Jones 1978;
Baggerman 1980). However, the generality of this
pattern in other multiple spawning temperate or
tropical fishes is not clear. Clark (1925) noted that
the relative abundance of mature, intermediate, and
immature eggs in Leuresthes tenuis was relatively
constant during the breeding season and concluded
from this that new oocytes must be continuously pro-
duced to replenish those spawned. Taylor and
DiMichele (1980) reached a similar conclusion based
on the relative abundance of different developmental
stages of oocytes during the semilunar spawning
cycle of Fundulus heteroclitiis. However, analyses
based on relative proportions do not take into ac-
count that gonad weight (GSI) generally declines as
the season progresses (e.g., Fig. 2) and that number
of eggs in the most advanced mode is not necessarily
constant during the breeding season. Comparison of
the relative abundance of egg sizes from sections of
an ovary may not reflect changes in absolute
number. For example, the relative abundance of
recruitment eggs in M. menidia during 1977 was
0.88 on 6 May, 0.78 on 6 June, 0.76 on 22 June, and
0.79 during 6-13 July. Hence, the relative proportion
of recruitment eggs did not consistently decline dur-
ing the breeding season even though the absolute
number of eggs declined by a factor of 2.4. In any
event, too little is known about patterns of oocyte
growth in fishes to recommend that the annual
fecundity of multiple spawners can generally be
determined by monitoring the decline in the standing
stock of ova as was done here. For instance, in
tropical species that breed most of the year recruit-
ment eggs may be produced continuously. Whenever
possible, the results of several different api)roaches
to estimating fecundity should be compared.
The results of the laboratory study demonstrated
that M. menidia is physiologically capable of spawn-
ing much more frequently and over a shorter interval
338
rONO\ KK I'AITKKNS IN KKdNDI TV I )K ATLANTIC SIlAKkSlDK
than normally occurs in the field. The reasons for the
higher spawning frequency an(i cumulative egg pro-
duction for fish in captivity are probably several.
Fecundity may have been increased because ration
size was unlimited. Fecundity is dependent on the
food supply in many species (Wootton 1979). In the
stickleback, Gasterosteus aculeatus, (Wootton 1977)
and the convict cichlid, Cichlasoma nigrofasciatum,
(Townsend and Wootton 1984) experimental studies
have demonstrated that the number of spawnings
was positively related to food ration and the interval
betu'een spawnings was inversely related to ration.
In my experiments on M, nienidia, spawning fre-
quency may also have been increased beyond that in
nature due to the continuous availability of appro-
priate spawning substrates and lack of tidal spawn-
ing cues in the laboratory. Conover and Kynard
(1984) noted that both marine and freshwater
populations of Menidia spp. tend to spawn during
midmorning, and speculated that spawning in nature
may be restricted by the fact that suitable spawning
substrates are covered by high tide during midmorn-
ing only at fortnightly intervals. Correspondingly, a
lacustrine population of M. beryllina spawns daily at
midmorning (Hubbs 1976). Hence, in the laboratory
where tidal cues are removed, spawning substrates
are continuously available, and food is abundant, M.
menidia responded by spawning more frequently.
The high egg production of female A also suggests
that if the supply of recruitment eggs is exhausted,
new recruitment eggs can be formed. It is clear that
estimates of fecundity in natural populations of
multiple spawners based on laboratory studies alone
should be interpreted with caution.
Many aspects of the fecundity and spawning
periodicity of M. menidia are paralleled in a west
coast atherinid, Leuresthes tenuis. The California
grunion has a well-known semilunar spawning cycle
(Walker 1952). Clark (1925) conducted a detailed
study of egg diameter frequencies in ovaries of L.
tenuis and concluded that each female spawns once
about every 15 d. Batch fecundity was very similar
to that reported here for M. menidia. Although
Clark measured batch fecundity in only a few indivi-
duals, a 118 mm grunion contained 1,613 ova. I
calculate that a 118 mm Atlantic silverside would be
expected to have 1,704 ripening eggs during the mid-
dle of the breeding season. Clark also found reten-
tion of recruitment eggs at the end of the breeding
season and presented histological evidence that re-
tained eggs were being resorbed.
Based on my estimate of the average annual fecun-
dity of M. menidia (893 ± 197 eggs/g ovary-free
body weight) and the wet weight of ripe eggs (0.8
g/1,000 eggs), an Atlantic silverside produces nearly
0.7 of its body weight in eggs during the breeding
season in nature. In the laboratory, females pro-
duced 1.1-2.7 times their body weight in eggs.
Studies of other multi[)le spawners have yielded
similar results. DeMartini and Fountain (1981) esti-
mated that the queenfish could spawn about 114% of
its body weight in a year. Experiments on several
species of cyprinids indicate that they are capable of
spawning 0.7 to 6.8 times the volume of the female in
eggs, at least in the laboratory ((lale and Gale 1977;
(iale and Buynak 1978, 1982; Gale 1983). Hubbs
(1976) estimated that a freshwater population of
Menidia beryllina spawned 6-8 times female weight
in eggs, although his assumption that each female
spawns daily throughout the length of the breeding
season needs further documentation.
Subseasonal trends in batch fecundity among
multiple spawners have been examined by few inves-
tigators. If trends in batch fecundity within the
breeding season are the adaptive result of natural
selection, then periods of maximum batch fecundity
should reflect the period when the probability of off-
spring survival is greatest. On the other hand, trends
in batch fecundity could simply result from varying
food conditions for adults. Three general relation-
ships between the batch fecundity and the time of
the breeding season have emerged from field studies
with which I am familiar. These include 1) constant
batch fecundity during the breeding season (Fig. 6,
curve A), 2) a concave downward relation between
batch fecundity and the breeding season (Fig. 6,
curve B), and 3) a constant decline in batch fecundity
during the breeding season (Fig. 6, curve C). Con-
stant fecundity (curve A) might be expected where
the optimal environmental conditions for reproduc-
tion and offspring survival are constant or vary un-
predictably during the breeding season. This pattern
has been found in the queenfish (DeMartini and
Fountain 1981), a pelagic spawner of the western
North American coast where aperiodic upwelling
events produce unpredictable variations in plankton
productivity and potential larval survival (Lasker
1978). When seasonal environmental conditions
change in a predictable manner, there may be an op-
timal period for reproduction that occurs at roughly
the same time each year, and batch fecundity would
be expected to be maximal at that time (curve B). In
M. menidia, the relation between batch fecundity
and the breeding season was concave downward,
suggesting that reproductive success is maximal dur-
ing the middle of the breeding season. There is some
independent evidence to support this hypothesis.
Winter mortality during the offshore migration is
339
FISHERY BULLETIN: VOL. 83, NO. 3
>-
O
2
O
X
u
<
CD
4-
BEGINNING
END
BREEDING SEASON
Figure 6. -Three hypothetical relationships between batch fecun-
dity and time of the breeding season that have empirical support in
the literature. A) Constant batch fecundity. B) Batch fecundity
maximal during the middle of the breeding season. C) Batch fecun-
dity maximal at the beginning of the breeding season and declining
continuously thereafter.
strongly size- selective in M. menidia (Conover and
Ross 1982; Conover 1984): the largest young-of-the-
year have the highest probability of surviving.
Hence, there should be selection pressure to breed as
early in the spring as physical conditions (such as
temperature) permit, and perhaps before conditions
are optimal. Any offspring that managed to survive
early in the breeding season will ultimately benefit
from having a longer growing season. Conversely,
towards the end of the breeding season, energy
placed into reproduction becomes wasted because
these offspring will have almost no chance of grow-
ing to a size that will permit winter survival. It
follows that somewhere in the middle of the breeding
season will be the optimal period for reproduction.
Declining batch fecundity during the breeding
season (curve C) has been reported for a population
of the common mummichog, Funduhis heteroclitus,
where batch fecundity was greatest at the beginning
of the breeding season and became progressively less
thereafter (Kneib and Stiven 1978). A continuous
decline in batch fecundity may evolve when the value
of putting energy into current reproduction, as op-
posed to somatic growth, declines continuously as
the breeding season progresses. Although few data
are now available for comparing the subseasonal pat-
terns of batch fecundity in multiple spawning fishes,
such information may eventually prove useful in
understanding the general reproductive strategies of
fishes.
ACKNOWLEDGMENTS
I thank the staff of the University of Massachu-
setts Marine Station for logistic support. D.
Chevalier assisted in maintaining the laboratory fish
and in counting eggs. F. Sutter helped with field
sampling. The comments of two anonymous
reviewers improved the clarity of the manuscript.
During part of the this study, I received support
from the Massachusetts Cooperative Fishery
Research Unit, which is jointly funded by the
Massachusetts Division of Marine Fisheries, the
Massachusetts Division of Fish and Wildlife, the
University of Massachusetts, and the U.S. Fish and
Wildlife Service.
LITERATURE CITED
Bagenal, T. B.
1967. A short review of fish fecundity. In S. D. Gerking
(editor), The biological basis of freshwater fish production, p.
89-111. Blackwell Sci. Publ., Oxf., Engl.
Bagenal, T. B., and E. Braum.
1971. Eggs and early life history. In W. E. Ricker (editor),
Methods for assessment of fish production in fresh waters, p.
166-198. IBP (Int. Biol. Programme) Handb. 3, 2d ed.;
Blackwell Sci. Publ., Oxf., Engl.
Baggerman, B.
1980. Photoperiodic and endogenous control of the annual
reproductive cycle in teleost fishes. In M. A. Ali (editor).
Environmental physiology of fishes, p. 533-567. Plenum
Press, N.Y.
Ball, J. N.
1960. Reproduction in female bony fishes. Symp. Zool. See.
Lond. 1:105-135.
Bayliff, W. H., Jr
1950. The life history of the silverside Menidia menidia
(Linnaeus). Chesapeake Biol. Lab. Publ. 90, 27 p.
Clark, F. N.
1925. The life history of Leuresthes tenuis, an atherine fish
with tide controlled spawning habits. Calif. Fish Game
Comm., Fish Bull. 10, 51 p.
Conover, D. 0.
1984. Adaptive significance of temperature-dependent sex
determination in a fish. Am. Nat. 123:297-313.
Conover, D. 0., and B. E. Kynard.
1984. Field and laboratory observations of spawning periodi-
city and behavior of a northern population of the Atlantic
silverside, Menidia menidia (Pisces: Atherinidae). Environ.
Biol. Fishes 11:161-171.
Conover, D. 0., and S. A. Murawski.
1982. Offshore winter migration of the Atlantic silverside,
Menidia menidia. Fish. Bull., U.S. 80:145-150.
Conover, D. 0., and M. R. Ross.
1982. Patterns in seasonal abundance, growth and biomass of
the Atlantic silverside, Menidia menidia, in a New England
estuary. B^stuaries 5:275-286.
DeMartini, E. E., and R. K. Fountain.
1981. Ovarian cycling frequency and batch fecundity in the
340
OONOVEK: PATTERNS IN FECUNDITY OK ATLANTIC SILVKRSIDE
queenfish, Seriphits politus: Attributes representative of
serial spawning fishes. Fish. Bull.. I'.S. 79:547-560.
Gale. W. F.
1983. Fecunditj' and spawning frequency of caged bluntnose
minnows- fractional spawners. Trans. Am. Fish. Sex-. 112:
398-402.
Gale, W. F., and G. Buynak.
1978. Spawning frequency and fecundity of satinfin shiner
(Notropis nnalostamis)-a fractional, crevice spawner.
Trans. Am. Fish. Soc. 107:460-463.
1982. Fecundity and spawning frequency of the fathead
minnow -a fractional spawner. Trans. Am. Fish. Soc. Ill:
35-40.
Gale, W. F., and C. A. Gale.
1977. Spawning habits of spotfin shiner {Notntpis spilotenis)
-a fractional, crevice spawner. Trans. Am. Fish. Soc. 106:
170-177.
Hempel, G.
1979. Early life history of marine fish. Univ. Wash. Press,
Seattle, 70 p.
HiSLOP, J. R. G., A. P. ROBB, AND J. A. Gauld.
1978. Observations on effects of feeding level on growth and
reproduction in haddock, Melarwgrammus aeglefinus (L.) in
captivity. J. Fish Biol. 13:85-98.
HUBBS, C.
1976. The diel reproductive pattern and fecundity of Menidm
audens. Copeia 1976:386-388.
Hunter, J. R., and S. R. Goldberg.
1980. Spawning incidence and batch fecundity in northern
anchovy, Engraulis mordax. Fish. Bull., U.S. 77:641-652.
Hunter, J. R., and R. Leong.
1981. The spawning energetics of female northern anchovy,
Engraulis mordax. Fish. Bull., U.S. 79:215-230.
Hunter, J. R., and B. J. Macewicz.
1980. Sexual maturity, batch fecundity, spawning frequency,
and temporal pattern of spawning for the northern anchovy,
Engrmdis mordax. during the 1979 spawning season. Calif.
Coop. Oceanic Fish. Invest. Rep. 21:139-149.
Jessop, B. M.
1983. Aspects of the life historj' of the Atlantic silverside
(Menidia menidia) of the Annapolis River, Nova Scotia.
Can. Manuscr. Rep. Fish. Aquat. Sci. 1694, 41 p.
Johnson, M. S.
1975. Biochemical systematics of the atherinid genus Meni-
dia. Copeia 1975:662-691.
Jones, R. E.
1978. Ovarian cycles in nonmammalian vertebrates. In R. E.
Jones (editor), The vertebrate ovary, p. 731-762. Plenum
Press, N.Y.
Kneib, R. T., and a. E. Stiven.
1978. Growth, reproduction, and feeding oi Fundulus hetero-
clitvs (L.) on a North Carolina salt marsh. J. Exp. Mar. Biol.
Ecol. 31:121-140.
Lasker, R.
1978. The relation between oceanographic conditions and lar-
val anchovy food in the California current: identification of
factors contributing to recruitment failure. Rapp. P. -v.
R6un. Cons. int. Explor. Mer 173:212-230.
MiDDAUGH, D. P.
1981. Reproductive ecology and spawning peritxlicity of the
Atlantic silverside, Memidm menidia (Pisces: Atherinidae).
Copeia 1981:766-776.
MiDDAUGH, D. P., G. I. Scott, and J. M. Dean.
1981. Reproductive behavior of the Atlantic silverside, Menir
dia menidia (Pisces, Atherinidae). Environ. Biol. Fishes 6:
269-276.
Snyder, D. E.
1983. Fish eggs and larvae. In L. A. Nielsen and D. L.
Johnson (editors). Fisheries techniques, p. 165-197. Am.
Fish. Soc, Bethesda, MD.
Taylor, M. H., and L. DiMichele.
1980. Ovarian changes during the lunar spawning cycle of
Fundulus heteroclitus. Copeia 1980:118-125.
TOKARZ, R. R.
1978. Oogonial proliferation, oogenesis, and folliculogenesis in
nonmammalian vertebrates. In R. E. Jones (editor). The
vertebrate ovary, p. 145-179. Plenum Press, N.Y.
TOWNSHEND, T. J., AND R. J. WOOTTON.
1984. Effects of food supply on the reproduction of the convict
cichlid. Cichlasoma nigrofasciatum. J. Fish Biol. 24:91-104.
Walker, B. W.
1952. A guide to the grunion. Calif. Fish Game 38:409-420.
WOOTTON, R. J.
1973. The effect of size of food ration on egg pnxluction in the
female three-spined stickleback, Gasterosteus acuLeatvs L.
J. Fish Biol. 5:89-96.
1977. Effect of food limitation during the breeding season on
the size, body components and egg production of female
sticklebacks {Gasterosteus aeuleatus). J. Anim. Ecol. 46:823-
834.
1979. Energy costs of egg production and environmental
determinants of fecundit>' in teleost fishes. Symp. Zool. Soc.
Lond. 44:133-159.
341
PARASITES OF SKIPJACK TUNA, KATSUWONUS PELAMIS:
FISHERY IMPLICATIONS
R. J. G. Lester,' A. Barnes,^ and G. Habib^
ABSTRACT
The numbers of 26 types of parasites were counted in 878 fish, of which all but 3 were from 1 4 areas in the
Pacific. Data from the 22 most reliable parasites gave no evidence of discrete stocks of skipjack tuna in the
Pacific, either when analyzed singly or when usinjj combinations of parasites in multivariate analyses. New
Zealand fish carried many tropical parasites, particularly didymozoids, in numbers similar to fish caught in
the tropics, indicating;: that the bulk of these fish had recently migrated from the tropics. The number oiTen-
tirriilnria nnyphaenac. a larval tapeworm, was positively correlated to fish size in the tropics. In New
Zealand, however, fish over 5.5 cm carried about the same number of T. coryphaenxw as fish 45 to 55 cm,
suggesting they had left the tropics when they were 45 to 55 cm and had not returned.
Analysis of the numbers of parasites from particular schools suggested that school members stayed
together for several weeks i)ut not for life.
The use of parasites to delineate stocks for manage-
ment purposes is a well-established technique. For a
comprehensive review of the many examples see
MacKenzie (1983).
The skipjack tuna, Katsuwonus pelamis, is one of
the most valuable fishery resources of the central
and western Pacific. At least 50 species of parasites
have been reported from it. The distribution of only
one, the hemiuroid digenean Hirudinella ventricosa,
has previously been investigated. In the Atlantic,
Watertor (1973) found it in 7% of skipjack tuna off
West Africa, 40% off Brazil, and < 1% off Florida. In
the Pacific, Nakamura and Yuen (1961) found it in
21% of skipjack tuna off the Marquesas and 34% of
fish from Hawaii. Sindermann (1961) pointed out
that analyzing the distributions of combinations of
parasites may provide more information than the ex-
amination of individual species. That, in general, has
been our approach here.
In addition, school-school variation in parasite
numbers was studied to determine how long schools
stayed together, and secondarily to evaluate the
degree of permanence of the parasites.
MATERIALS AND METHODS
Of the 878 fish dissected, 386 were collected by the
Hatsutori Mam on charter to the South Pacific Com-
'Department of Parasitology, University of Queensland, St.
Lucia, Brisbane, Australia 4067.
^Faculty of Science, University of Queensland, St. Lucia,
Brisbane, Australia 4067.
^Fisheries Research Division, New Zealand; present address:
Southpac Fisheries Consultants, P.O. Box 7230, Auckland 1, New
Zealand.
mission (SPC), 246 by the New Zealand Ministry of
Agriculture and Fisheries (NZ), and the remainder
by other governments and fishing companies (see
Acknowledgments). Fish were obtained from 15
areas (Fig. 1, Table 1).
Gills and viscera were frozen and flown to Bris-
bane for dissection. The SPC and NZ fisheries offi-
cers sampled 5 fish/school from a maximum of 3
schools/d. Commercial companies were unable to
sample from individual schools and usually supplied
the head and the anterior ventral body, removed
from frozen fish by a single slanting cut using a band
saw. Fork length, if not supplied, was calculated
Table 1.— Sources of fish dissected.
Avg.
No.
length
Area
Date
fish
(cnn)
A
Palau. Helen
R.
Aug. 1980
35
41
B
Ponape
July 1980
45
59
C
Papua New G
uinea
June 1981
30
50
D
Papua New G
uinea
Nov. 1981
60
41
E
Solomon Is.
June 1980
30
46
F
Coral Sea
Jan. 1982
19
57
G
Fiji
Feb., Mar., Apr..
May 1980
100
50
H
Norfolk Is.
Mar. 1980
21
57
1
New South Wales
Jan. 1981
103
47
J
New Zealand,
west
Mar. 1980;
Jan.. Feb.
1982
69
52
K
New Zealand,
east
Jan. 1980;
Jan., Feb.
1982
163
49
L
Marquesas
Dec. 1979;
Jan. 1980
150
47
M
California
Aug. 1981
30
47
N
Ecuador
Jan. 1982
20
48
0
Atlantic
Mar. 1981
3
50
(Puerto Rico)
Manuscript accepted November 1984.
FISHERY BULLETIN; VOL. 83, NO. 3, 1985.
343
FISHERY BULLETIN: VOL. 83. NO. 3
0
r>
§
o
O
\^
^ ' "^^
J . 0
+3
<
CN
7 — ' 'vrty*^
II
- r^
Z
/^^^Y~^-^
0
^^^^ Vv? \
i\
.-'
fc"'
J / /^
3
II
z
.is
c
\ J^- — '
-
-■— ^— ^-^ 11/
i---7
t.
n /
0
\ /
1 ^"^^"""--^ 1 1
Ja
\ y
\ \ ^^"""""X^ 1
13
J^
1 / / "-^^ /
0
5:
■ / /
II
in
T3
C
1 /
iS
. — ■
—
~__^ /
CO
~^~^^^^~-J /
"i
— ~--^ /o
en
^^^CD
3
/ 1 ^
S
II
1
J
-^
_J
k"
1
and Eas
ico).
-1 —
■— —
"~~ —
15 OJ
1
O; 0
N] iS
s-
'^'
S Si
••
■
£ 3
Z ^
»
i
•
•
0
1
•
0
'
- (O
< II II
•
^ ^ '
. ^ ■Hi
l--g ^
.
•
g iS ^
15 c= 5
•
S 0 js
Ed £ S
- -S N
00
^-— -^
.-t; CO s
0
A —
1
W^
2 ''^
g.W 11
0 sf '^
^
1
'^-> P\>
Z^ C to
1 \
"O -rl Qi
1 \ 1
a> 3 -3
. X °o
> 0 ^
»\
:=■
V
y \Jf
were r
apua N
w Sout
• ,
^— — -"''^^ I \
-C Cm 01
p~~~~--~
LjJ*
'_t --T'''''^ \ 1— 1 \ ,^
« 11^
^•'•'
u_ ^
1.
-^\\^
"Q Jl
1
m
^
1 f^ \ w^
Ic T3 .-
'^ OS C
M
'.■
f^
\A^\f\
^s, A to 0, from
i = Panape; C
= Norfolk Isla
/ ~
\ / \ \ \ /^
.■5 . 1
^ <*-
f
tV^f
1/ \ \ \^
15:
Ree
Fiji;
1 ^
0^.* ^
\ H^~-^ \ V^^
J= S II
^^
<-*!
1
0 "
§3=^-"^^'^
CURE l.-T
Palau, Hel(
iral Sea; G
/
■cr^r-^
— 0
Ci. II 0
344
LESTKK KT Al..; I'AKASITKS OK SKUMACK Tl'NA
from head length using the formula 7.8 + 2.75 x
(head length) for heads under 14.5 cm and - 1.7 +
3.3 X (head length) for larger heads (from measure-
ments of 80 and 83 fish, respectively). Prior to
dissection, fish were thawed overnight at 6°C. In
general, all viscera parasites were counted whereas
gill parasites were counted on one side only and the
numbers doubled in the final tables. A didymozoid
capsule was counted as one parasite though most
contained two individuals. Representative parasites
were fixed and stored in 10% Formalin"* except for
nematodes which were fixed and stored in 70%
alcohol.
An additional set of data on the abundance of the
larval cestode Tentacularia coryphaenae was col-
lected at sea by SPC and NZ fisheries officers. They
recorded the number of Tentacularia visible through
the peritoneum in the wall of the body cavity of 1,529
fish.
Besides some summary statistics, two types of
statistical analysis were done: 1) investigation into
the similarities and dissimilarities of the parasite
fauna between the various areas sampled, and 2) a
study of school integrity.
The similarities and dissimilarities between areas
were examined using a series of cluster analyses and
multivariate canonical analyses (Mardia et al. 1979).
Strictly speaking, canonical analyses require data
which are normally distributed and which have a
common variance. However, the frequency distribu-
tions of the parasites were not normal. They showed
considerable differences from one parasite to
^Reference to trade names does not imply endorsement by the Na-
tional Marine Fisheries Service. NOAA.
another and most appeared to have two components:
one which could be adequately approximated by a
negative binomial distribution; and a second compo
nent consisting of a disproportionately large zero
category, presumably arising because some schools
had not been exposed to infection. Precise trans-
formations to normalize the data would thus have
been complex and of doubtful accuracy considering
the small size of the samples from each school. A
single transformation for all species was therefore
used: the natural logarithm of the number of
parasites plus 1.0.
To avoid possible biases due to associations be-
tween parasite numbers and fish length, such as that
shown in Figure 2, the transformed counts were
then adjusted for fish length. This was done for each
species by regressing log (parasite number + 1.0) on
fish length, for all Pacific tropical fish (489), to esti-
mate the magnitude of any relationship. This was
used to adjust the transformed parasite numbers, ex-
cept where this was zero, to that expected for a fish
of a standard length of 50 cm. (This length was very
close to the overall mean length of the fish.) The
method could not be trusted to eliminate all effects of
length, so, as an added safeguard, only fish 39.5 to
57.5 cm were used in the multivariate analyses (83%
of the total). These are likely to have been 1 yr old
(Uchiyama and Struhsaker 1981; Wankowski 1981).
In a few instances a parasite was absent from all
fish in one area. To allow matrix inversion in the
canonical variate analyses, a random number be-
tween -0.005 and -1-0.005 was added to the data.
This did not influence the outcome. The results of the
canonical variate analyses were displayed graphi-
cally as plots of the first versus the second canonical
25-
20
15
10
5-
30
\ Total tropics (1017 fish)
k New Zealand (512 fish)
AO
50 60
Fish length, cnn
Figure 2. -Relationship between
number of T. coryphaenae and fish
lenjrth. Mean ±2 SE. Each mean from
minimum of 19 fish. In the tropics the
number increased with length but this
was not reflected in the New Zealand
samples.
345
FISHERY BULLETIN: VOL. 83, NO. 3
axes. Confidence limits (95%) for the positions of dif-
ferent areas on these plots are presented as circles
with radius equal to the square root of 5.99/number
of fish in sample (Mardia et al. 1979).
Analyses on the same combinations of parasites
were also done by calculating minimum spanning
trees (Gower and Digby 1981), and dendrograms
from nearest neighbor and centroid cluster analyses
(Clifford and Stephenson 1975), basing similarity
measures on logarithms of area means. Areas were
grouped in a similar way by all methods. Using
clustering algorithms which either ignored or allow-
ed for matches between areas where parasites were
not recorded did not significantly influence results.
For these reasons, and because only canonical
variate analysis provided some measure of reliabili-
ty for its conclusions (confidence rings), only the
results of the canonical analyses are presented
below.
School integrity was examined by comparing the
variability in parasite numbers per fish between
schools, to that within schools, for the two areas
(Marquesas and east New Zealand) where the largest
numbers of schools were sampled. This showed
which parasites were strongly linked to schools, and
also allowed tentative estimation of the length of
time schools remained intact. In theory, for parasites
to show strong school associations two conditions
need to be met: the parasite must heavily infect some
schools and not others, and its life span in the fish
must be equal to or shorter than the life of the school.
Parasites which showed strong school-school associa-
tion were therefore likely to be shorter lived than
those not showing such associations, and other
evidence being equal, were considered less reliable as
population markers than related species.
Two methods were used to compare within and be-
tween school variability in each of the two areas.
First, a series of univariate analyses of variance of
log (parasite numbers -f- 1.0) were done to calculate
the ratio of between school to within school
variances. The magnitude of these ratios, and the
corresponding probabilities that they do not differ
from 1.0, were interpreted as measures of school in-
tegrity. A limitation of this method was that the data
were only approximately normally distributed, par-
ticularly for rare parasites, and thus the derived pro-
babilities were also approximations.
The second method, a median test, was based on
the binomial distribution. The number of parasites of
a particular species in each fish was transformed to a
zero if it was less than or equal to the median number
per fish for the area, and to a one otherwise. The
zeros and ones of each school were then considered
as a binomial sample. If these samples showed
evidence of greater variation than expected by
chance (i.e., too many schools with nearly all zeros or
nearly all ones), then the schools differed with
respect to the distribution of the parasite. A statistic,
approximately distributed as a x^ random variable,
was calculated using GLIM (Baker and Nelder 1978)
to determine whether the binomial samples showed
evidence of differences. Its associated probability
was used as a measure of school integrity. The
method had the useful property of being independent
of the distribution of parasite numbers. For parasites
with a median per fish of <1, the test was based on
the presence or absence of the parasite, though ob-
viously the rarer the parasite the less sensitive the
test.
It is possible that some schools were sampled
twice. If this did happen, the results of both methods
err on the conservative side. Only those species that
gave consistent results by both methods were used to
draw conclusions about school integrity.
RESULTS
Evaluation of Parasite Species
Information was collected on 26 different types of
parasites (species or species complexes) from 15
areas. A summary of the raw data unadjusted for
fish length is given in Table 2.
The parasite species were evaluated for their prob-
able longevity on or in skipjack tuna. For them to be
useful as markers they needed to be relatively long-
lived, preferably surviving for the life of the fish.
Nothing was known specifically about their longevity
in skipjack tuna, though data were available on
related forms (Table 3). In general, intestinal lumen
dwellers appear to be more easily lost than larval
forms encapsulated in the tissues. The 26 skipjack
tuna parasites were divided into four groups, those
considered "temporary", "semi-permanent", and
"permanent", and those not used at all.
Four parasites were not used in any analyses. Two
of the nematodes, Ctena.searophis sp. and Spinitec-
tus sp. (Nos. 23 and 24 in Table 2), were found in the
gut of virtually every fish in which they were sought,
from every area. Their small size meant that the
number recovered was a function of the time spent
searching. They were only counted in every fifth fish,
as were the two larval cestodes from the large intes-
tine, Scolex polymorphus (large) and S. polymorphus
(small) (Nos. 25 and 26). Counting these was time
consuming, their apparent abundance may have
been inversely related to the state of preservation of
346
LESTER ET AL.: PARASITES OK SKllMACK TUNA
Table 2 —Average numbers of parasites per fish in all skipjack tuna (878) from the areas listed in Table 1, unadjusted for
length. The last column gives the correlation coefficient (r) for length against log (parasite number + 1) for Pacific tropical fish.
No.
Parasites
B
H
I
K
M N
1
Caligus spp.
5
17
5
5
10
36
4
3
3
3
1
7
0
1
7
0.37
2
Didymocylindms filiformis
16
5
2
3
4
4
7
3
6
8
10
4
4
3
10
-0 14
3
Didymocylindrus simplex
16
7
4
6
13
11
14
12
18
26
18
14
15
6
3
-0.08
4
Didymoproblema fusitorme
4
1
0
1
1
1
4
1
4
2
3
3
3
1
1
-0.06
5
Lobatozoum multisacculatum
0.1
0.1
0.0
0.0
0.0
0.0
0.1
0.5
0.0
0.1
0.4
0.2
0.3
0.1
0.0
0.03
6
Syncoelium filiferum
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.1
13.1
0.0
0.0
0.0
0.0
0.0
0.0
—
7
Philometra sp.
1
3
4
29
5
P'
2
2
3
3
1
6
6
1
8
002
8
Anisakis type 1
1.0
0.2
2.7
1.0
0.7
1.6
0.2
0.5
0.9
2.1
1.5
0.6
0.2
0.1
2.7
0.13
9
Anisakis type II
0.2
0.0
0.0
0.1
0.0
0.1
0.0
0.4
0.1
0.8
0.2
0.0
0.4
1.2
2.3
-0.02
10
Terra nova sp.
0.0
0.1
0.0
0.0
0.0
0.1
0.1
0.0
0.0
0.0
0.0
0.2
0.1
0.0
0.0
0.06
11
Coeliodidymocystis sp.
1.3
2.1
0.3
0.2
0.9
0.2
1.2
0.5
0.3
0.7
1.3
0.8
0.1
0.7
0.0
0.03
12
Tentacularia coryphaenae
3
22
P'
3
4
19
8
6
4
5
6
10
3
P'
P'
0.48
13
Oesophagocystis dissimilis
12
6
8
7
8
12
9
3
6
3
9
8
8
9
11
-0.05
14
Kollikeria 1 Didymocystis spp.
13
4
1
5
9
4
7
7
8
4
5
6
11
5
6
-0.11
15
Dinurus euthynni
55
9
19
35
66
1
2
3
0
0
0
15
0
0
0
-0.34
16
Dldymocystoides intestino-
musculans'
30
27
26
37
49
39
54
18
15
12
16
44
134
17
64
-0.14
17
Hirudinella ventricosa
0.4
0.6
0.4
0.2
1.1
0.7
0.4
0.3
0.1
0.0
0.0
1.1
0.1
0.2
1.0
-0.10
18
Raorhynchus terebra
22
16
13
17
15
18
25
65
4
2
4
12
3
1
0
-0.00
19
Dldymocystoides intestino-
muscularis'
14
3
3
9
3
8
5
8
6
6
6
7
13
3
2
-0.24
20
Lagenocystis 1
Univitellannulocystis spp.
76
40
29
29
22
45
43
16
38
17
30
61
178
34
41
-0.11
21
Tergestia laticollis
0.0
0.0
0.0
0.0
0.0
0.0
0.1
0.8
0.0
0.0
0.0
0.1
0.0
0.0
0.0
0.00
22
Rhipidocotyle sp.
0.0
0.3
0.0
0.2
0.2
2.3
2.4
0.0
1.3
0.0
0.0
0.1
0.0
0.0
0.0
0.08
23
Ctenascarophis type
35
7
6
2
18
22
38
49
7
17
21
33
4
1
108
24
Spmitectus type
10
7
20
2
12
5
9
10
5
6
18
13
5
3
10
25
Scolex polymorphus (large)
4
0.4
0.2
0
7
166
33
P'
122
101
27
10
161
9
7
26
Scolex polymorphus (small)
200
124
1,089
287
8,900
257
463
140
211
53
24
206
495
153
105
'P
' = present.
^N
lo. 16— stomach; No. 19— intestine.
the fish, and their longevity was doubtful.
Philometra sp. (No. 7) was found predominantly in
developed ovaries, which were present in less than
half of the fish sampled. The data were used for com-
paring school-school variability only.
Seven parasites were considered "temporary".
They appeared to be short-lived or easily lost from
the fish. The caligoid copepods (No. 1, primarily
Caligits productus in the tropics and C. bonito in
temperate waters) were not permanently attached
and probably moved from fish to fish (Kabata 1981).
Syncoelium filiferum (No. 6) was common on the
gills in New South Wales and New Zealand samples
(I, J, and K), but was not recovered from anywhere
in the tropics. It is common on fish endemic to New
Zealand (D. Blair^). It was considered possibly a
temperate short-lived parasite, at least on skipjack
tuna, and this was verified by the school integrity
study and by conventional tagging data (see later).
Some hemiurids are known to be readily lost from
the gut of other species of fish (Table 3). Margolis
and Boyce (1969) observed that over half the Leci-
thaster gibbosus were lost from salmon fingerlings
*D. Blair, Deparlment of Zoology, University of Canterbury,
Christx;hurch, New Zealand, pers. commun. September 1984.
within 3 wk of bringing the fish into captivity. We
found Dinurus euthynni (No. 15) in all tropical sam-
ples from the central and western Pacific but not in
the temperate samples I, J, and K. As it showed
strong school associations and as the didymozoid
data described later showed that New Zealand fish
had a recent origin in the tropics, D. euthynni was
evidently a short-lived tropical parasite that was lost
as the fish migrated south. This also appeared to be
true for Hirudinella ventricosa (No. 17) and possibly
for two relatively rare gut-lumen digeneans, Terges-
tia laticollis (No. 21) and Rhipidocotyle sp. (No. 22).
In other fish, adult acanthocephalans may be short
lived (Table 3). Moller (1976) found that over half the
Echinorhynchus gadi in three species of fish were
lost within 2 wk of the fish being brought into capti-
vity. In our data, Raorhynchus terebra (No. 18) was
present in reduced numbers in I, J, and K, sug-
gesting it was lost in southern waters. All these
parasites then were labelled "temporary".
Didymozoid digeneans were considered "semi-
permanent" parasites. In other fish, some didymo-
zoids, or at least the remains of them, are believed to
stay in the tissues for the life of the fish. Others, in-
cluding some species found in the gonads or gills, are
lost annually (Table 3). In general, therefore, skip-
347
FISHERY BULLETIN: VOL. 83, NO. 3
0)
o
c
<0
cc
CO
c
♦^
o
CO
CO
T3
C
3
o
CD
CO
O
T3
CD
m
CO
v
CO
CO
CO
o.
CO
c
CO
o.
CO
E
3
E
"x
CO
E
«
CO
o
I
ffi
<
c
to
Q.
CO
CO
o
CD
CO
CO
k_
CO
t^ r^ t^ i^ -j-
<y> <y> o> o>
03 flj 0) ^
o o o o
CO
c
<D
Q.
CO
Q.
0> O) 05
CO CO C£>
G) 0> CT)
0} (1) 0)
o o o
o o o
CO CD CD
^•O T3 T3 ^^
1- CO (O (O 05
Q) o o o ■""
cj (3) ra o) J:
>- ^ b b o
Q CO (0 (0 Q
CD s 2 :s CO
CO
CO
o>
^ ^
^
o
o
- —
oo
00
:
O)
CJ)
♦-
fc_
^
OJ
Q)
CD
•«-
in
CO
(U
0)
(1)
w
_j
_J
C- ^'CD
._ c o>
9^ E -
III
-§ C (0
-I w 2
CO
3
S.
cr
CO
3
o
o
CO
3
CO
s
CO
CO
to
CO
•S
2
Q.
3
3
.C
CO
_s
•~
CD
CO
k>
s
O
-C
>,
3
CO
S
(D
<b
CO
o
-c
CO
CJ
3
o
o
5
ncdS
1^
Q. CO
CD CD
■c x:
CJ o
CO CO
3 3
■s-s
o o
CO CO
3 3
-C -C
o o
c c
CO
3
C
CO C
3 <P
CO
3
CD
C
CO
E
3
-B
is
o
<D
w .i.. «^
CD CD .;;
c
0)
CD
O O QJ <D
OOO O «?:
3 CD
w S^ o
•S ~ CD
•^ i5 CJ
CO
3
a.
CO <=^
3 <"
D) CO
ri C 3
C Q) ir
5 §.§
a> 3 c:
S OO
03 0) 0) O CD
E E E E E
CO CO CO CO CO
CD (D (D d) d)
C C C C C
CJ CJ o
<X) a> 0}
CO CO CO
o o o ^ ^
"a "D "o o o
C C C CO CO
CO CD CD E £
.^ *: *j O o
£ S £ CO w5
■O 13 ■©
CD CD CD
O) O) O)
CO
CO ^
"co o
-I
CO Uu
o
<
CO CO
3 3
-C j:
o o
c c
■c -c
o o
c c
■c -c
o o
UJ UJ
CD CO
(o to
^2
p o
■S o
o -c
S c
i: CO
O CJ
UJ <
CO
3
CO
O
Q lo
5.S
o 5
CO
3
CO
o
« -Q
5:9 —
B) 5) 3
^ ^ .9
CD Cb
E
3
O
o
i^
O CD
•Q CD r-
esI
3 rj)
^^-§
o o o
o E E
-~l TJ ^
CO
cn
CO S'
O .^
QJ CU
■C C
cS
O Q.
O CO
O E
E
C is >~
- o o
CD -(3
O
E 2^
O S m
Q) Q) 5
CO
CO
3 ci
CD n
c o
■=^ ^
1 1
II
O H
CO
(T>
...i^
o
^—^
t^
a>
c
'-
CO
CO
r^
E
T3
C3>
o
C-
O)
j;
C
CO
CO
CO
S
Q.
CO CO
CB CD
>% >>
^ J£ ^
^ .^
o o
o o o
o
CO
CO
CO
5 5 5
5 5
E E
E E E
E
O
i^
^ CO «
CM CO t^
■>- oo
C3> ID
oo •.- o
oo
T—
,- <D 0)
■^ V
V A
CO 1-
A
A
A
A
A A
, > >
A CD CD
CO CO
3
Cn
CD
cr
3
<ii
*-
•i
r
CD
CO
o
•C
^
E
CD
CD
fn
U>
C
•^
U.
■^
■n
CO
CD
O
bo
>~ >N
>%
>->.>.
k_ k_
>
CD CD
QJ
CD CD CD
CO (D
.^ O —
C C
C
C C C
£" "
0) CD
(D
<D CD CD
CO cj CO
CO CO
CO
CO CO CO
> 3 3
CD (D
CD
CD CD 0)
O CQ S
2 S
2
2 S 5
CD
CO
c
CD
CO
3 C
k^ —
O -^
.C CO
Q_ CO
OC _
CD ■;= £
CJ
Cb
CO
cn
E
3
O
CO CD
CD
>
CD
348
I.KSTKKKTAL.: PAKASITKSOF SKIIMACK TUNA
jack tuna didymozoids were thought to be in the fish
probably for at least several months. However, there
was some suggestion that 3 of the 10 skipjack tuna
didymozoids had a shorter adult life span than the
others. Didymozoid No. 16 was much less common in
New Zealand waters than in the tropics (Table 4),
and didymozoid Nos. 19 and 20 were also less com-
mon and, in addition, showed strong school associa-
tions (see later). These three didymozoids (possibly
representing four species) were omitted from the
analysis for Figure 3.
The remaining four parasites (Nos. 8, 9, 10, and
12) were classed as "permanent". Larval cestodes
and nematodes, particularly those found in the
tissues, are generally believed to survive for several
years, often for the life of the fish (Table 3). They
have been used successfully many times as fish
population markers (see MacKenzie 1983). In skip-
jack tuna, the larva of a trypanorhynch cestode, Ten-
tacuLaria coryphaenae, was found in the wall of the
body cavity and occasionally in the viscera. No
degenerating forms were seen, suggesting that it
survived for an extended period and hence could be
an excellent population marker, though counts were
not available from areas C, N, and 0. Larval
anisakids were found on the wall of the stomach or in
the mesentery. The literature suggested that they
should also be good long-term markers (Table 3).
They were counted in all areas.
Protozoan parasites have been used successfully to
separate stocks of several species of fish. However,
none has been reported from skipjack tuna, and we
found none in this study.
Table 4— Average number of didymozoids in New Zealand
fish (all lengths) compared with fish caught m the tropical
western Pacific (areas A, B. C, D, E, F, G, and L). In paren-
theses, log (X -I- 1) length-adjusted means for fish 40 to 57 cm
only.
No.'
Parasite
New Zealand
Trop
ics
2
D. filiform is
9
(1.1)
6
(0.8)
3
D. simplex
20
(1.7)
12
(1.3)
4
D. fusiforme
2.7
(0.6)
2.5
(0.5)
5
L. multisacculatum
0.3
(0.1)
0.1
(0.0)
11
Coeliodidymocystis sp.
1.1
(0.4)
0.9
(0.3)
13
0. dissimllis
7
(1.3)
9
(1.9)
14
Kollikeria 1 DIdymocystis
spp.
5
(1.2)
6
(1.5)
16
D. mtestinomuscularis'
15
(1.8)
41
(3.3)
19
D Intestinomuscularis^
6
(1.3)
7
(1.4)
20
L. katsuwoni 1 U. kat-
suwoni
26
(1.9)
47
(2.3)
No. of fish
232
(213)
469
(364)
'Code no. from Table 2.
^Stomach.
^Intestine.
Relationships Between Areas
Analyses of individual distributions of permanent
and semipermanent parasites showed that the abun-
dances of individual parasites varied across the
Pacific. However, these differences were inconsis-
tent, the pattern established by one parasite being in
conflict with that of a second, and so on.
The data from the three anisakid nematodes and
the seven didymozoids considered longest lived were
therefore analyzed using canonical variate analysis.
Because of the more permanent nature of these
parasites and the completeness with which they were
recorded from all areas, these data were considered
the most reliable for statistically assessing the
similarities and dissimilarities between areas. The
first three canonical axes accounted for 75% of the
Figure 3. -Results of multivariate analysis using 3
"permanent" and 7 "semipermanent" parasites (Nos. 2,
3, 5, 8, 9, 10, 11, 13, and 14). Values for first two can-
nonical vectors plotted, and 95% confidence rings in-
dicated for samples of more than 24 fish. The letters
refer to the sampling sites indicated in Figure 1.
349
FISHERY BULLETIN: VOL. 83, NO. 3
variation in area-to-area differences in parasite
numbers. A plot of the first two, accounting for 58%
of the variation, showed the Atlantic fish (0) to be
distinct from all the Pacific ones, even though only
three fish from the Atlantic were dissected (Fig. 3).
However, fish from California (M) and Ecuador (N)
fell close to the western Pacific samples. They were
separated out on the third axis (not shown), but
nevertheless it is evident that they had a somewhat
similar parasite fauna. The fish from western New
Zealand (J) appeared distinct, and so too, to a less ex-
tent, were the Papua New Guinea samples (C and D).
There is no suggestion that fish from Ponape (A),
Palau (B), Solomon Islands (E), Fiji (G), and the Mar-
quesas (L) had distinct faunas of these long-lived
parasites.
H-
Figure 4. -Results of multivariate analyses using 7 "temporary'"
parasites (Nos. 1, 6, 15, 17, 18, 21, and 22). 95% confidence rings
given for samples of more than 24 fish.
In this analysis, Anisakis II had the most powerful
discriminating properties, though at least 7 of the 10
parasites used were capable of substantial discrimi-
nation in their own right.
An analysis based on the 7 "temporary" parasites
(Nos. 1, 6, 15, 17, 18, 21, and 22) produced a much
greater separation of areas (Fig. 4). They are
grouped into two broad classes: one containing New
South Wales (I), New Zealand (J, K), and the eastern
Pacific (M, N); and the other the western tropical
areas. Each area in the latter group had a temporary
parasite fauna that was distinct from most other
areas. Over 83% of the variation was accounted for
by the first two axes, and 90% by the first three. It is
interesting to note that New South Wales (I) is more
similar to east New Zealand (K) than to west New
Zealand (J) (this was much more marked on the third
axis, not shown, where I and K were pulled to one
side), and that west New Zealand is similar to
California (M) and Ecuador (N).
Taken together. Figures 3 and 4 indicate that
several distinct skipjack tuna parasite faunas existed
within the tropical Pacific, and the longer lived
parasites were more evenly distributed than the
shorter lived ones.
To check these results and to look for links be-
tween the New Zealand fish and the tropical areas,
the west Pacific data were reanalyzed using first the
10 "semipermanent" parasites (the didymozoids) and
second the 4 "permanent" parasites (anisakids and T.
coryphaenae).
The average numbers of didymozoids in the New
Zealand fish were almost identical to the overall
average for the central and western tropics (Table
4). In the multivariate analyses, the temperate water
samples fell to one side of the tropical samples (Fig. 5
Figure 5. -Results of multivariate analysis using 10
didymozoids only (Nos. 2, 3, 4, 5, 11, 13, 14, IK, 19, and 20).
95% confidence rings given for samples of more than 24 fish.
350
LESTKKKTAL.: I'AKASI TKSOK SKIIMACK Tl'NA
- H, I, J, K), possibly because of the three didymo-
zoids suspected of being relatively short-lived (Nos.
16, 19, and 20). The east and west New Zealand sam-
ples (J, K) were identical on the first two axes, and
separated only slightly on the third axis (not shown).
There was no obvious link between New Zealand and
any particular tropical area.
Similarly, the larval nematodes and T. cory-
phaenae (Nos. 8, 9, 10, and 12) did not suggest a link
between New Zealand fish and those from any par-
ticular tropical area (Fig. 6). However, west New
Zealand (J) now appeared distinct from east New
Zealand (K) and New South Wales (I). The separa-
tion was due to areas having either high Anisakis I
and II and low Terranova and T. coT^phaenae or low
Anisakis I and II and high Terranova and T. cory-
phaenae. West New Zealand (J) was at one extreme
(high Anisakis) and the three most northwestern
areas- Ponape (B), Fiji (G), and Marquesas (L)-at
the other. Tentacularia coryphaenae and probably
Terranova were picked up in the tropics. It seems
likely that one or both of the Anisakis larvae were
picked up predominantly in temperate waters, par-
ticularly in west New Zealand. This may explain the
separation of west New Zealand from the other areas
in Figure 4.
In summaiy, the New Zealand fish were not close-
ly aligned with any particular tropical sample, and
the eastern and western New Zealand fish were
probably carrying similar parasite faunas when they
arrived in New Zealand.
Tentacularia coryphaenae
Data on this parasite are presented in detail
because we had more than for any other parasite and
because potentially it was our most valuable marker.
It also was the subject of many queries from skipjack
tuna processors. The parasite was common through-
out the south, central, and west Pacific (Table 3,
parasite No. 12). The means of samples of over 22
fish within the length range 44 to 53.9 cm suggested
an east-west cline across the Pacific, with twice as
many parasites being found in fish from around the
Marquesas (L) as around Papua New Guinea (C and
D) (Fig. 7). A regression analysis of number of para-
sites against longitude using tropical data on the
number of parasites in 972 fish, transformed and ad-
justed for differences in host length (data collected
independently by the SPC), showed that the relation-
ship was statistically significant, though it only ac-
counted for about 7% of the fish-to-fish variation.
Considering fish of all sizes, the number of T. cory-
phaenae in the tropics increased with the size of the
Figure 6. - Results of multivariate analysis using the four
"permanent" parasites (anisakids and T. coryphaenae, Nos.
8, 9, 10, and 12). 95% confidence rings given for samples of
more than 24 fish.
fish (Fig. 2, solid circles). The increase around 47 cm
is due to many of the Marquesas fish being this size
and Marquesas fish tended to have more T. cory-
phaenae. In New Zealand, smaller fish had about the
same average number as fish from the tropics. How-
ever, this number did not increase with size (Fig. 2,
open circles). Thus, the 58 -t- New Zealand fish had
fewer parasites than their peers in the tropics, and
about the same number as the 45 to 50 cm fish.
School-to-School Variation
An analysis of variance, and a median test, were
carried out on 30 schools from the Marquesas and 19
schools from eastern New Zealand (areas L and K,
respectively. Table 5). The results of the two
methods on each data set show close agreement.
In the Marquesas, five parasites showed strong
evidence of association with particular schools, i.e.,
the probability that schools differed was at least 0.95
with both methods. The parasites were Caligtis spp.
(No. 1), D. euthynni(bio. 15), H. ventricosa{No. 17),
D. intestinomuscularis (No. 19), and Lagenocystisl
Univitellannulocystis spp. (No. 20). For these para-
sites to show significant differences, they must have
heavily infected some schools and not others, and
their life span in the fish must have been equal to or
shorter than the life of the school. The literature
review suggested that the first three species could
possibly be readily lost from fish, and this is vin-
dicated by their strong school association. The evi-
dent impermanence of the last two, however, was
unexpected. It was as a consequence of this finding
that they were not included in the analysis for Figure
3.
351
FISHERY BULLETIN: VOL. 83, NO. 3
0
5
(26)
^=:^
X-
7
7
(40)
(156)
11
(309)
Figure 7. -The average numbers ofT. coryjihaenne in skipjack tuna 44 to 58.9 cm long in samples of over 22 fish. Note that the iiumi)er in-
creased to the east. (In parentheses, number of fish sampled.)
Several other parasites thought to be short-Hved,
such as R. tereba, did not show up in the test,
presumably because their infective stages were
relatively evenly distributed in the tropical Pacific.
In New Zealand, parasites showing close associa-
tion with particular schools (using both tests) were L.
multisacculatum (No. 5), S. filiferum (No. 6),
Philometra sp. (No. 7), Coeliodidymocystis (No. 11),
T. coryphaenae (No. 12), R. terebra (No. 18), and D.
intestinomuscularifi (No. 19). Syncoelium filiferum
and R. terebra were both thought to be temporary
parasites that could be gained in New Zealand or ad-
jacent waters (Norfolk Island). The origin of the
Philometra was unknown. Their number reflected
the state of maturity of the fish and this varied be-
tween schools. However, we were left with three
didymozoids and T. coryphaenae, all of which dif-
fered markedly between schools in eastern New
Zealand. One of the didymozoids, L. multisaccula-
tum, a normally rare tropical parasite, was found on
all five fish from one school (numbers per fish 1, 2, 8,
3, and 1). As the three didymozoids and T. cot^-
phaenae are essentially tropical parasites, the schools
had evidently not fully mixed while in temperate
waters.
If this is true, these four parasites could not have
been picked up uniformly across the Pacific. Evi-
dence is given above that D. intestinmnuscularis
(No. 19) was not picked up uniformly even within the
Marquesas. For the other species, a comparison of
their mean numbers per fish per school in different
areas of the tropical Pacific showed that Coeliodidy-
m.ocystis sp. and particularly T. coryphaenae were in-
deed more abundant in some areas than others.
Lobatozoum multisacculatum was too rare for any
conclusions to be drawn in this respect.
352
LESTER ET AL.: PARASITES OF SKIPJACK TUNA
Table 5.— Comparison of within and between sctiooi vari-
ability in numbers of parasites per fish for two areas.
no.
Marquesas
New Zealand
Parasite
Analysis of
Median
Analysis of Median
(see Table 3)
variance'
test'
variance test
1
. ..a
* * *
2
* *
3
*
4
5
* * * * *
6
(no parasites found)
* * • * * *
7
* *
8
*
9
10
(no parasites found)
11
* *
12
* * * *
13
*
14
15
* * *
* *
(no parasites found)
16
17
*
*
18
* * * * * *
19
* * *
* * *
* * * *
20
* *
* * *
21
*
22
'The probabilities that the ratio of the between and within
school variances is no greater than one. (Based on transform-
ed data, i.e., log (parasite no. + 1.0).)
'The probabilities that the proportion of fish with more
than the area median is the same for all schools.
3* * • = P< 0.001 ; * * = P < 0.01 ; * = P < 0.05; blank = P >
0.05.
Rate of Mixing of Schools
To estimate the rate of mixing of schools we need-
ed to know the distribution of the parasites among
schools before, and after, some known time interval.
This we did not have for any of the Marquesas
samples.
In New Zealand, however, some approximate
calculations could be made because schools arrived
from the tropics at different times. Sixteen of the 19
east New Zealand schools were of similar-sized fish
and were all caught within 1 mo. These schools were
divided into two groups: "early arrivals" and "recent
arrivals". (This was done by ranking the schools
using a combination of four parasites whose
prevalences were positively correlated with each
other, Nos. 16, 18, 19, and 20, and which were
thought to be relatively short-lived parasites picked
up in the tropics. Thus high numbers indicated a
recently arrived school.) From catch data (Habib et
al. 1980), we calculated that there was an average of
3 to 4 wk between the capture of 25% and 75% of
the annual catch. This interval was taken as the ap-
proximate period between the arrival times of the
early group and the recent group. If mixing was
occurring, one would expect that the school-school
differences for tropical parasites would be greater
when the fish first arrived (the recent arrivals) than
after they had been there for a few weeks (the early
arrivals). However, this we could not demonstrate.
Our sample sizes at this point were rather small
(eight schools in each category), and in fact the
reverse appeared to be the case, the early schools
having a generally higher variability than the recent
arrivals. This suggested that the early arrivals had
come from several areas (and still had not fully mix-
ed), whereas many of the later arrivals had perhaps
come from one area.
DISCUSSION
Ten of the 26 parasites counted were species of
didymozoid trematodes. These are almost exclusively
a tropical group. Yamaguti (1970), for example,
found 84 different species of didymozoid in fish
around Hawaii. None were recorded in checklists of
parasites from New Zealand (Hewitt and Hine 1972)
or Canada (Margolis and Arthur 1979). Thus,
although skipjack tuna are caught in both tropical
and temperate waters, their didymozoid infections
are evidently picked up primarily in the tropics.
Larval didymozoids have been found in small fish
and in invertebrates. It is almost certain that the
definitive host becomes infected by feeding on an in-
fected intermediate host (Cable and Nahhas 1962;
Nikolaeva 1965). In the tropics skipjack 40 to 60 cm
in length feed largely on fish, squid, and stomatopods
(Argue et al. 1983). In New Zealand, however, they
feed almost exclusively on euphausids (Habib et al.
1980, 1981). This completely different diet in New
Zealand, together with the fact that no endemic New
Zealand fish are known to carry any didymozoids,
lead us to the conclusion that few, if any,
didymozoids are picked up in New Zealand waters.
The occurrence of 10 species of didymozoids in
skipjack tuna caught in New Zealand, in numbers
very similar to fish of the same size caught in the
tropics, thus indicates that New Zealand and tropical
fish were found until recently in a similar tropical en-
vironment. Almost certainly, the New Zealand
fishery is based on fish that have recently migrated
from the tropics, and not on fish recruited as post-
larvae in temperate waters. This disagrees with tag-
ging data which show that the bulk of New Zealand
skipjack tuna of known origin were off New South
Wales 10 mo earlier. However, the tagging inference
is applicable to < 4% of the total New Zealand fish
(Argue and Kearney 1983). Our conclusion is in
agreement with Argue et al. (1983) who found no
juvenile skipjack tuna in the stomachs of adults from
353
FISHERY BULLETIN: VOL. 83, NO. 3
subtropical waters, though juveniles formed a signi-
ficant component of the adult diet in the tropics.
The absence of degenerating T. coryphaenae and
the positive correlation of parasite number and host
length suggest that the parasite was long-lived and
accumulated in the fish with age. The low numbers of
Tentacuiaria in the 57 -i- cm fish caught in New
Zealand indicate that these fish have had a different
history from their peers in the tropics. The bulk of
the skipjack tuna caught in New Zealand are 45 to 55
cm long. Less than 10% measure 60 cm or more
(Habib et al. 1980, 1981). We have concluded above
that the majority of New Zealand fish recently
arrived from the tropics. The T. coryphaenae data in-
dicate that the 57 -i- cm fish left the tropics at 45 to
55 cm long and have not returned. Evidently as fish
age, they become less migratory. This was hypothe-
sized by Kearney (1978).
Large fish were not necessarily permanent resi-
dents in New Zealand, however. Of 17 57-t- cm fish
on which full dissections were carried out, 2 were
carrying the acanthocephalan R. terebra, a parasite
thought to be relatively short-lived (see above) and
not picked up in New Zealand. Raorhynchus terebra
was common in fish from Norfolk Island (area H).
Thus some of the large fish may have recently come
from areas as far away as Norfolk Island.
The first two canonical variate analyses comparing
all areas sampled suggested that fish 40 to 57 cm
long had moved between areas and carried the
longer lived parasites with them. Parasitologically,
there was no evidence of more than one stock of skip-
jack tuna in the Pacific. Richardson (1983) observed
an east-west cline in the gene frequency of two en-
zymes across the Pacific. From an analysis of 200
gene frequencies he proposed an "isolation by
distance" model for skipjack tuna. In this, the degree
of mixing of skipjack tuna genes was inversely pro-
portional to the distance between the spawning
areas. Tagging data have confirmed that there is
some mixing of adult skipjack tuna in the central and
western Pacific (Kleiber and Kearney 1983), though
more than 95% of the tagged fish recovered during
the SPC program were caught within 1,000 mi of
their point of release (Kearney 1982).
Schools of skipjack tuna have been observed to
break up when feeding (Forsberg 1980). This and
observations from aircraft where schools have been
seen to merge and later separate (Habib unpubl.
obs.) have led to the hypothesis that skipjack tuna do
not remain in a particular school for more than a day
or so. Certainly the pattern of recovery of SPC tags
suggested that tagged skipjack tuna underwent con-
siderable mixing amongst schools soon after release
(Argue and Kearney 1983). However, using Mar-
quesas data we found that several parasites showed
strong school associations, particularly didymozoid
Nos. 19 and 20 (D. intestinomfiuscularis and Lageno-
cystislUnivitellanulocystis spp.). In another didymo-
zoid, Neometadidymozoon helwis from the gills of
Platycephalus fuscus, it takes up to a year for the
worms to migrate through the tissues, pair up,
mature, and die (Lester 1980). Though only a short
migration is needed for didymozoids 19 and 20, as
they are intestinal parasites, the worms are still like-
ly to be in the skipjack tuna for a period of weeks.
Thus, their strong association with particular schools
suggests that school half-life is likely to be in terms of
at least weeks rather than days.
In New Zealand, the large school-school differ-
ences observed in the numbers of T. coryphaenae
and several other tropical parasites, especially in the
early arrivals, indicate that at the time of catching,
the New Zealand schools had not mixed sufficiently
to mask their previously distinct tropical faunas.
Do schools remain intact for an extended period,
perhaps for the life of the fish? Sharp (1978) found
evidence of genetic similarity between individuals in
core schools, suggesting that some members of the
school were siblings. However, none of L. multi-
sacculatum, Coeliodidymocystis sp., or T. coinj-
phaenae, three long-lived parasites that showed
significant school-school differences in New Zealand,
showed any significant differences in the Marquesas.
This suggests that within the probable long life of
these parasites, fish caught in the Marquesas had
changed schools and had thus obscured any patchi-
ness in the distribution of the infective stages of the
parasites. The parasitological data, then, do not sup-
port the hypothesis that fish stay in the same school
for life.
ACKNOWLEDGMENTS
We are indebted to R. E. Kearney, A. W. Argue,
and other officers of the Skipjack Program, South
Pacific Commission, for much of our material, much
of the Tentacuiaria data, and assistance in preparing
this report. Other material was obtained with the
help of David Bateman, Heinz Tuna Cannery, Eden,
N.S.W.; Paul Dalzell, D.P.I. Fisheries Research, Ka-
vieng, P.N.G.; Bernie Fink, Van Camp Sea Food Co.,
San Diego, CA; James Joseph, lATTC, La Jolla, CA;
Ted Morgardo, Star-Kist PNG Pty. Ltd., Rabaul,
P.N.G.; and Ronald Rinaldo, Southwest Fisheries
Center, La Jolla, CA. Their cooperation is greatly
appreciated.
Taxonomic assistance was rendered by David
354
LKSTKKKTAl..: I'AkASITKS (IK SKllMACK 'ITNA
Blair, Department of Zoology, University of Canter-
bury. N.Z.; Rod Bray, British Museum (N.II.). Lon-
don, U.K.; and Arlene Jones, Commonwealth Insti-
tute of Parasitology, St. Albans, U.K. For help with
the dissections we thank C. Boel, K. Couper, B. M.
Heath, M. K. Jones, M. S. Kennedy, G. G. Lane, and
A. G. West. K. MacKenzie, D.A.F., Scotland, kindly
reviewed an earlier draft of the manuscript.
The project was supported by a grant to H. M. D.
Hoyte, Department of Parasitology, University of
Queensland, from the Nuffield Foundation, U.K.
LITERATURE CITED
Argue, A. W., F. Conand, and D. Whyman.
1983. Spatial and temporal distributions of juvenile tunas from
stomachs of tunas caught by pole-and-line fjear in the central
and western Pacific Ocean. Tuna Billfish Assess. Pro-
tjranime Tech. Rep. 9, 47 p. South Pacific Commission,
Noumea, New Caledonia.
.Arcte. A. W.. AND R. E. Kearney.
1983. An assessment of the skipjack and baitfish resources of
New Zealand. Skipjack Survey Assess. Programme Final
("try. Rep. 6, 68 p. South Pacific Commission, Noumea, New
Caledonia.
Baker, R. J., and J. A. Nelder.
1978. Ceneralised linear interactive modelling. Numerical
Algorithims (Jroup. Oxford. p]ngl., 184 p.
BOYCE. N. P.
19(i9. F'arasite fauna of j.iink salmon (()nciirhynchui< gor-
hu,'<rha) of the Bella Coola River, central British Columbia,
during their early sea life. J. Fish. Res. Board Can. 26:813-
820.
Cable, R. M., and F. M. Nahhas.
1962. Lepo.s sp., second intermediate host of a didymozoid
trematode. J. Parasitol. 48:34.
Clifford, H. T., and W. Stephenson.
1975. An introduction to numerical classification. Acad.
Press, N.Y., 229 p.
Forsberg, E. D.
1980. Synopsis of biological data on the skipjack tima, Katsu-
ivonu.'i pelami,'< (Linnaeus, 17,58), in the Pacific Ocean.
lAlTC Spec. Rep. 2, p. 296-360.
(iOWER, J. C, AND P. G. N. DiGBY.
1981. Expressing complex relationships in two dimensions.
In \'. Harnett (editor). Interpreting multivariate data, p. 83-
118. Wiley. N.Y.
Habib, G, I. T. Clement, and K. A. Fisher.
1980. The 1979-80 purse-seine skipjack fishery in New Zea-
land waters. N.Z. Fish. Res. Div. Occas. Publ. 29:1-43.
1981. The 1980-81 purse-seine skipjack fishery in New Zea-
land waters. N.Z. Fish. Res. Div. Occas. Publ. 36:1-52.
Hewitt, G. C, and P. M. Hine.
1 972. Checklist of parasites of New Zealand fishes and of their
hosts. N.Z. J. Mar. Freshw. Res. 6:69-114.
Kabata, Z.
1981. Copepoda (Crustacea) parasitic on fishes: problems and
fierspectives. Adv. Parasitol. 19:1-71.
Kearney, R. E.
1978. Some hypotheses on skipjack (Katsuwonus pelamis) in
the Pacific Ocean. South Pac. Comm. Occas. Pap. 7, 23 p.
South Pacific Commission, Noumea, New Caledonia.
1982. An assessment of the skipjack and baitfish resources of
Fiji. Skipjack Survey Assess. Programme P^inal Ctry. Rep.
1 , 48 p. South Pacific Commission, Noumea, New Caledonia.
Kleiber, p., and R. E. Kearney.
1983. An assessment of the skipjack and baitfish resources of
Kiribati. Skipjack Survey Assess. Programme Final Ctry.
Rep. 5, 49 p. South Pacific Commission, Noumea, New
('aledonia.
Lester, R. J. G.
1980. Host-parasite relations in some didymozoid trematodes.
J. Parasitol. 66:527-531.
Lubieniecki, B.
1976. Aspects of the biology of the plerocercoid of Grillotia
erinaceus (van Beneden, 1858) (Cestoda: Trypanorhyncha)
in haddock Melanogrammus aegkfinus (L.) J. Fish. Biol. 8:
431-439.
Mackenzie, K.
1983. Parasites as biological tags in fish population studies.
Adv. Appl. Biol. 7:251-331.
Mardia, K. v., J. T. Kent, and J. M. Bibby.
1979. Multivariate analysis. Acad. Press, N.Y., 521 p.
Margolis, L.
1965. Parasites as an auxiliar\' source of information about the
biology of Pacific salmons (Genus Oncorhynchus). J. Fish.
Res. Board Can. 22:1387-1395.
1970. Nematode diseases of marine fishes. In S. F. Snieszko
(editor), A symposium on diseases of fishes and shellfishes, p.
190-208. Am. Fish. Soc. Spec. Publ. 5.
Margolis, L., and J. R. Arthur.
1979. Synopsis of the parasites of fishes of Canada. Bull.
Fish. Res. Board Can. 199, 269 p.
Margolis, L., and N. P. Boyce.
1969. Life span, maturation, and growth of two hemiurid
trematodes, Tulmiovesicula Hndhergi and Lecithaster gihho-
STis, in Pacific salmon (genus Oncorhynchus). J. Fish. Res.
Board Can. 26:893-907.
MOLLER, H.
1976. Reduction of the intestinal parasite fauna of marine
fishes in captivity. J. Mar. Biol. Assoc. U.K. 56:781-785.
Nakamura, E. L., and H. S. H. Yuen.
1961. Incidence of the giant trematode, Hirudinella marina
Garcin, in skipjack tuna, Euthynnus pe/am(^ (Linnaeus), from
Marquesan and Hawaiian waters. Trans. Am. Fish. Soc. 90:
419-423.
NiKOLAEVA, V. M.
1965. On the developmental cycle of trematodes belonging to
the family Didymozoidae. [In Russ.] Zool. Zh. 44:1317-
1327.
PaPERNA, I., A. COLORNI, H. Gordin, a.nd G. W. Kissil.
1977. Diseases of Sparun auratn in marine culture at Elat.
Aquaculture 10:195-213.
Platt, N. E.
1976. Codworm - a possible biological indicator of the degree
of mixing of Greenland and Iceland cod stocks. J. Cons.
Perm. Int Explor. Mer 37:41-45.
Richardson, B. J.
1983. Distribution of protein variation in skipjack tuna {Kat-
suwonus pelamis) from the central and south-western Pacific.
Aust J. Mar. Freshw. Res. 34:231-251.
ScOTT, J. S.
1969. Trematode populations in the Atlantic argentine,
Argentina ,s?7m.s", and their use as biological indicators. J.
Fish. Res. Board Can. 26:879-891.
Self, J. T., L. E. Peters, and C. E. Davis.
1963. The egg, miracidium, and adult of Nernatohothrium
texomensis (Trematoda : Digenea). J. Parasitol. 49:731-
736.
355
FISHERY BULLETIN: VOL. 83, NO. 3
Sharp, G. D.
1978. Behavioral and physiolo^cal properties of txinas and
their effects on vulnerability' to fishing gear. In G. D. Sharj)
and A. E. Dizon (editors), The physiological ecology of tunas,
p. 397-449. Acad. Press. N.Y.
SI^fDERMAN^^ C. J.
1961. Parasite tags for marine fish. J. Wildl. Manage. 25:
41-47.
UCHIYAMA, J. H.. AND P. STRUHSAKER
198 1 . Age and growth of skipjack tuna, Katsuivonus pelamus,
and yellowfin tuna, Thunnua albacares, as indicated by daily
growth increments of sagittae. Fish. Bull., U.S. 79:151-162.
Wankowski, J. W. J.
1981. Estimated growth of surface-schooling skipjack tuna,
KntJiuwomis peland,^. and yellowfin tuna, Thunnu,^ (ilhacares,
from the Papua New Guinea region. Fish. Bull., U.S. 79:
517-532.
Watertor, J. L.
1973. Incidence oi Hir%idinella marina Garcin, 1730 (Trema-
toda: Hirudinellidae) in tunas from the Atlantic Ocean. .1.
Parasitol. 59:207-208.
Yamaguti, S.
1970. Digenetic trematodes of Hawaiian fishes. Keigaku
Publ. Co., Tokyo, 436 p.
356
BEHAVIOR OF BOWHEAD WHALES, BALAENA MYSTICETUS,
SUMMERING IN THE BEAUFORT SEA: A DESCRIPTION'
Bernd Wursig,2 Eleanor M. Dorsey,^ Mark A. Fraker,^
Roger S. Payne,^ and W. John Richardson'^
ABSTRACT
Behavior of bowhead whales summerinj^ in the Canadian Beaufort Sea was observed from an airplane and
occasionally from shore during 1980-82, mainly during August. Behavior varied between years. In 1980,
whales alternated periods of socializing with periods of feeding in several different ways: near the bottom (as
evidenced by surfacing with mud), in the water column (suspected during long dives), and skim-feeding at
the surface. In 1981, more time was spent apparently feeding in the water column, with some socializing and
skim feeding. In 1982, almost all activity appeared to be feeding in the water column. In 1980, most whales
studied were in water only 10-40 m deep. In 1981 they were farther from shore and in > 20 m depth, and in
1982 long (10-30 min) dives were common in depths of 40-600 m. Variability in distribution and behavior
presumably was related to availability of prey.
Besides feeding and scx-ializing, we saw sporadic bouts of aerial activity (breaches, tail slaps, etc.) and
log play. During 1981 and 1982 we observed young-of-the-year calves apparently waiting at the surface
while adults fed below. In 1982, two such lone calves played with debris in the water.
During near-surface skim feeding, whales often associated in V-shaped or echelon formations, with up to
14 animals staggered behind and to the side of each other, all moving in the same direction at the same
speed, with mouths wide open. We hypothesize that such coordinated movement may increase the efficiency
of feeding on concentrations of small invertebrates.
In recent years, much has been learned about
behavior of several species of baleen whales (e.g.,
Payne 1983). Most long-term studies of whales have
been carried out during winter, when social inter-
actions, mating, and calving occur more often than
feeding. Recently, however, detailed studies have
been conducted in summer, when whales are pri-
marily feeding (e.g., Dorsey 1983).
This paper describes the general behavior of bow-
head whales, Balaena mysticetus, in the summers of
1980-82. A companion paper gives a quantitative
description of the surfacing, respiration, and dive
patterns (Wursig et al. 1984). This study was done to
provide background data necessary to interpret
observations of bowhead behavior in the presence of
'This paper has been reviewed by the U.S. Minerals Manage-
ment Service (MMS) and approved for publication. Approval does
not signify that the contents necessarily reflect the views and
policies of MMS, nor does mention of trade names or commer-
cial products constitute MMS endorsement or recommendation for
use.
^Moss Landing Marine Laboratories, P.O. Box 450, Moss Land-
ing, CA 95039.
'New York Zoological Society, Weston Road, Lincoln, MA 01773;
present address: Center for Long Term Research, Inc., Weston
Road, Lincoln, MA 01773.
"LGL Ltd., Environmental Research Associates, 22 Fisher
Street, King City, Ontario LOG IKO, Canada; present address:
Sohio Alaska Petroleum Co., Pouch 6-612, Anchorage, AK 99502.
^LGL Ltd., Environmental Research Associates, 22 Fisher
Street, King City, Ontario LOG IKO, Canada.
offshore industrial activities (Richardson et al. in
press).
The Western Arctic population of bowheads
winter in the Bering Sea, and migrate north and east
to the eastern Beaufort Sea in spring. During sum-
mer (late June to early September), most are off
northwestern Canada in Amundsen Gulf and the
eastern part of the Beaufort Sea (Fig. 1). In the com-
mercial whaling era in the 19th century, many bow-
heads apparently summered in the Chukchi and
western Beaufort Seas off Alaska (Townsend 1935),
but bowheads are no longer present in significant
numbers off Alaska in summer (Dahlheim et al.
1980). The eastern Beaufort Sea is believed to be a
major feeding area for bowheads (Fraker and Bock-
stoce 1980), but previous to 1980 there had been no
comprehensive studies of bowheads in that area.
METHODS
Aerial Observations
We observed from a Britten-Norman*^ Islander air-
craft based at Tuktoyaktuk (Fig. 1). The Islander has
two piston engines, high wing configuration, and low
^ Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Manuscript accepted October 1984.
FISHERY BULLETIN; VOL. 83, NO. 3, 1985.
357
FISHERY BULLETIN: VOL. 83, NO. 3
BEAUFORT
SEA ^ /
Tuktoyaktuk
Kugmallit Bay
N.W.T.
100
I30*»
Figure l.-The eastern Beaufort Sea.
Stall speed. An OnTrac VLF/Omega navigation
system indicated the latitude and longitude. A hand-
held color video camera (JVC-CV-0001 in 1980 and
1981, Sony HVC-2000 in 1982) connected to a por-
table video cassette recorder (Sony SLO-340 in 1980
and 1981, Sony SL-2000 in 1982) was used through
the side windows to record oblique views of
bowheads.
Our usual strategy was to search until we encoun-
tered bowheads, and then circle over them as long as
possible while making observations. If contact was
lost, we searched for another group. We created a
fixed reference point about which to circle when
bowheads were below the surface by dropping a
fluorescein dye marker. Near the start of most
periods of circling above whales, a sonobuoy
(AN/SSQ-41B or AN/SSQ-57A) was dropped to
broadcast underwater sounds to the aircraft, where
they were recorded.
In 1980-82, we flew for a total of 340 h during 71
offshore flights. Of this time, we circled over bow-
heads for 97.7 h during 46 flights. Flight duration
was typically 4-5.5 h. Flights were made between 3
and 31 August 1980, 31 July and 8 September 1981,
and 1 and 31 August 1982. We encountered bow-
head whales during every day we flew in 1980, and
during the majority of days in 1981 and 1982.
We usually did not fly when wind speed exceeded
25 km/h; in more severe conditions whales are dif-
ficult to detect and behavior cannot be observed
reliably. While searching for whales, we usually flew
at 457-610 m (1,500-2,000 ft) above sea level (ASL),
358
Wl'KSlCKT Al..; HKHAVIOK OK HI (WIIKAI > VVHAl.KS
and at 185 km/h. While circling over whales, we
reduced speed to 148 km/h. Bowheads rarely ap-
peared to be disturbed by the aircraft when it re-
mained at or above 457 m (Richardson et al. in
press).
The aircraft crew usually consisted of four biol-
ogists and the pilot. Three biologists were seated on
the right side of the aircraft, which circled clockwise
during behavioral observations. Biologists seated in
the right front (copilot's) seat and in the seat directly
behind it described behaviors. These descriptions
were recorded onto audiotape, onto the audio chan-
nel of the video recorder, and, in 1981, directly onto
data sheets by a biologist in the left rear seat. The
biologists in rear seats videotaped whales, handled
sonobuoys, and kept records. All personnel on board
were in constant communication through an inter-
com.
While circling bowheads, we usually were able to
obtain consistent records of 12 variables and types of
behavior:
1) Location of sighting (and, therefore, water
depth);
2) Time of day;
3) Individually distinguishing features, if any, on
whales;
4) Number of individuals visible in area and
number of calves;
5) Headings and turns of each whale in degrees
true;
6) Distances between individuals (estimated in
whale lengths);
7) Length of time at surface, and sometimes
length of dive;
8) Timing and number of respirations or blows,
including underwater blows;
9) Possible indications of feeding: mouth open,
defecation, mud streaming from mouth;
10) Socializing, possible mating, probable nursing
by calves;
11) Aerial activity: breaches, tail slaps, flipper
slaps, lunges, rolls;
12) Type of dive: flukes out, peduncle arch, pre-
dive flex.
Descriptions of these behaviors appear later.
In most parts of this paper we consider only the
observations under "presumably undisturbed" condi-
tions. Bowheads were considered "potentially
disturbed" if our aircraft was at < 457 m ASL, if a
boat was underway within 4 km, or if sonobuoys
showed that industrial noise was readily detectable
in the water. The "presumably undisturbed"
n 1982
^1981
□ 1980
TIME OF DAY (MDT)
Figure 2. - Hourly distribution of behavioral observation time from
the air of bowhead whales.
w 20
LJ
<
'■%
tr
LjJ
>
o
CO
(T
ZD
O
X
10 -
5-
7
6
5
4 ■
3
2 -i
I
0
I I 1982
^1981
□ 1980
0 10 20 30 40 50
1
rrrr.
h=H-
o
200 400
DEPTH (m)
600
Figure 3. - Distribution of behavioral observation time from the air
by depth of water of bowhead whales. The inset shows effort for the
0-50 m range by 10 m intervals.
behavioral observations were distributed by hour of
day and water depth as presented in Figures 2 and 3.
Shore-Based Observations
Shore-based observations were obtained in 1980
and 1981 from the east end of Herschel Island,
Yukon (lat. 69°35'N, long. 138°51'W), and about 225
km west of Tuktoyaktuk (Fig. 1). A surveyor's theo-
dolite was used from a high point (50 m ASL in 1980,
359
FISHERY Bl'LLETIN: VOL. 83. NO. 3
90 m ASL in 1981) on the coast. We used a Wild Tl
theodolite with 6-s accuracy and 30-power optics in
1980, and a Nikon NT-2A with 20-s accuracy and
30-power optics in 1981. Horizontal and vertical
bearings were later translated to x and y map coor-
dinates. This transiting technique, developed by R.
Payne, is described by Wiirsig (1978). The station
was in use from 19 August to 1 September 1980, and
23 August to 13 September 1981.
Locations of most whales within a 10 km radius of
the theodolite station during fair weather and day-
light hours were documented. Unfortunately, whales
rarely approached Herschel Island closer than 5 km
during the 1980 field season, so details of behavior
were difficult to discern. In 1981, fewer whales were
seen, but they were closer to shore, allowing more
detailed behavioral observations.
RESULTS
The Surfacing-Dive Cycle
In the Beaufort Sea in summer, nonmigrating
bowhead whales typically alternate between dives of
variable length, depending on activity, and sur-
facings within which there are several respirations.
This pattern differs slightly from that during migra-
tion, when sounding dives (around 15 min long) are
separated by periods when several brief surfacings,
each with a single respiration, alternate with "series"
dives about 15 s long (Rugh and Cubbage 1980; Car-
roll and Smithhisler 1980). Presumably, migrating
animals dive between respirations to avoid hydro-
dynamic drag imposed by the air-water interface. No
such submergence is necessary for a whale that is
not moving rapidly through the water. However, the
basic repertoire of breathing several times in
relatively, closely spaced series and then not
breathing for many minutes (during the long dive) is
similar during both prolonged directed movement
and more stationary activity. The pattern extends to
some degree even to whales that remain at the sur-
face for long periods (up to 30 min or more during
surface skim feeding, socializing, or play). They
generally breathe several times within a few
minutes, and then cease breathing for a longer time,
despite their near proximity to the surface and the
availability of air. Similar patterns are seen in other
whales, including right whales, Eubalaena glacialvi,
(Kraus et al. 1982) and gray whales, Eschrichtiua
robicstus, (Sumich 1983). Durations of surfacings and
dives, intervals between successive blows, and
number of blows per surfacing are described in Wur-
sig et al. (1984).
Surfacing and Respiring
Whales in water deeper than about 30-45 m usual-
ly surface head and blowhole first after a sounding
dive, with the body oriented at some angle (such as
30°) from horizontal. When whales do not dive very
deeply (as in shallow water), the surfacing is less due
to active swimming upward, and the head and tail
surface at approximately the same time.
A blow is an exhalation of air by a whale. Blows
can occur above or below the surface. Surface blows
are usually visible as a white cloud of water spray,
but may be so weak as to be undetectable. The first
blow after a surfacing usually appears strong, prob-
ably because it is a more forceful exhalation and
because water is present above the blowholes during
or just after surfacing. On calm days and when
whales lie at the surface with the blowholes exposed,
the blowholes are relatively dry, and blows may be
difficult to detect. Blows of calves can also be dif-
ficult to see.
Surface exhalations of gray; humpback, Megaptera
novaeangliae; fin, Balaenoptera physalus; and
southern right whales, Eubalaena australis, are
almost always followed immediately by an inhalation
(B. Wiirsig, pers. obs.). Hence we suspect, following
Scoresby (1820), that exhalations and inhalations
generally occur together in bowhead whales as well.
Diving and Associated Behavior
The predive flex is a distinctive concave bending of
the back seen several seconds before many dives.
The whale flexes its back by about 0.5-1 m, so that
the snout and tail disrupt the surface. Considerable
white water is created at these two points. The whale
then straightens its back and lies momentarily still
before arching the back convexly as it begins its roll
forward and down. The predive flex is seen from low
vantage points as an abrupt lifting of the head,
because the flukes apparently only touch the water
surface from below.
The predive flex was seen more often during 1980
than during 1981 or 1982. Although it occurred
previous to dives well over 50% of the time in 1980,
it occurred in only 8% of the observations (before 29
of 352 dives) in 1981. For 1982, we have especially
detailed analyses of predive flexes. In that year,
predive flexes occurred in presumably undisturbed
noncalves before 32 of 132 dives (24.2%); flexes
occurred more often in late August than earlier
(Table 1). Dives following predive flexes were, on the
average, about twice as long as dives without predive
flexes (19.00 ± SD 7.877 min, n = 13, vs. 10.15 ±
360
WI'KSK; KTAL.: BKIIA\1()K(»F HOWHKAI) whalks
Table 1. — Dives preceded by a predive flex among noncalf
bowheads early and late August 1982. The frequency of
occurrence is significantly highier after 19 August (chi-square
= 4.29, df = 1, 0.025 < P< 0.05).
Up to
19 Aug. 1982
After
19 Aug. 1982
Total
Dives with predive flex
Dives without predive
flex
Total
9
49
58
23
51
74
32
100
132
7.465 min, n = 36; Mann-Whitney U = 97.5, P <
0.01). Five dives were preceded by two predive
flexes, with the flexes separated by a blow. Two
dives were preceded by three flexes. We have no
data on durations of dives following multiple flexes.
During the dive, which can at times be predicted
by the predive flex, the whale makes its body convex
and pitches forward and down. If the angle of sub-
mergence is steep, the tail is usually raised above the
surface; if not, the tail may remain below or just
touch the surface. Rarely do bowheads sink down
without visibly arching the back.
In 1982, 59 of 138 dives (42.8%) were preceded by
raised flukes. Of the 32 dives preceded by one or
more predive flexes, 21 also showed raised flukes.
These two predive behaviors tended to occur
together (x" = 3.94, P < 0.05, df = 1), and dives with
raised flukes were significantly longer than those not
preceded by raised flukes (18.67 ± SD 9.966 min, n
= 12, vs. 10.05 ± 6.956 min, n = 38; Mann-Whitney
U = 114, P< 0.01).
There was no difference in durations of surfacings
concluded with and without raised flukes. However,
surfacings including predive flexes tended to be
longer than those without predive flexes (3.09 + SD
1.038 min, n = 14, vs. 1.79 ± 1.284 min, w = 52; i =
3.50, df = 64, P < 0.001), probably because dura-
tions of surfacings and dives are correlated (Wiirsig
et al. 1984).
The function of the predive flex is unknown.
Flexes occur more often before longer dives (which
may take the whales deeper in the water column).
Raising the flukes before a dive appears related to
the steepness of the dive; whales that roll forward
while dropping the front of the body at least 30°
below the water surface usually raise their flukes.
The weight of the raised tail stock in the air must
help propel the animal downward (much as human
skin divers raise their legs above the surface during
the initiation of a steep dive). Although raised flukes
are common during steep dives in many whales, the
predive flex has not been reported in other spe-
cies.
The Underwater Blow
The underwater blow is a burst of air emitted
underwater. The bubble burst is circular and up to 15
m in diameter when it arrives at the surface. Release
of air underwater was recorded about 10 times via
nearby (< 1 km away) sonobuoys; the noise was
detectable for 3-4 s, but the white water and expand-
ing concentric wave were visible much longer. On
one occasion, we definitely saw that the air came
from the blowhole rather than the mouth, and we
believe that this is always true. We saw underwater
blows immediately after whales dove and just before
they surfaced, but more usually in the middle of the
dive, when the whales were out of sight.
Underwater blows were most frequent in 1980
during periods of pronounced feeding in water < 14
m deep (see Feeding section). In 1980, we saw 158
underwater blows in 30.4 observation hours; in 1981,
57 blows in 30.8 observations hours; and in 1982,
only 6 blows in 36.5 observation hours. (The dif-
ference between years is statistically significant; x^
= 189, df = 2, P < 0.001.) Concurrently, whales
tended to be found in progressively deeper water
from 1980 to 1982.
Underwater blowing occurred more often in the
morning and evening than around solar midday in
both 1980 and 1981 (Fig. 4; solar noon occurs about
1500 MDT in the eastern Beaufort Sea). The midday
"lull" in underwater blowing coincided with a peak in
frequency of socializing, the main nonfeeding
behavior observed (see Social Behavior section
below). Nemoto (1970) suggested that baleen whales
in general show a high level of feeding activity in the
UJ
Q.
CO
o
_l
ffl
UJ
I-
<
UJ
o
q:
3
O
^ 8 H
z
o
i= 6
<
If)
CD
o
. 2
UJ
<
34/3.8
50/7 9
65/11 2
0/0 3
16/154
12/9 3 6^*5
41/9 I
8
12
20
24
TIME OF DAY (MDT)
Figure 4. - Number of underwater bowhead whale blows per aerial
observation hour in relation to time of day, 1980 and 1981 com-
bined. There were few underwater blows in 1982. The numbers at
the top of each column are number of blows seen/number of obser-
vation hours.
361
FISHERY BULLETIN: VOL. 83, NO. 3
morning and a lower level during midday, but we
have no direct evidence of this in bowheads.
Although underwater blows seem to occur more
often in shallow water when whales may be feeding,
we have not included this behavior as a definite part
of feeding. There is only a general similarity to
bursts of bubbles associated with feeding humpback
whales in the North Atlantic (Hain et al. 1982), and
the bubble nets reported for humpbacks by Jurasz
and Jurasz (1979) are very different.
Social Behavior
Behavior was termed social when whales appeared
to be pushing, nudging, or chasing each other, or
when they were within half a body length of one
another. Whales within half a body length almost
always stayed close to each other, and oriented
towards each other or interacted in some manner.
Thus, our use of proximity as an indication of social-
ity was appropriate. Interactions between mothers
and calves, and between whales skim feeding in close
proximity, were not included as social interactions in
this analysis. Whales may, of course, communicate
by sound, and thus may socialize over far greater
distances than those described here. Our sonobuoys
often detected bowhead calls while socializing was
underway. However, we could not verify whether
acoustic communication was occurring between any
particular whales, so we restricted our definition of
socializing to visible behavior. Synchronous diving
and surfacing over areas many kilometers in
diameter (see below) may represent a different form
of social interaction from what we discuss in this sec-
tion. Because groups of whales usually could not be
reidentified positively from one dive to the next, we
treated observations of social behavior at intervals of
> 5 min as independent for the purpose of counting
number of interactions. Conversely, we did not score
social behavior by one group more than once in 5 min
when counting frequency.
Frequency of Socializing
Social behavior was seen less frequently in late
August-early September than in early August, both
in 1980 and 1981 (Table 2). Rugh and Cubbage
(1980) and Carroll and Smithhisler (1980) reported a
higher incidence of social interactions during the
spring migration around Alaska than we saw at any
time. The apparent waning of social activity from
early to late August may be part of a continuing
decrease from a higher level in spring.
Little socializing was observed in 1982. In presum-
ably undisturbed whales, we observed only seven
cases, all on 8, 19, and 23 August. Throughout
August 1982, most whales were alone and making
long dives. The overall socializing rate for each year
(Table 2) demonstrates the dramatic decrease in
socializing in 1982 compared with the two previous
years. This decrease may be related to the increase
in 1982 in the average distance from shore and depth
of water at locations where bowheads were studied.
However, we found no consistent trend for social-
izing to occur more often in shallow water than in
deep water within 1 yr.
There was some indication of hour-to-hour vari-
ation in amount of social activity in all 3 yr (Fig. 5).
In 1980 and 1981, it peaked around 1400-1600 MDT,
the noon period by sun time. In 1982, the few (7)
cases were recorded from 1600 to 2000 MDT, some-
what after solar noon (Fig. 5). In both 1980 and
1981 , there was another peak after 2000 MDT. Why
whales should engage in more social activity around
noon (and possibly in the evening) than at other
times is unknown. However, diel rhythms are well
known in several mammals (e.g., Saayman et al.
1973 for bottlenose dolphins; Matsushita 1955 for
sperm whales; Schevill and Backus 1960 for hump-
back whales). The increased level of socializing
around noon may reflect a lowered level of feeding at
that time, which Nemoto (1970) suggested for baleen
whales in general.
Physical Interactions
During surface interactions with nearby whales,
socializing whales often turned. In contrast, non-
socializing whales often surfaced and dove again
without changing direction. In the 3 yr, turns oc-
Table 2.— Number of social interactions per aerial observation hour, divided
into about 10-d periods, in 1980, 1981, and 1982. Only presumably undisturbed
periods are included.
Year 1-10 Aug. 11-20 Aug. 21-31 Aug. 1-10 Sept.
1980 28/7.0 = 4.0
1981 14/4.3 = 3.3
1982 1/1.5 = 0.7
6/2.9 = 2.1
12/5.5 = 2.2
3/7.6 = 0.4
8/7.7 = 1.0
9/3.3 = 2.7
3/12.8 = 0.2
4/4.0 = 1.0
Overall
42/17.6 = 2.4
39/17.1 = 2.3
7/21.9 = 0.3
362
Wl'KSlCKTAI,.: HKHAVIOKOK HOWUKAD WHALKS
cr
cr
UJ
3
Q.
O
I
(rt
z
z
o
o
H
(-
o
<
<
>
q:
cr
UJ
UJ
H
(r>
Z
ffl
o
_J
_i
<
<
O
cr
o
UJ
(O
<
12 16 20
TIME OF DAY (MDT)
Figure 5. - Number of bowhead whale social interactions per aerial
observation hour in relation to time of day.
curred during 53 of 133 (40%) surfacings with social-
izing, and in 128 of 484 (26%) without sociaHzing (x^
= 9.04; df = 1,P< 0.005).
When bowhead whales touched, they often appear-
ed to push each other. Pushing or touching was
usually done with the head, while oriented head to
head, or head to tail. However, we also saw whales of
adult size dive under the bellies of other whales and
apparently nudge or push the other whales near their
genital areas. At other times, whales dove under
each other at very close range without any indication
that they were touching.
Apparent chase sequences involved two or three
whales in a line, usually < 2 body lengths apart. Dur-
ing these chases one whale often turned abruptly left
or right, and the second (and third) followed. Move-
ment was faster during chases than at all other times
when we saw presumably undisturbed whales at the
surface.
Both touching and chasing may at times represent
low levels of sexual activity, but this is unproven
because we cannot determine the sex of a bowhead
whale from a distance. Payne and Dorsey (1983) and
Tyack and Whitehead (1983) described physically
interacting right and humpback whales, respectively,
which appeared to be engaging in social-sexual
activity.
Possible Mating
In 1981, we twice observed apparent mating. The
more prolonged observation was on 10 August 1981,
within a 25 km- area where there were 20-30 whales
whose main activity was socializing. Two whales
interacted for over 1 h with chases, flipper caresses,
belly-to-belly orientation, rolls toward and away
from each other, head nudges to the genital area and
to the rest of the body, tail slaps, and flipper slaps.
One whale, a recognizable animal that we termed
"Whitespot", was about 1-2 m longer than the other
("B") and was the more aggressive. Although B
originally nudged the genital area of Whitespot, it
was Whitespot who appeared to initiate flipper
caressing and rolls toward B. The two whales rolled
their ventral surfaces together for about 5 s, but B
then rolled its ventrum in the air in an apparent
attempt to avoid ventral contact with the larger
animal. As it rolled away from Whitespot, B
defecated, and when Whitespot moved its head
toward the genital area of B, B defecated two more
times in rapid succession. B then dove away from
Whitespot, and Whitespot followed it at the surface
in an apparent chase. Whitespot then stopped and,
alone at the surface, rolled two times and tail slapped
while on its back. It then dove, and the two appeared
together again at the surface 4 min later, with no fur-
ther energetic surface interaction.
We do not know the sex of either animal, but it ap-
peared that Whitespot was attempting to copulate
with the reluctant animal. Some of us (Wiirsig and
Payne) have observed southern right whale females
frequently roll their ventra away from aggressive
males, leaving their genital areas above the surface
of the water, where the males cannot reach them.
Everitt and Krogman (1979) photographed very
similar behavior of a group of six bowheads off Bar-
row, AK, in May. Our observations here were highly
reminiscent of such behavior. Although adult
females are slightly larger than adult males in both
right and bowhead whales, we commonly see large
southern right whale males in pursuit of smaller
females, which attempt to avoid the males.
On 25 August 1981, two bowheads briefly placed
their ventral surfaces together and clasped each
other with their flippers. After 1 min, they rolled
apart, blew, and dove slowly as a third whale ap-
proached. The mutual rolling and leisurely diving
indicated that, if this was copulatory behavior, it was
mutually undertaken by the two whales in contrast
to the previous example.
Group Structure and Stability
Two observations of recognizable bowheads pro-
vided evidence about group structure and stability.
We observed a distinctively marked pair of adults,
one accompanied by a calf, at about lat. 70°10'N,
long. 133°50'W on 7 August 1980. We saw a similar-
363
FISHERY BULLETIN: VOL. 88. NO. 3
ly marked group of two adults and a caLf, almost cer-
tainly the same whales, on 20 August at lat. 70°07'N,
long. 131°30'W, which is about 85 km from the place
they had been seen 2 wk earlier. This observation
suggests that some groups of bowheads are main-
tained for at least a few weeks. The observation also
suggests that females with calves may sometimes be
accompanied by escorts, as has been observed for
wintering humpback whales (Herman and Antinoja
1977).
Feeding
Feeding appeared to occupy much of the time of
the bowheads that we observed, but we had to rely
on indirect clues, such as observations of swimming
with open mouth, mud streaming from the mouth, or
presence of feces in the water, to indicate that
feeding had taken place. The four possible types of
feeding behavior that we identified were 1) water-
column feeding; 2) near-bottom feeding; 3) skim
feeding; and 4) mud tracking. Of these, the first
three rather clearly represented feeding, whereas
the function of the last was less certain. As noted
above, underwater blowing showed some association
with feeding, but the connection was uncertain.
In 1980, certain feeding behaviors occurred in par-
ticular areas: only water-column feeding was seen
near the Issungnak artificial island site (Fig. 1),
whereas only skim-feeding was seen off the Tukto-
yaktuk Peninsula near McKinley Bay. In 1981, there
was less evidence for feeding, although we suspect
that most feeding occurred in the water column. In
1982, when whales dove for long periods (up to 30
min), we su.spected water-column feeding to be
occurring at almost all times.
Water-Column Feeding
Water-column feeding could not be observed
directly. Whales were scored as feeding in the water
column when they dove for long periods, and when,
between long dives, there was much defecation and
only slow forward motion. Defecation is simply an in-
dication of prior feeding. However, particular
behaviors such as a series of long dives usually con-
tinued for many hours, so occurrence of defecations
between long dives was considered indicative of on-
going feeding in the water column.
The frequency of apparent water-column feeding
was not constant. In 1980, we saw bowheads water-
column feeding from 3 to 22 August. Thereafter, few
whales were present in the area where we had ob-
served this behavior, and whales seen elsewhere did
not seem to feed in the water column. In 1981, when
we saw less defecation, we only scored as water-
column feeding some adult whales that dove for pro-
longed periods on 24 August, while calves remained
at the surface. In 1982, most whales made long
dives. These whales probably were feeding in the
water column, even though we saw little defecation
at the surface. Feeding below the surface may have
occurred during many other dives besides those that
we classified as dives with water-column feeding.
Observations on 3 August 1980 typify water-
column feeding behavior. On this date, bowheads
were north of Kugmallit Bay where water depth was
18-38 m. The surface water was turbid, brackish
water from the Mackenzie River, but beneath this
surface layer, there was a second layer of clearer,
saline Beaufort Sea water (Griffiths and Buchanan'^).
The whales occurred in groups of 2-10 animals, and
occasionally as individuals without others nearby.
Group members showed a high degree of synchrony,
often surfacing very close together and remaining
close at least until they dived again. Not only did the
members of a group surface and dive synchronously,
but various groups spread over an area several
kilometers in diameter all tended to be at the surface
or beneath it at the same time.
While the animals were at the surface, they moved
slowly forward while taking a series of breaths. As
each individual dived, it raised its tail clear of the
water, and disappeared from view in the turbid
water. Thus, these dives must have taken the whales
well below the surface. When the whales were at the
surface, they often disturbed the turbid surface
layer, exposing dark patches of seawater from
deeper depths. However, while submerged after a
dive that was preceded by raised flukes, they did not
affect the thin surface layer, indicating that they
were probably feeding in the underlying clearer
ocean water. Defecation was frequent, suggesting
that feeding may have taken place recently. The
feces clouds were red-orange.
Bottom Feeding
On 12 August 1980, we noticed clouds of mud
suspended in the water about 25 km west of Issung-
'Griffiths, W. B., and R. A. Bachanan. 1982. Characteristics
of bowhead feeding areas. In W. .1. Richardson (editor), Behavior,
disturbance responses and feeding of bowhead whales Balaena
myst}cetu.s in the Beaufort Sea. 1980-81, p. 347-455. Unpubl. Rep.,
456 p. LGL Ecological Research Associates, Inc. Bryan.
TX. for Bureau of Land Management, U.S. Department of the In-
terior, Washington, DC. Available from Minerals Management
Service Alaska DCS Region, P.O. Box 101159, Anchorage, AK
99510.
364
WCKSK; KTAl..; KKllAVIOKOF HOWUKAD WllALKS
nak artificial island (Fig. 1). The clouds represented
suspended mud and not plankton because the
material was of the same color as mud dredged up by
industrial activities. Whales surfaced with large
amounts of muddy water streaming from their
mouths, indicating they had been feeding from or
near the bottom. This behavior occurred in 24-29 m
of water and seemed very localized. We saw no in-
dication of bottom feeding in the same area on 22
August 1980, but we had observed similar mud
clouds nearby on 9 August, when prolonged observa-
tions were not possible. On 25 August 1981, whales
again surfaced with mud streaming from their
mouths. The location was 15 km south of the position
where we observed such behavior in 1980; water
depth was only 10-13 m.
These are, to our knowledge, the first published
behavioral observations of apparent near-bottom
feeding by bowhead whales. However, Johnson et al.
(1966), Durham (1972), and Lowry and Burns (1980)
detected pebbles and bottom-dwelling species in
bowhead stomachs.
Bottom-feeding whales were usually separated
from other whales by 150-300 m when at the surface.
On 12 August 1980, at least 10 whales were bottom
feeding within an area of 3 km radius. Whether they
were feeding on inbenthic or epibenthic inverte-
brates we do not know. In the eastern Beaufort Sea,
the average biomass of inbenthic animals greatly ex-
ceeds that of epibenthic animals (Griffiths and
Buchanan footnote 7). However, the latter may
occur in dense swarms in certain places. For a balae-
nid whale, such swarms would seem to be a much
more suitable type of food than inbenthic organisms.
Mud might be taken inadvertently along with epi-
benthic animals.
Skim Feeding
The only feeding type that we observed directly
was skim feeding. In the third week of August 1980,
we observed whales moving slowly and deliberately
at the surface with their mouths open wide. Usually
the rostrum just broke the surface of the water, and
was parallel to it. In these cases, the lower jaw was
dropped to varying degrees, as could be seen from
the depth of the white chin patch. In 1980, skim
feeding was observed along the Tuktoyaktuk Penin-
sula in water 12-22 m deep. Whales occasionally
skim fed alone, but more often did so in groups of
2-10 or more individuals. During any one observation
period, they stayed in the same general area by
repeatedly turning and did not appear to make any
net geographic movement. However, we found
groups of skim-feeding whales in different locations
on different days.
During 1981 , we witnessed skim feeding on a large
scale only on the evening of 18 August, 32 km NNW
of Pullen Island in water 25 m deep. About 20-30
whales in the 25 km^ area were swimming with
mouths open; they travelled slowly, usually just
below the surface (~ 2-3 m deep). Copepods were
unusually abundant in near-surface waters at this
location and time (Griffiths and Buchanan footnote
7). On 23 and 24 August 1981, we saw one isolated
example on each day of a whale feeding at the sur-
face briefly (observed for < 1 min) in approximately
the same area as on 18 August.
Typically, skim-feeding whales were oriented with
their backs at the water's surface. However, they
occasionally swam on their sides with mouths open at
an angle of about 60°, and once we saw two whales
separated by three body widths swimming on their
sides, belly to back. In one instance, a skim-feeding
whale swam inverted for at least 3 min, with the
underside of its chin at the surface.
Frequently, the skim-feeding whales swam in
echelon formation, each whale swimming just behind
the preceding whale, but offset laterally by one-half
to three body widths, reminiscent of geese in V for-
mation (Fig. 6). At other times, they swam abreast
and parallel to one another. Videotape from 18
August 1981 showed that whales within the echelons
were a mean of 0.53 whale lengths apart (SD =
0.599, n = 66), or about 8 m. These distances were
measured from different echelons or from the same
echelon at intervals of at least 5 min. We videotaped
a recognizable whale for almost 3 h on this day as it
skim fed in changing echelon formations, usually
taking the lead position. Echelons were clearly
dynamic in terms of membership, size, and organiza-
tion. In 1981, the mean echelon size was 4.7 animals
(SD = 4.05, n = 23). While the largest such forma-
tion observed in 1980 contained 5 individuals, the
largest in 1981 contained 14 animals.
We suspect that echelon feeding increases the
feeding efficiency of those animals staggered behind
and to the side of other individuals, perhaps by help-
ing them to catch prey that escape or spill from the
mouth of the whale in front, or by reducing the abili-
ty of prey to escape to the side. Skim feeding in eche-
lon may allow more effective exploitation of concen-
trated patches of small prey than would be possible if
whales were feeding alone. If so, the change in effi-
ciency that accrues when echelons are formed may
have an important cost/benefit effect on energy ex-
pended per whale. The predominant prey types of
bowheads include copepods and euphausiids (Lowry
365
FISHERY BULLETIN: VOL. «3, NO. S
Flcn'REK.-Fivebowhead whales skim feeding in echelon formation. Drawing after a 35 mm photograph and video footage from the air.
and Burns 1980). The latter are adept at avoiding
most sampling gear because of their rapid move-
ment. However, bowheads at times collect euphau-
siids in very large numbers, despite the bowhead's
slow swimming speeds relative to the better known
euphausiid predators such as rorquals. Perhaps
echelon feeding is especially helpful in catching fast-
swimming prey such as euphausiids.
During 1982, little direct evidence for feeding was
noted. We saw no skim feeding at the surface, and
noticed only nine isolated instances when a whale's
mouth appeared to be open slightly. These brief, slight
366
WI'KSK; KT A1..: HKIl.WKiKOF HOVVMKAlt WIIAI.KS
openings of the mouth contrasted sharjaly with the
sustained large gajjes observed in 1980 and 1981, and
probably did not represent feeding. In southern right
whales, Payne (pers. obs.) has observed mouth open-
ing that he interprets as yawning following sleep.
Mud Tracking
Mud tracking occurred when whales swimming in
shallow water (< 12 m depth) disturbed the bottom
sediments with each fluke beat, producing clouds of
mud joined by a narrower trail of muddy water.
These elongated clouds of mud were different from
mud clouds produced during presumed bottom feed-
ing. Although we often could not see the whales, in
at least a few instances their mouths were open. We
saw mud tracking during only three flights in the
third week of August 1980.
Mud tracking probably represented incidental
disturbance of bottom sediments by a whale feeding
near the bottom in shallow water. We saw no
evidence that bowheads ever turned and swam back
along a mud track made previously. The mud tracks
tended to be straight, and some extended for well
over 1 km. At certain times, clouds of mud streamed
from the whale's body as it swam near the surface. In
this case, we suspect that the whales had contacted
the bottom, and that the mud had stuck to their
bodies. Sometimes, mud-tracking whales exhaled
while submerged, producing a characteristic burst of
bubbles (see section on The Underwater Blow).
Defecation
Defecation usually was evident as a cloud (2-3 m
diameter) of red-orange feces near the surface.
Whales almost invariably were moving forward or
diving when they defecated, and over 50% of the
bowheads observed defecating in 1980 did so while
the tail was arched up high out of the water just
before the dive. The anus was thus close to or at the
surface. No part of the body appeared to touch the
feces cloud, which was visible at the surface for up to
10 min. When whales moved forward while defecat-
ing, the feces were more dispersed and disappeared
within 1-2 min. Brown (1868) noted that feces of
eastern arctic bowheads were also red. Renaud and
Davis* observed red clouds of feces off the Tuktoyak-
tuk Peninsula in 1980.
Defecation was seen more often in 1980 (23 cases
during 30.4 h over whales) than in 1981 (11 cases
during 30.8 h over whales). The difference is statis-
tically significant (x^ = 4.39, df = 1, 0.025 <P <
0.05), and may be related to year-to-year differences
in feeding patterns. In 1982, we saw only one defec-
ation (by a lone whale playing with a log). Because
we can only observe defecations by whales at the sur-
face, we compared the rates in reference to the num-
ber of whale-hours of observation at the surface. In
1980, there were 2.29 defecations/whale-hour at the
surface, as opposed to 0.73 in 1981, and 0.09 in 1982
(X^ = 27.58, df = 2, P < 0.001). This decrease could
result either from decreased defecation (indicative of
less feeding), or from an increasing tendency to
defecate under the surface where we could not ob-
serve it. During 1982, dives were longer than in the
2 previous years (Wiirsig et al. 1984), and we suspect
that much water-column feeding was taking place.
Adult-Calf Pairs
Calves of the year are a light tan color, distinct
from the dark black of noncalf bowheads. An adult
that remained close to a calf was assumed to be the
calf s mother. For the closely related southern right
whale in winter, Payne and Dorsey (1983) found that
in unambiguous adult-calf pairs, the adult was always
a female, and that identified calves were always seen
with the same individually identified female. At
times, we saw apparent nursing as calves submerged
briefly, oriented toward the teat region of the adult.
In 1982, we made longer observations of calves than
in either 1980 or 1981.
The relative lengths of six calves measured from
videotape sequences recorded during August 1981
were a mean of 0.57 ± SD 0.052 adult body lengths.
Many of the calves we observed in August 1982 ap-
peared to be smaller, about one-third adult size. This
is corroborated by the fact that 14 calves measured
via photogrammetry in August-early September
1982 were 4.1-7.6 m long, or 33-45% (mean 41%) of
the length of the accompanying adult (Davis et al.^).
It may be that births occurred earlier in the year in
1981 than in 1982, or that the females videotaped in
1981 were smaller, on average, than those measured
in 1982.
* Renaud, W. E., and R. A. Davis. 1981. Aerial surveys of bow-
head whales and other marine mammals off the Tuktoyaktuk Penin-
sula, N.W.T., August-September 1980. Unpubl. Rep., 55 p. LGL
Ltd., Toronto, for Dome Petroleum Ltd., Box 200, Calgary, Alberta
T2P 2H8, Canada.
sDavis, R. A., W. R. Koski, and G. W. Miller. 1983. Prelim-
inary assessment of the length- frequency distribution and gross an-
nual reproductive rate of the western arctic bowhead whale as
determined with low-level aerial photography, with comments on
life history. Unpubl. Rep., 91 p. LGL Ltd., ToronU), for National
Marine Mammal Laboratorv, National Marine Fisheries Service,
NOAA, 7600 Sand Point Way N.E., BIN C15700, Seattle, WA
98115.
367
FISHERY BULLETIN: VOL. 83, NO. 8
When an adult and calf were both at the surface,
they were usually within one adult-length of each
other. Videotape sequences showed the mean
distance apart to be 0.61 adult whale lengths (SD =
0.564, n = 8, range = 0.1-1.5), or about 9 m. The
calves spent most of the time lying beside the adult,
and facing in the same direction as the adult. At
times, the calf strayed up to two whale lengths from
the adult, and then oriented toward the adult. While
the adult lay at the surface, the calf often submerged
near the belly of the adult with its tail close to the
adult's tail. This position is probably indicative of
nursing. The calf then often swam under the adult,
surfaced on the other side, respired one or two times,
and submerged again toward the adult's belly, alter-
nating sides with each surfacing. The calf also ap-
peared at times to rest, lying quietly on the back and
tail of the adult.
Calves were sighted at similar frequencies in all 3
yr (Table 3). However, durations of surfacings by
calves were longer in 1982 than in 1980-81. Because
of this, calves accounted for 15% of whale-hours of
observation in 1982, but only 3% in 1981, and 4% in
1980 (Table 3).
Calves Alone
In 1982, calves spent almost 40% of their time at
the surface unaccompanied by an adult. This was
comparable with their behavior in 1981, but unlike
1980 when they were rarely seen alone. (Table 3).
On 24 August 1981, we saw three calves separated
from each other and from the closest adults by 100 m
to more than 300 m. It was, therefore, often not
possible to assign calves to particular females. The
nearest adults spent much time submerged, but the
calves remained stationary at the surface. At one
point, we videotaped an adult that surfaced 4.9 adult
lengths from a calf lying stationary at the surface.
During another videotaped sequence, an adult-calf
pair, 0.2 lengths apart, was separated from a lone
calf by 7.6 adult lengths. We suspect that the adults
were feeding in the water column while calves
waited at the surface.
In 1982, we observed four lone calves at the sur-
face, on 18, 19, and 23 August, and on three of these
occasions we saw the calf rejoin its presumed
mother. On 18 August, a lone calf surfaced and
oriented straight toward an adult at a distance of 1 .6
km. When it came within 75 m of the adult, the adult
also began to swim rapidly toward the calf. During a
second incident on the same day, a calf and adult
swam rapidly toward each other from at least 300 m
distance. In both cases, the two dove simultaneously
after coming together. On 23 August 1982, an adult
surfaced 180 m from a lone calf, and the adult
oriented toward the calf. When the two whales were
~ 120 m apart, the calf also oriented toward the
adult, but the adult was mainly responsible for clos-
ing the distance between them, as it swam at
medium speed toward the calf. When the two whales
were ^ 20 m apart, the calf dove and reappeared 18
s later, reoriented by 180°, lying to the right of the
adult, and facing in its direction. The calf then
Table 3. — Calf sightings and observation time in 1980, 1981, and
1982. Only flights with behavioral observations are considered,
and both presumably undisturbed and potentially disturbed
periods are included. The number of sightings of calves is an
approximate count because multiple counts of the same calf
were possible in cases where the calf and its mother were not in-
dividually recognizable.
1980
1981
1982
No. sightings of calves
12
16
16
No. flights
14
18
14
Calf sightings/flight
0.86
0.89
1.14
Hours in plane over whales
30.4 h
30.8 h
36.5 h
Calf sightings/hour
0.39
0.52
0.44
Calf time at surface with
mother
20.4 min
17.5 min
63.1 min
Calf time at surface alone
1.6 min
12.7 min
38.2 min
Total calf time at surface
22.0 min
30.2 min
101.3 min
% of calf surface time
alone
7.3%
42.1%
37.7%
Whale-hours of observation
at surface
10.03 h
14.98 h
10.95 h
Calf-hours of observation/
whale-hour of observation
0.037
0.034
0.154
Calf time at surface/
sighting
1.57 min
1.89 min
6.33 min
368
WflRSICKTAL.: BFHAVIOK OK HOWUKAH WIIAI.KS
submerged several more times toward the belly of
the adult, probably nursing.
Our observations of adults and calves orienting ac-
curately toward one another at distances up to 1.6
km apart suggest that there was acoustic communi-
cation between the two. There is possible evidence
for this from the incident on 23 August 1982. The
rate of low-frequency tonal frequency-modulated
calls, which we suspect to be long-distance contact
calls, increased while the mother and calf were swim-
ming toward each other from some distance apart,
and then ceased altogether once the two whales were
joined. Several unusual higher pitched calls of
undetermined origin were also recorded by a
sonobuoy near the calf while the two whales were
separated.
Nursing
When the lone calf of 23 August 1982 joined its
mother after a separation of at least 71 min, we
observed the longest probable nursing bout seen dur-
ing the study. As the two animals approached each
other head on, the calf dove out of sight for the first
apparent nursing dive when they were still about 22
m apart. The calf dove toward the teat region of the
adult six times in all, with submergences lasting 18,
11, 27, 17, 12, and 10 s (mean = 15.8 ± SD 6.37 s).
These brief dives were separated by brief surfacings
lasting 6, 6, 9, 11, 23, and 17 s (mean = 12.0 ± SD
6.75 s). Each surfacing included a single respiration.
Nursing ended as the calf and adult dove out of sight
at the same time. Although there was no apparent
progression in the durations of the calf's nursing
dives over the entire nursing bout, surfacings tended
to lengthen, suggesting an appeasement of the calf 's
eagerness to nurse. The duration of the probable nur-
sing bout from the start of the first nursing dive to
the start of the deep dive by both mother and calf
was 2.78 min.
The other bouts of probable nursing were shorter,
sometimes < 1 min, and involved adult-calf pairs that
had not recently been separated, as far as we knew.
Usually, all that we could see was one or two short
dives by the calf toward the teat region of the mother
at the end of a surfacing sequence, followed imme-
diately by a dive by both animals.
Other Behaviors
Aerial Activity
or a pectoral flipper onto the water. During
breaches, 50-60% of the body length left the water.
The whale emerged head first at a small angle from
the vertical, usually with the ventrum down. It then
twisted and fell back onto the water on its side or
back. Forward lunges differed from breaches in that
the body came out of the water at a shallower angle
and did not twist; the whale reentered belly first. The
forward lunge had a larger forward component than
did the breach.
Breaches, tail slaps, and flipper slaps sometimes
occurred in bouts. Within bouts, intervals between
successive breaches were generally greater than
those between tail or flipper slaps. For example,
breaches, tail slaps, and flipper slaps by one whale
that engaged in all three behaviors on 6 August 1980
were at average intervals of 46, 8, and 4 s, respec-
tively.
The incidence of aerial activity was comparable in
the 3 yr (0.60, 0.93, and 0.82 bouts/whale-hour in
1980, 1981, and 1982), but much lower than
reported for spring migration. Rugh and Cubbage
(1980) saw breaching by 23% of all bowheads {n =
280) observed passing Cape Lisburne, AK, in spring.
Play
Although many social interactions may involve
play, we could not distinguish low levels of mating
activity or aggression from play. We scored play
behavior only when whales spent some time at the
surface associating with an object other than a con-
specific. We saw no such behavior in 1980, but
several incidents in 1981 and 1982. Few such inter-
actions have been described for other baleen whales.
LOG PLAY. -We witnessed whales playing with
logs in the water on two occasions in 1981, and once
in 1982. Log play, which consisted of a whale
nudging, pushing, or lifting a log, lasted 5 s, 10 min,
and at least 1.5 h during these three observations. In
1981, other researchers saw bowheads playing with
logs twice in the same general area as our 1981
observations (C. R. Evans and J. Hickieio). During
two of our three observations the water was en-
sonified by noise pulses from distant seismic explor-
ation (Richardson et al. in press). However, there
was no proof of a connection between log play and
seismic noise.
Some elements of log play by bowheads were
similar to play with seaweed observed in southern
Bowhead whales sometimes leaped or breached
from the water, forward lunged, or slapped the tail
>oC. R. Evans, Biologist, and J. Hickie, Biologist, LGL Ltd., En-
vironmental Research Associates, 22 Fisher St., King Citj-, Ontario
LOG IKO, Canada, pers. commun. September 198L
369
FISHERY BULLETIN: VOL. 83. NO. 3
right whales (Payne 1972). Both involved lifting the
object with the head, moving the object along the
back, and patting it with the flippers. Two log-play-
ing bowheads attempted to push the log under water
with the head. This action was reminiscent of a
motion commonly made by male right whales when
attempting to mate with uncooperative females
(Payne, pers. obs.).
CALF PLAY. -On two occasions in 1982, lone
calves at the surface interacted with debris in the
water, and the actions had the appearance of play.
The first incident occurred over 12.3 min on 19
August 1982, when a lone young-of-the-year calf
followed a line of surface debris ■^ 2 m wide, prob-
ably composed mainly of invertebrates. The calf
stayed at or just below the surface and oriented
directly along the windrow, changing course as the
line meandered left or right. Although the calf ap-
peared to have its mouth open slightly for brief
periods, it did not appear to feed extensively, if at all.
However, its movements thoroughly disrupted and
dispersed the line of debris. The movements were
rapid and jerky, reminiscent of any uncoordinated
young mammal. The calf lunged forward while in the
debris on three occasions, and slapped its tail onto
the water surface twice. For -^ 30 s, it moved rapidly
along the line, ventrum up, with rapid up-and-down
movements of the tail for the entire time. The se-
quence ended when the calf dove out of sight at the
end of the windrow; we did not see it with an adult.
Although the incident did not seem to represent con-
certed feeding, this "play" by the calf may have been
practice in skills required for feeding.
A second incident of "calf play" occurred on 23
August 1982. This calf was first encountered hang-
ing quietly just below the surface, or moving forward
very slowly. During slow movement, it entered an
area marked by dispersed fluorescein dye from one
of our dye markers (see section on Methods). The dye
covered an area about 40 m by 100 m. Immediately
upon entering the area of bright green water, the
calf became active. During the 22.3 min of associa-
tion with the dye, the calf rolled ventrum up eight
times for 5-20 s each time, and moved back and forth
within, and to the edge of, the dye-clear water inter-
face. Although not as active and not beating its tail
as fast as the calf in the windrow, this calf made
abrupt turns of > 90° on 25 occasions during its stay
in the dye, reorienting itself at the dye's edge in
order to remain within the dye. The calf ultimately
moved out of the dye and oriented toward an ap-
proaching adult. When the two joined, the calf ap-
parently began nursing.
Synchrony of Activity and Orientations
There was often an impressive degree of syn-
chrony of basic behaviors among members of quite
widely spaced groups. We observed apparent syn-
chronization of behaviors on time scales ranging
from seconds to days.
Synchrony in General Activity
During 1980, we found that all or most bowheads
in various areas did the same thing for up to several
days. Some days later, the whales had usually
moved, and whales were then found elsewhere
engaged in different activities. For example, on 3
and 5 August 1980, whales north and east of Issung-
nak artificial island were mainly engaged in water-
column feeding, with frequent defecation. By 6 and 7
August, whales in this area shifted to more surface-
active behavior, interacting in groups with pushes
and apparent chases. We saw little defecation at this
time. On 12 August, at least 15 animals about 30-40
km west of this area were all apparently bottom
feeding.
Whales were encountered in two additional areas
in 1980: east of Pullen Island (19 and 20 August) and
just west of McKinley Bay (19-22 August). In the
Pullen Island area, all whales were mud tracking as
described above. In the second area, mud also was
evident, but there was much less underwater blow-
ing. Some animals had mouths open at the surface.
On 22 and 23 August 1980 almost all whales we en-
countered were skim feeding in groups of 10-30
animals north of McKinley Bay. However, in the
Issungnak area farther west, substantial numbers of
whales were still water-column feeding. On 27, 29,
and 31 August 1980, whales interacted in small
groups of 2-5 individuals. Some small groups oriented
SSW, perhaps indicating the beginning of migration.
In summary, during 1980 (but not 1981 or 1982)
we found that whales in various areas did much the
same thing for up to '^ 5 d, but then shifted location,
activity, or both. A partial explanation for the syn-
chrony of behavior seen in 1980 may be that whales
moved to exploit new food resources, and that the
most appropriate feeding mode changed according to
site-specific conditions. In the subsequent 2 yr, it ap-
peared that whales were doing more water-column
feeding in deeper water, perhaps because of a more
consistent food supply.
Synchrony in Dives and Surfacings
We sometimes had the impression that all whales
370
WfKSIC, ETAL.: BKHA\I()K()K HOWllKAD WHALKS
in an area were synchronizing? their surfacin^s and
dives. Many were too far apart to be in visual con-
tact. Ljungblad et al (1980) also reported synchrony
among whales engaged in water-column feeding ~75
km east of Kaktovik, AK. They reported that
"... whales were observed on the surface almost at
regular intervals and gave the impression of resting
between dives; then, suddenly, no whales would be
seen in any quadrant for several minutes."
Although synchrony in surfacings by animals far
apart suggests acoustic contact between animals, it
is not proof of communication over that distance.
The synchrony could be established through indepen-
dent responses to common external cues. It could
also occur if the animals were close together and
visually synchronized before observations began; the
observed synchrony would then be a residual
phenomenon that persisted because of whales diving
and surfacing for similar lengths of time. None of
these possible explanations -acoustic communica-
tion, common external cues, or residual phenomenon
- can be either proven or discounted at this time.
Synchrony in Orientations
Analysis of orientations provides additional
evidence that widely separated whales at times syn-
chronize their behavior during summer. Our best
data were from three flights in 1980 when we flew in
a straight line. At these times, we counted each in-
dividual only once. Rayleigh and x^ tests (Batschelet
1972) show that whale orientations were significant-
ly nonrandom (Table 4).
For flights when we circled to make detailed
behavioral observations, we analyzed orientations
using the first heading noted for each surfacing of a
whale. Because we were making repeated observa-
tions on the same animal in some cases, any consis-
tency in orientations during those flights is attrib-
utable in part to different whales, and in part to
subsequent surfacings of the same whale. In 1980
and 1981, the whales were oriented nonrandomly
during 7 of the 11 flights with enough data for
analysis (Table 4). The headings changed from day to
day, however, and bore no apparent relationship to
the general behavior of the whales. In 1982, no signi-
ficant departures from uniformity were found during
any of the five flights with sufficient data for
analysis.
The headings on the latest day with observations
in 1980 and 1981 usually were not in the direction to
be expected at the beginning of the westward migra-
tion. On 31 August 1980, most bowheads observed
while we circled north of the Tuktoyaktuk Peninsula
were oriented north, east, or south (mean 121 °T
(true). Table 4). However, later that day on a direct
flight, we found other bowheads to be oriented
toward the south (mean 189° T). In this same general
area, Renaud and Davis (footnote 9) also recorded a
slight eastward tendency for bowheads seen on
21-24 August 1980, but a significant southwestward
tendency (236 °T) on 3-4 September 1980. On 8
September 1981, most whales west of Herschel
Island were oriented toward the northeast (62 °T),
again not the direction to be expected at the begin-
ning of westward migration. These results support
our impression that most of the whales we observed
were not migrating.
Table 4— Bowhead orientations, judged relative to true north from the air, 1980-81. Only during the direct flights was each
observation known to represent different animals. During the circling flights, each whale was scored an unknown number of
times (but only once per surfacing).
Vector
Chi-square
No. of
animals
with these orientations
mean
direction
Rayleigh
test
test
Date
N
NE
E
SE
S
sw
W
NW
Total
P
Direct flights
11 Aug 1980
16
1
3
0
5
2
10
6
43
321°
<0.001
<0.001
12 Aug. 1980
7
5
16
5
7
6
9
2
57
bimodal
n.s.
<0.025
31 Aug. 1980
1
1
1
3
8
8
0
1
23
189°
<0.001
7
Circling flights
31 Aug. 1980
4
4
6
3
11
1
0
2
31
121°
<0.05
10 Aug. 1981
0
3
0
2
0
4
0
1
10
—
n.s.
10 Aug. 1981
3
1
7
2
1
6
0
1
21
bimodal
n.s.
13 Aug. 1981
12
9
11
1
1
0
1
1
36
43°
«0.001
18 Aug. 1981
2
5
10
5
6
1
2
1
32
111°
<0.001
18 Aug. 1981
3
0
0
0
0
1
6
0
10
289°
<0.005
23 Aug. 1981
0
4
1
1
0
0
0
0
6
62°
<0.02
24 Aug. 1981
1
0
3
2
5
8
10
5
34
243°
<0.001
6 Sept. 1981
1
7
2
1
0
2
3
3
19
—
n.s.
7 Sept. 1981
2
5
1
1
0
2
2
3
16
—
n.s.
8 Sept. 1981
1
8
3
1
1
0
0
0
14
62°
<0.001
'/ means cell sizes too small for a chl-square test.
371
FISHERY BULLETIN: VOL. Ki. NO. :i
We do not know whether consistent orientations
represented a type of social synchrony, or whether
the whales independently reacted to environmental
stimuli (such as currents or wave orientations).
Norris et al. (1983) and Braham et al. (1984)
reported gray and bowhead whales, respectively,
that may have been feeding by stationing themselves
against a current. Shane (1980) has reported a
similar stationing against the current for bottlenose
dolphins in Texas. Gray whales in lagoons have been
observed to move in the same direction as the tidal
current (Norris et al. 1977), but in that case move-
ment may have been related to avoiding shallow
water as the tide receded.
Miscellaneous Observations
Speed of Travel
In 1980 and 1981, some data were gathered on
bowheads visible from Herschel Island. The whales
were usually > 3 km from shore, and detailed
behavioral observations were infrequent. However,
speed was sometimes measurable with a surveyor's
theodolite. Whales rarely changed direction within
any one 30 s period, so we calculated speeds from
theodolite readings taken within 30 s of each other.
This criterion was changed to 60 s for 30 August
1981 , when a whale was followed at the surface for a
long period, and changed direction relatively little.
For 1980, average speed was 5.1 km/h(w = 18, SD
= 2.93) at the surface, and 4.3 knVh {n = 4, SD =
0.79) below the surface. The 1980 speeds are com-
parable with the most reliable estimates derived by
Braham et al. (1979) and Rugh and Cubbage (1980)
for migrating bowheads: 4.8-5.9 km/h and 4.7 ± SD
0.6 km/h, respectively. However, based on additional
data, Braham et al. (1980) estimated the mean speed
at Point Barrow in spring to be 3.1 ± SD 2.7 km/h.
Speeds during active migration along the coast of
Baffin Island in fall were 5.0 ± SD 1.3 km/h (n = 22)
based on theodolite observations from a cliff (Koski
and Davis'').
On 30 August 1981, an adult whale traveling east
was observed continuously for 1.52 h. Its behavior
was unusual- it did not submerge during the entire
time. Its mean speed was 2.3 ± SD 1.26 km/h, con-
siderably slower than the speeds mentioned above.
Its mean blow interval was 10.0 ± SD 13.55 s (n =
420), significantly lower than the mean for all other
undisturbed whales observed from Herschel Island
(14.6 ± 9.56; n = 60; t = 2.54, P < 0.02).
On 8 September 1981, a mother-calf pair was
observed by theodolite for 1.8 h. The average speed
of the calf was 8.9 ± SD 5.57 km/h (n = 28). During
this rapid movement, the calf exhibited breaches,
forward lunges, tail slaps, and flipper slaps.
Associations of Bowheads with Other Species
We saw several marine mammal species in the
same general areas in which we observed bowheads:
ringed seals, Phoca hispida; white whales, Delphi-
napterus leucas; and a gray whale. There was no ob-
vious interaction between these species and bowhead
whales. The gray whale was about 500 m from the
closest bowhead. The Canadian Beaufort Sea is the
extreme northeastern limit of the gray whale's sum-
mer range (Rugh and Fraker 1981).
Flocks of up to 50 phalaropes {Pkalaroptis sp.)
were often present near skim-feeding bowheads.
These birds often alighted on water that had been
disturbed by the whales, sometimes only a few
meters from the whales. Phalaropes and bowheads
probably feed on some of the same plankton species.
The whalers used the presence of phalaropes as an
indicator of where "whale feed" was present and,
therefore, where whales were likely to be found (J.
R. Bockstoce in press). Aside from phalaropes, we
noticed glaucous gulls, Lamis hyperboreus; arctic
terns. Sterna paradisaea; and unidentified gulls
circling briefly over whales on eight occasions.
DISCUSSION
Activities of Bowheads in Summer and
Other Seasons
From 1980 through 1982 we observed a steady
progression in the August distribution of bowhead
whales near Tuktoyaktuk from shallow water near-
shore to deeper water farther from shore (Fig. 3;
Richardson et al.'^). Such a dramatic difference in
distribution over the 3 yr may be due to many dif-
ferent ecological and behavioral factors. Disturbance
"Koski, W. R., and R. A. Davis. 1980. Studies of the late sum-
mer distribution and fall mipration of marine mammals in NW Baf-
fin Bay and E Lancaster Sound, 1979. I'npubl. Rep., 214 p. LGL
Ltd., Toronto, for Petro-C'anada E^xplorations, Caljarary. Available
from Pallister Resource Management Ltd., 700 - 6th Avenue S.W.,
Calgary, Alberta T2P 0T6, Canada.
'^Richardson, W. J., K. A. Davis. C. K. Kvan.s, and P. Norton.
1983. Distribution of bowheads and industrial activity, 1980-82.
In W. J. Richardson (editor). Behavior, disturbance responses and
distribution of bowhead whales Balnenti ynysticetics in the eastern
Beaufort Sea, 1982. Unpubl. Rep., p. 269-3.'J7. L(]L Ecological
Research Associates, Inc., Bryan, TX, for U.S. Minerals Manage-
ment Service, Reston, VA. Available from Minerals Management
Service Alaska CX:S Region, P.O. Box 101159, Anchorage, AK
99510.
372
WI'RSIOETAL.: BEHAVIOR (IF HOWIIKADWHALKS
by industrial activity in nearshore waters is also a
possibility (see footnote 12). The fact that predomi-
nant feeding modes shifted from year to year is con-
sistent with the "variable food supply" explanation.
In 1980, whales in shallow water exhibited bottom
feeding and skim feeding, while whales in slightly
deeper water apparently fed in the water column. In
1981, most feeding appeared to be water-column
feeding and skim feeding. In 1982, whales made long
dives and presumably were often feeding in the
water column.
Bowhead whales have finely fringed baleen, the
longest of any whale species, and are adapted to
strain small zooplankters from the sea. Stomach con-
tents indicate that, at least in Alaskan waters, bow-
heads feed mainly on copepods. euphausiids, and
amphipods (Marquette et al. 1982). Summering bow-
heads tend to occur at locations where copepod abun-
dance is above average (Giiffiths and Buchanan foot-
note 7). Lowry and Burns (1980) examined five
whales killed off Barter Island, AK, in autumn and
found about 60% copepods and about 37% euphau-
siids in their stomachs. However, all five whales may
have fed at least partially near the sea floor; about
3% of the stomach contents consisted of mysids,
amphipods, other invertebrates, and fish. Durham
(1972) also suggested, based on stomach content
analyses showing mud-dwelling tunicates, vegeta-
tion, silt, and small pebbles, that bowheads feed at
times near the bottom. Lowry and Burns concluded
from stomach content analyses that "... a feeding
dive probably involves swimming obliquely from sur-
face to bottom and back, feeding the entire time."
Although this may be true at times, there is no direct
information on underwater feeding behavior. We
suspect that bowheads can detect concentrations of
prey and open their mouths when appropriate. The
bowhead whale is perhaps a more catholic feeder
than once thought, capable of taking advantage of
many different types of prey items at various posi-
tions in the water column and near the bottom. Year-
to-year changes in distributions and availability of
prey may account for the distributional changes that
we have observed, but data on yearly changes in
prey are lacking.
During spring migration around Alaska, bowhead
whales appear to do little feeding; their stomachs
usually are nearly empty (Marquette et al. 1982). On
the other hand, feeding continues in autumn after
bowheads have moved from the Canadian to the
eastern part of the Alaskan Beaufort Sea (Lowry
and Burns 1980; Marquette et al. 1982). Some
feeding occurs in autumn as far west as the Point
Barrow area (Lowry et al. 1978; Braham et al. 1984),
and perhaps farther west off the Soviet coast
(Johnson et al. 1981).
Feeding is not the only activity of bowheads in
summer. Socializing, perhaps with occasional sexual
activity, is also important. In 1982, however, there
was less socializing than in 1980-81. Whales were in
close proximity to each other less in 1982. This year-
to-year difference in proximity may be related to the
difference in type of feeding. While skim feeding at
the surface, whales are often in close echelons. The
proximity necessary for echelon feeding offers more
chance for socializing, and socializing before or after
feeding in echelon may be important to that mode of
feeding. When whales appear to feed in the water
column, however, they usually do not stay as close
together. Thus, this type of feeding may neither re-
quire nor stimulate aggregations of animals, and the
suspected predominance of water-column feeding in
1982 may explain the low socializing rate that year.
Even when there is no close socializing, however,
animals are often in a dispersed group within which
acoustic communication is probably possible. Our
observations of surfacing and dive synchrony by
whales spread over distances of several kilometers
indicate that they may have been in touch by acoustic
communication.
The primary mating period of bowhead whales
occurs in spring, including the spring migration
(Everitt and Krogman 1979; Carroll and Smithhisler
1980; Johnson et al. 1981; Nerini et al. 1984). We
saw some evidence for sexual activity in the Cana-
dian Beaufort Sea in both 1980 and 1981, but not in
1982. Even the active rolling at the surface that we
observed in 1981, however, was not as boisterous as
observed by Everitt and Krogman in spring. Also,
we found an indication of less social activity in late
August-early September than in early August. This
apparent waning in social activity may be a contin-
uation of the waning of sexual activity that started in
late spring.
Many calves are born in winter or spring before
the whales reach Point Barrow, although some may
be born in early summer (Davis et al. footnote 9).
During summer, the activities of female bowheads
with accompaning calves are closely coordinated
with those of their calves, and differ in some details
from the activities of other adult bowheads (this
study; Wursig et al. 1984). At least some calves re-
main with their mothers for the fall migration (Davis
and Koski 1980). We know of no information con-
cerning the age of weaning of bowhead calves, but in
the closely related right whale, at least some calves
remain with their mothers for 1 yr and ultimately
separate from their mothers after returning to the
373
FISHERY BULLETIN: VOL. 83, NO. 3
wintering area (Taber and Thomas 1982).
Aerial activity similar to what we observed in the
eastern Beaufort Sea- breaches, tail slaps, pectoral
flipper slaps, and rolls- has been observed in bow-
heads during spring migration (Rugh and Cubbage
1980; Carroll and Smithhisler 1980). It appears that
aerial behavior is more frequent during spring
migration than on the summer feeding grounds, and
this may be related to the high levels of social-sexual
activities during spring.
Comparisons with Other Baleen Whales
Bowhead whales spend their entire lives in arctic
and near-arctic waters. This habit separates them
from all other baleen whales, which may move into
temperate or subtropical waters (Lockyer and
Brown 1981). However, behavior is in large part
determined by feeding mode and related ecological
factors (Gould 1982), and here similarities between
bowhead whales and several other species are evi-
dent.
Gray, bowhead, and right whales are often found
in shallow water, and all three species feed on small
invertebrates. Gray whales usually feed near the bot-
tom (Bogoslovskaya et al. 1981; Nerini and Oliver
1983), whereas right and bowhead whales may skim
their food at or near the surface (see Watkins and
Schevill 1976, 1979 for right whales). But all three
species are adaptable in feeding behavior. Gray
whales apparently will feed on mysids associated
with kelp (Darling 1977) or on crab Pleuroncodes in
the water column (Norris et al. 1983). Right whales
also feed below the surface, probably straining
swarms of copepods and other small invertebrates in
the water column (Pivorunas 1979). While it has long
been known that bowhead whales feed at the surface
and in the water column (Scoresby 1820), it was
recently established from stomach content analyses
(Durham 1972; Lowry and Burns 1980), and by
observing bowhead whales surfacing with muddy
water streaming from their mouths (this study), that
bowheads sometimes feed near or on the bottom. It
is not surprising that there are many similarities in
the behavior of these species. Bowhead and right
whales, in particular, are morphologically and tax-
onomically quite similar, and appear to obtain their
food in very much the same ways. In fact. Rice
(1977). mainly relying on a detailed comparison of
morphology of bowhead and right whales, suggested
that they be put in the same genus, Balaena.
The sleeker rorquals (Balaenopterid whales)
generally gather their food more actively by lunging
through concentrations of prey, and at least in the
case of humpback whales, have developed compli-
cated behavioral strategies for confining and concen-
trating their prey (Jurasz and Jurasz 1979; Hain et
al. 1982). The rorquals are more often found in
deeper water far from shore, and their behavior in
general appears to be less similar to that of the
bowhead whale than its behavior is to that of gray
and right whales.
Gray whales spend part of the winter in warm
water, near the shores of Baja California, and most
of the summer they feed in the northern Bering and
southern Chukchi Seas. Western Arctic bowheads
make much shorter migrations, spending their
winter in the pack ice of the Bering Sea and their
summer predominantly in the Beaufort Sea. The two
species thus use the Bering Sea at different seasons
and for different purposes -gray whales to feed in
summer and bowheads apparently to mate and calve
in winter. Like bowhead whales summering in the
Beaufort Sea, the primary activity of gray whales
summering in the Bering and Chukchi Seas is
feeding. However, both bowheads and gray whales
(Sauer 1963; Fay 1963) occasionally socialize during
summer.
Right whales, like bowhead whales, often appear
to feed in the water column or at the surface
(Watkins and Schevill 1976, 1979) and may stay in
the same general area for days. While skim feeding,
both species at times aggregate into echelons. In
right whales, these echelons usually consist of only
3-6 whales (Payne, pers. obs.), while up to 14 bow-
head whales have been seen skim feeding in echelon.
However, Payne observed right whales during
winter when little feeding occurs, so apparent dif-
ferences in feeding details may be due to seasonal
factors.
Apparent differences between the social activity of
bowheads and right whales may also be largely attri-
butable to the different times of year when they have
been studied. The same kinds of nudges and pushes
have been observed for interacting whales of both
species, but the winter-spring social activity of right
whales is much more boisterous than the summer
social activity of bowheads. Observations of bowhead
whales in spring indicate that their social-sexual acti-
vity at that season can be as boisterous as is seen in
mating groups of right whales (Everitt and Krogman
1979; Carroll and Smithhisler 1980; Rugh and Cub-
bage 1980; Johnson et al. 1981). The belly-up posi-
tion of a female bowhead photographed in spring in
the Alaskan Beaufort Sea (Everitt and Krogman
1979) indicates that females may attempt to evade
potential mates who pursue them in large mating
aggregations in the same way that female right
374
Wl'KSlCKTAl..: HKHAVK )K OK BOWIIKAD WHALKS
whales evade males in Argentine waters (Payne and
Dorsey 1983). A photograph showing a remarkably
similar mating group of right whales is shown in the
article by Payne (1976). The fact that similar-looking
social aggregations are seen in both species argues
for a similar social system, although it does not show
that the social systems are similar in all details.
Female right whales have young only at intervals
of 3 yr or more (Payne, pers. obs.). The same appears
to be true of bowheads (Davis et al. footnote 9;
Nerini et al. 1984). This long calving interval may
help to explain why bowhead and right whales have
not made as dramatic a recovery from commercial
exploitation as has, for example, the gray whale.
Payne also found that right whale females that calve
along the shore of southern Argentina in winter are
usually not present in the years between calving.
Each winter, a different segment of the population of
mature females is present, in a 3-yr cycle. It is not
known whether this cycling extends to the summer
feeding grounds of these right whales. During the
present 3-yr study, year-to-year variation in feeding
and social behavior was dramatic, but we do not
know whether this was due in part to some cyclic and
synchronized activity of individual whales. We
suspect that variable prey distibution was largely
responsible.
ACKNOWLEDGMENTS
This project, including preparation of this paper,
was funded by contracts from the Bureau of Land
Management and the Minerals Management Service,
U.S. Department of the Interior, to LGL Ecological
Research Associates. We thank the Polar Continen-
tal Shelf Project of the Department of Energy,
Mines, and Resources (Canada) for logistical help.
Dome Petroleum Ltd. and Esso Resources Canada
Ltd. shared data and assisted with logistics.
NORCOR Engineering and Research Ltd. provided
the Islander aircraft, and J. Merilees was its capable
pilot. Personnel of the Beaufort Weather Office were
helpful. K. Finley, P. Tyack, and R. Wells helped
with aerial observations. K. Hazard, G. Silber, S.
Taber, P. Thomas, and M. Wiirsig collected data
from Herschel Island. C. Greene of Polar Research
Laboratory set up the sonobuoy system. S. Heimlich-
Boran prepared the illustrations of bowheads in this
paper. J. Bird, L. Guinee, and V. Rowntree of the
New York Zological Society, and C. R. Evans, R.
Wells, and M. Wiirsig assisted with data analysis. H.
Braham provided helpful suggestions on an earlier
draft. We thank all of these organizations and in-
dividuals.
LITERATURE CITED
Batschelet, E.
1972. Recent statistical methods for orientation data. In S.
R. Galler, K. Schmidt-Koenig, G. J. Jacobs, and R. E. Belle-
ville (editors), Animal orientation and navigation, p. 61-91.
NASA SP-262, Natl. Aeronaut. Space Admin., Wash.,
D.C.
BOGOSLOVSKAYA, L. S., L. M. VOTROGOV, AND T. N. SEMENOVA.
1981. Feeding habits of the gray whale off Chukotka. Rep.
Int. Whaling Comm. 31:507-510.
Braham, H. W., B. D. Krogman, and G. M. Carroll.
1984. Bowhead and white whale migration, distribution, and
abundance in the Bering, Chukchi, and Beaufort Seas, 1975-
78. U.S. Dep. Commer., NOAA Tech. Rep. NMFS SSRF-778,
39 p.
Braham, H., B. Krogman, J. Johnson, W. Marquette, D. Rugh,
M. Nerini, R. Sonntag, T. Bray, J. Brueggeman, M.
Dahlheim, S. Savage, and C. Goebel.
1980. Population studies of the bowhead whale {Bakierwi mys-
ticetus): results of the 1979 spring research season. Rep.
Int. Whaling Comm. 30:391-404.
Braham, H. B. Krogman, S. Leatherwood, W. Marquette, D.
Rugh, M. Tillman, J. Johnson, and G. Carroll.
1979. Preliminary report of the 1978 spring bowhead whale
research program results. Rep. Int. Whaling Comm. 29:291-
306.
Brown, R.
1868. Notes on the history and geographical relations of the
Cetacea frequenting Davis Strait and Baffin's Bay. Proc.
Zool. Soc. Lond., 35:533-556.
Carroll, G. M., and J. R. Smithhisler.
1980. Observations of bowhead whales during spring migra-
tions. Mar. Fish. Rev. 42(9-10):80-85.
Dahlheim, M., T. Bray, and H. Braham.
1980. Vessel survey for bowhead whales in the Bering and
Chukchi Seas, June-July 1978. Mar. Fish. Rev. 42(9-10):51-
57.
Darling, J. D.
1977. Aspects of the behavior and ecology of Vancouver
Island gray whales, Eschrichtius glaucus Cope. M.S. Thesis,
Univ. Victoria, 200 p.
Davis, R. A., and W. R. Koski.
1980. Recent observations of the bowhead whale in the
eastern Canadian High Arctic. Rep. Int. Whaling Comm.
30:439-444.
Dorsey, E. M.
1983. Exclusive adjoining ranges in individually identified
minke whales (Balaewyptera acutorostrata) in Washington
state. Can. J. Zool. 61:174-181.
Durham, F. E.
1972. Greenland or bowhead whale. In A. Seed (editor).
Baleen whales in eastern North Pacific and arctic waters, p.
10-14. Pacific Search Press, Seattle, WA.
EVERITT, R. D., AND B. D. KROGMAN.
1979. Sexual behavior of bowhead whales observed off the
north coast of Alaska. Arctic 32:277-280.
Fay, F. H.
1963. Unusual behavior of gray whales in summer. Psychol.
Forsch. 27:175-176.
FRAKER, M. a., and J. R. BOCKSTOCE.
1980. Summer distribution of bowhead whales in the eastern
Beaufort Sea. Mar. Fish. Rev. 42(9-10):57-64.
Gould, J. L.
1982. Ethology, the mechanisms and evolution of behavior.
W. W. Norton & Co., N.Y. 544 p.
375
FISHERY Bl'LLETIN: VOL. Ki. NO. S
Hain, J. H. W., G. R. Carter, S. D. Kraus, C. A. Mayo, and H. E.
Winn.
1982. Feeding behavior of the humpback whale, Megaptera
navaeangliae, in the western North Atlantic. Fish. Bull.,
U.S. 80:259-268.
Herman, L. M.. and R. C. Antinoja.
1977. Humpback whales in the Hawaiian breeding waters:
Population and pod characteristics. Sci. Rep. Whales Res.
Inst 29:59-85.
Johnson, J. H., H. W. Braham, B. D. Krogman, W. M.
Marquette, R. M. Sonntag, and D. J. Rugh.
1981. Bowhead whale research: June 1979 to June 1980.
Rep. Int Whaling Comm. 31:461-475.
Johnson, M. L., C. H. Fiscus, B. T. Ostenson, and M. L.
Barbour.
1966. Marine mammals. I-n N. J. Wilimovsky and J. N. Wolfe
(editors). Environment of the Cape Thompson region, Alaska,
p. 877-924. U.S. At. Energy Comm., Oak Ridge, TN.
JuRASZ, C. M., and v. p. Jurasz.
1979. Feeding modes of the humpback whale, Megaptera
nm^aeangliae, in Southeast Alaska. Sci. Rep. Whales Res.
Inst. 31:69-83.
Kraus, S. D.. J. H. Prescott, P. V. Turnbull, and R. R. Reeves.
1982. Preliminary notes on the occurrence of the North Atlan-
tic right whale, EvhaUiena glacialis. in the Bay of Fundy.
Rep. Int. Whaling Comm. 32:407-411.
Ljungblad, D. K., M. F. Platter-Rieger, and F. S. Shipp, Jr.
1980. Aerial surveys of bowhead whales. North Slope Alaska:
final report fall 1979. Nav. Ocean Syst Cent Tech. Doc.
314, 181 p. Naval Ocean Systems Center (Code 5131), San
Diego, CA.
Lockyer, C. H., and S. G. Brown.
1981. The migration of whales. In D. J. Aidley (editor).
Animal migration, p. 105-137. Soc. Exp. Biol. Semin. Sen
13, Cambridge Univ. Press.
LowRY, L. F., AND J. J. Burns.
1980. Food utilized by bowhead whales near Barter Island,
Alaska, autumn 1979. Mar. Fish. Rev. 42(9-10):88-91.
LowRY, L. F., K. J. Frost, and J. J. Burns.
1978. Food of ringed seals and bowhead whales near Point
Barrow, Alaska Can. Field-Nat 92:67-70.
Marquette, W. M., H. W. Braham, M. K. Nerini, and R. V.
Miller.
1982. Bowhead whale studies, autumn 1980 -spring 1982:
harvest, biology and distribution. Rep. Int Whaling Comm.
32:357-370.
Matsushita, T.
1955. Daily rhythmic activity of the sperm whale in the
Antarctic Ocean. Bull. Top. Soc. Sci. Fish. 20:770-773.
Nemoto, T.
1970. Feeding pattern of baleen whales in the ocean. IvJ.U.
Steele (editor). Marine food chains, p. 130-141. Oliver and
Boyd, Edinburg.
Nerini, M., H. Braham, W. Marquette, and D. Rugh.
1984. Life history of the bowhead whale. J. Zool. (Lond.).
204:443-468.
Nerini, M. K., and J. S. Oliver.
1983. Gray whales and the structure of the Bering Sea
benthos. Oecologia 59:224-225.
NoRRis, K. S., R. M. Goodman, B. Villa-Ramirez, and L. Hobbs.
1977. Behavior of California gray whale, Eanhrichtius robua-
tns, in southern Baja California, Mexico. Fish. Bull., U.S.
75:159-172.
NoRRis, K. S., B. Villa-Ramirez, G. Nichols, B. Wursig, and
K. Miller.
1983. Lagoon entrance and other aggregations of gray whales
(Eschrichtms rotnistus). In R. Payne (editor). Communica-
tion and behavior of whales, p. 259-298. AAAS Selected
Symp. 76, Westview Press, Boulder, CO.
Payne, R.
1972. Swimming with Patagonia's right whales. Nat Geogr.
142:576-587.
1976. At home with right whales. Nat Geogr. 149:322-339.
1983. Intnxiuction. In R. Payne (editor), Communication
and behavior of whales, p. 1-6. AAAS Selected Symp. 76,
Westview Press, Boulder, CO.
Payne, R., and E. M. Dorsey.
1983. Sexual dimorphism and aggressive use of callosities in
right whales (Eubalaena aristralis). In R. Payne (editor).
Communication and behavior of whales, p. 295-329. AAAS
Selected Symp. 76, Westview Press, Boulder, CO.
Pivorunas, a.
1979. The feeding mechanisms of baleen whales. Am. Sci.
67:432-440.
Rice, D. W.
1977. A list of the marine mammals of the world. U.S. Dep.
Commer., NOAA Tech. Rep. NMFS SSRF-711, 15 p.
Richardson, W. J., M. A. Fraker, B. Wursig, and R. S. Wells.
In press. Behaviour of bowhead whales, Balaena myMicetua.
summering in the Beaufort Sea: reactions to industrial
activities. Biol. Conserv.
Rugh, D. J., and J. C. Cubbage.
1980. Migration of bowhead whales past Cape Lisburne, Alas-
ka. Mar. Fish. Rev. 42(9-10):46-51.
Rugh, D. J., and M. A. Fraker.
1981. Gray whale (Earhrichtius robustus) sightings in eastern
Beaufort Sea. Arctic 34:186-187.
Saayman, G. S., C. K. Tayler, and D. Bower.
1973. Diurnal activity cycles in captive and free- ranging
Indian Ocean bottlenose dolphins {Tvrsiopg aduncus Ehren-
burg). Behaviour 44:212-233.
Sauer, E. G. F.
1963. Courtship and copulation of the gray whale in the
Bering Sea at St Lawrence Island, Alaska. Psychol. Forsch.
27:157-174.
Schevill, W. E., and R. H. Backus.
1960. Daily patrol of a Megaptera. J. Mammal. 4 1 :279-28 1 .
Scoresby, W., Jr.
1820. An account of the Arctic regions, with a histor\' and
description of the northern whale-fisher>'. Archibald Con-
stable and Co., Edinburgh: 2 Vols. Reprinted (1969) by
David and Charles (Holdings) Ltd., Newton Abbot Devon,
Engl.
Shane, S. H.
1980. Occurrence, movements, and distribution of bottlenose
dolphin, Tursiops truncatiis, in southern Texas. Fish. Bull.,
U.S. 78:593-601.
SUMICH, J. L.
1983. Swimming velocities, breathing patterns, and estimated
costs of locomotion in migrating gray whales, Eschrichtms
robustus. Can. J. Zool. 61:647-652.
Taber, S., and p. Thomas.
1982. Calf development and mother-calf spatial relationships
in southern right whales. Anim. Behav. 30:1072-1083.
Townsend, C. H.
1935. The distribution of certain whales as shown by logbook
records of American whaleships. Zoologica (N.Y.) 19:3-50.
Tyack, p., and H. Whitehead.
1983. Male competition in large groups of wintering hum|>-
back whales. Behaviour 83:132-154.
Watkins, W. a., and W. E. Schevill.
1976. Right whale feeding and baleen rattle. J. Mammal. 57:
376
WI'RSICKTAL.: BKHAVIOK OK HOWIIKAl i WIIAI-KS
58-66. dolphins. Ph.D. Thesis, State Univ. New York, Stony Brook,
1979. Aerial observation of feeding behavior in four baleen 326 p.
whales: Eubalaena glacialvt, Balaenoptera borealis, Mega- WiJRSlG, B., E. M. DoRSEY, M. A. P'raker, R. S. Payne, W. .1.
ptera nomeangliae, and Balaenoptera physalus. J. Mammal. Richardson, and R. S. Weels.
60:155-163. 1984. Behavior of bowhead whales, Balaena mysticetus,
WuRSiG, B. summering in the Beaufort Sea: surfacing, respiration and
1978. On the behavior and ecology of bottlenose and dusky dive characteristics. Can. J. Zool. 62:1910-1921.
377
FOOD HABITS OF BAIT-CAUGHT
SKIPJACK TUNA, KATSUWONUS PELAMIS, FROM
THE SOUTHWESTERN ATLANTIC OCEAN
Lisa Ankenbrandt'
ABSTRACT
Stomach cdntents ofskipjai'k tuna captured in 1981-82 by live jiole-aml-lino vessels off the southern coast of
Brazil were analyzed for the presence of larval and juvenile skipjack tuna. The percentage frequency of
occurrence, perc'ent number, and percent volume were evaluated. Of the 1,041 stomachs that were exam-
ined for food. 48B were empty. The mean volume of focxi in all stomachs analyzed was 3ti.9 niL. of which
18.9 mL was bait and 18.0 mL was prey.
The g-onostomatid Moiirolicii.'i muelleri and the euphausiid Euphauxin simHi^ were the principal foods.
Other important food.s were the chub mackerel, Sramberjaponiem; the fripjate tuna, Auj-is thuziird; ^jem-
pylids: trichiurids; and carangids. In the study area, adult skipjack tuna were not found to feed on their
young.
Kruskall-Wallis nonparametric one-way analysis of variance was used to test for differences in the mean
volumetric ratios of food items in relation to skipjack size. The percentage oiE. xiwUv^ in the diet was found
to decrease, while the proportion of M. muelleri was found to increase with increasing skipjack size.
Seasonal variations in the diet were also examined and discussed.
Apparently the anatomy of their gill raker apparatus allows skipjack to ingest a wide variety of prey
ts'pes above a minimum size. These variations in the food can be attributed to the number and size of the
prey species in an area.
A Brazilian skipjack pole-and-line fishery has been
developing in the Rio de Janeiro area since 1979
(Fig. 1). Because skipjack tuna, Katswonus pelamis,
is one of the major tuna species harvested at maxi-
mum sustainable yield in the tropical and subtropical
oceans (Kearny 1976; Evans et al. 1981), estimation
of the fishery potential requires information on the
distribution and concentration of its spawning stock.
One technique used to determine the existence of a
spawning stock is to quantify the distribution of its
larvae. Obviously, the presence of large numbers of
larvae would indicate a spawning stock occupies an
area.
Knowledge of the distribution and abundance of
juvenile skipjack tuna is limited. Occasionally, speci-
mens have been found in experimental plankton
hauls or in the stomachs of apex predators (Kearny
1976). From ichthyoplankton surveys, Matsuura
(1982) and Nishikawa et al. (1978) reported larvae in
warm tropical waters north of the study area (Fig.
1), and juvenile skipjack tuna have been found in the
stomachs of adult skipjack tuna captured off west
Africa and in the Caribbean (Suarez-Caabro and
■Southwest Fisheries Center La JoUa Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271. La Jolla, CA
92038; present address: School of Fisheries, University of
Washington, Seattle, WA 98195.
Duarte-Bello 1961; Klawe 1961; Dragovich 1970;
Dragovich and Potthoff 1972). Their occurrence in
the diet of central and south Pacific skipjack tuna
caught by pole-and-line has been used to deduce their
distribution and abundance (Waldron and King 1963;
Nakamura 1965; Argue et al. 1983).
—
~~
~~
~~
■H
"~
^^^
BRAZIL ^
/
1 'M
5 w.
((•
<i w
f
\A
Rio de Janerio^^^
^ (T
.4^mf^
AM^
<-jM
r_H
m
/
}
j>
1
i
i
/]
/
<^
tS:^-^
)
■ Adult Occurrence
A
^ Larval Occurrence
'TI
J
1 II II 1 1 1 1 1 1 1 1 1 1 1 1 II
20°S
30°S
60°W
500W
40°W
30°W
40°S
Manuscript accepted October 1984.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
Figure 1.- Solid area indicates fishing localities from where skip-
jack tuna stomachs were obtained. Hatched area shows larval occur-
rence (Matsuura 1982).
379
FISHERY BILLETIN: \( )L. Ki. NO. -.i
Dragovich (1969) reviewed existing information on
the food habits of Atlantic skipjack tuna. Since that
time food habits have also been reported in studies
by Dragovich (1970) and Dragovich and Potthoff
(1972) for skipjack from the East and West Atlantic
and by Batts (1972) for skipjack in North Carolina
waters. Zavala-Camin (1981) examined predator-
prey interactions of fishes, including skipjack cap-
tured north of the area in this study.
The primary objective of this study was to discover
if skipjack tuna feed upon their young. The presence
of juveniles in bait-caught skipjack stomachs would
verify the study area as a spawning-rearing ground.
Knowledge of the prey and their relative importance
also contributes to the understanding of prey-
predator interactions, which affect population
distributions and fluctuations.
MATERIALS AND METHODS
Stomach samples for this study were collected on a
monthly basis from October 1981 to December 1982
from skipjack tuna caught off Rio de Janeiro (Fig. 1).
National Marine Fisheries Service (NMFS) person-
nel collected stomachs from frozen fish transhipped
to Puerto Rico, and Superintendencia do Desenvol-
viemento da Pesca (SUPEDE) personnel sampled
fish landed locally in Rio de Janeiro. Fish from the
Puerto Rican source were caught within 1 mo prior
to sampling; fish from the Brazilian source were sam-
pled 3 to 5 d after the recorded catch date. The sam-
pling design required collecting about 15 stomachs
from each 10 cm length group, measured to the
nearest cm per month. However, the number of
stomachs collected was dependent on the catch-size
distribution. Once the stomach was removed from
the fish, it was preserved in 10% buffered Formalin-
and shipped to the Southwest Fisheries Center
(SWFC) for analysis.
Stomachs were examined from 1,041 fish between
44 and 81 cm fork length. In the laboratory each
stomach was opened. The volume of the food bolus
was measured, and the contents were identified to
the lowest possible taxon. The taxonomic groupings
were then measured by volumetric displacement.
and the individuals counted. Whole undigested fish
were identified by comparing external characters
with those described in published keys or with iden-
tified museum specimens from Scripps Institution of
Oceanography, La Jolla, CA. Digested animals, par-
ticularly juvenile scombrids, were identified by verte-
bral, gill raker, and fin ray counts, as well as other
skeletal characteristics, described by Potthoff and
Richards (1970), Miller and Jorgenson (1973), and
other published keys. Cephalopods were identified by
comparing beak characters with published illustra-
tions, descriptions, and keys (see Wolff 1981). Crus-
taceans and other invertebrates were identified by
specialists from Scripps Institution of Oceanography
and SWFC.
The occurrence of bait in the stomachs may have
biased the relative importance of fish in the diet. The
bait primarily consisted of Sardinella brasiliensis,
Harengula jaguana, and Engraulis anchoita;
however, other fish families may have been included
in the captured bait. The sardines were readily iden-
tifiable from their external characters and usually
were undigested. The anchovies, in contrast, were
often quite digested, creating difficulties in identifi-
cation. Gary Nelson^ nevertheless was able to verify
these fish as Engraulis anchoita. Although the least
digested item in the stomach was usually the last
meal (bait), stomachs were removed from a few days
to 1 mo after capture, and presumably postmortem
digestion occurred. As a result, the degree of diges-
tion was not a reliable indication of distinguishing
bait from natural prey. The time required for com-
plete gastric evacuation of smelt fed to skipjack tuna
is estimated to be 12 h (Magnuson 1969). Although
the bait was captured in nets from bays and estuaries
(Rinaldo4), Matsuura et al. (1978, 1981) have con-
firmed that a spawning stock of £■. anchoita does ex-
ist in waters inhabited by skipjack tuna. It is unlikely
that the sardines served as prey for skipjack.
However, I could not distinguish between E. an-
choita consumed as natural food and as bait. There-
fore, although these species were considered bait,
some may have been ingested as natural food. Bait
was not considered prey, and stomachs containing
only these species were treated as empty.
Two methods of analysis were employed to rank
the food items in terms of availability and impor-
tance to the skipjack tuna:
1) An index of relative importance (IRI) was calcu-
lated for each prey type in terms of numbers,
volumes, and fre(|uencies (Pinkas et al. 1971):
IRI = {N + V)F
''Reference to trade names does not innply endorsement by the Na-
tional Marine Fisheries Service, NOAA.
'G. J. Nelson, Department of Ichthyolojjx-. American Museum of
Natural History, New York, NY 10024. pers. commun.. May 1982.
■•R. R. Rinakid, Southwest Fisheries Center La .lolla Laboratory,
National Marine Fisheries Service, NOAA. I'.O. Box 271, La Jolla,
CA 92038, pers, commun., .June 1982,
380
ANKKNBRANDT: FdOD HABITS OF SKIPJACK TINA
v/hereN = numerical percentage
V = volumetric percentage
F = frequency of occurrence percentage.
2) The mean volumetric ratio measurement
(An'RAT) was used to illustrate the biomass impor-
tance of prey items without the numeric exaggera-
tion implicit in the IRI (John Hedgepeth^). The
MVRM was calculated from the volumetric analysis
of individual stomachs with each prey item contribu-
ting to the total stomach volume. MVRM for each
food type is expressed as
M\'RM = r^ X 100 = mean volumetric percentage
of prey j to the total volume of
n stomachs
where N = number of stomachs in a given strata
y, J = volume of prey type j in stomach i
V: = Z V: , = total volume of stomach i
j=i
'J
y.-
'J
i _ ratio of prey j to the total vol-
V^ ume of stomach i
'7
n =
'=^^ _ mean volumetric ratio of
n prey J to the total volume of
n stomachs.
Both the IRI and the MVRM, which examine dif-
ferent aspects of the diet, were used to evaluate
seasonal variations in skipjack tuna food habits. The
IRI presents a biased estimate caused by the
numerical percentage; the relative importance of
small numerous organisms, like euphausiids, is exag-
gerated in the IRI because of their high numbers,
when actually they may represent the same food
value as a few large fish. The M\^RM is an expression
of frequency of occurrence and volume without a
numeric bias, but does not provide any information
on prey abundance. The IRI contains information on
the availability of the prey in the environment in
terms of numbers, while the MVRM provides an in-
dication of its energetic importance to the fish.
The MVRMs, were stratified by fish length and
y. B. Hedgepeth, Southwest Fisheries Center La Jotta
Laboratorj', National Marine Fisheries Ser\'ice, NOAA, P.O. Box
271, La JoUa, CA 92038, pers. commun., April 1982.
annual quarter (Fig. 2), and tested with the Krus-
kal-Wallis nonparametric one-way analysis of
variance to evaluate differences in diet with changes
m size.
>-
O
z
UJ
3
o
UJ
300-
—
ALL MONTHS
200-
100-
n -
n
100-
I I T T T
QUARTER 4
75-
50-
25-
1
1
Ci -
rn
u
75-
I I I I I I 1 I
QUARTER 3
50-
25-
n -
n
yj
100-
I I
I I I T T-
QUARTER 2
75 -
50-
1
25-
n -1
u
75-
I 1 1 I 1
QUARTER 1
50-
25-
0 -
' — ^
' — ^
r — '•
i .,
^ *
.^=^
40 50 60 70 80
LENGTH (cm)
Figure 2. - Length-frequency distribution of skipjack tuna from
which stomachs were collected.
381
FISHERY BULLETIN: VOL. 83, NO. 3
RESULTS
Food Composition
Of the 1,041 stomachs that were examined, 436
were empty. The mean volume of food in all
stomachs examined was 36.9 mL, of which 18.9 mL
was bait and 18.0 mL was prey. A complete list of
the stomach contents in terms of numbers, volume,
and frequency is presented in Appendix Table 1. No
larval or juvenile skipjack were found in the stomach
contents. Overall contributions of each category are
presented in Figure 3.
In terms of the M\''RM, the gonostomatid Mauro-
licwi muelleri was the major prey item (MVRM =
26.7%). The euphausiid Ewphausia similis, with the
highest IRI, was also important {IRI = 1 ,998). These
items were major constituents of the diet throughout
the year. Other important fishes in terms of both the
ALL MONTHS
ME«N %
VOLUME (ranki
17 4 7 3 5 2 25 1 14 8 4 0
PERCENT FREQUENCY OF OCCURRENCE
FiGiiRE .3. -Index of relative importance (IRI) plots for selected
food items of skipjack tuna caught during 1982. The food categories
are ranked in terms of IRI and MVRM.
JANUARY-MARCH
5 60
X
o *o
^ Tl ^ e I
SPECIES
Euphausia similts
Maurolicus muelleri
Auxis thazard
Scomber japonicus
FISH
CRUSTACEANS
CEPHALOPODS
IRI
(rank)
1756 49 (I)
228 60 (3)
3805^^)
47 31 <5)
116 29^2)
58 92 (4)
1.57 (6)
MEAN %
VOLUME (rank)
19 80 (3)
14 IS (4)
Included in fish
1008 (5)
29 55 (1)
23 47 (2)
3.02 (6)
APRIL-JUNE
• Auxis thazard
included in fish for ranking
~ combined IRI = 309.66
70 73 24.3 22 6 27
PERCENT FREQUENCY OF OCCURRENCE
S 60
O 40
r
SPECIES
IRI MEAN %
(rank! VOLUME (rank)
-
1
Euphausia similis 275206(1) 38.32(1)
jLiS^
2
Maurolicus muelleri
771 62 (2) 25 96 (2)
„
•A**^
3
Caranx ruber
33.8 1*(3) Included in fish
/ /
4
FISH
30.14*(3) 20 02 (3)
S
CRUSTACEANS
6.42 (4) 8 16 (4)
6
CEPHALOPODS
0.584 (5) 7 4 (5)
-
4>
1 /
<
• Caranx ruber
included in fish for ranking
- combined IRI = 135.39
-
'^X^^^
-
^
-^
1 1
1 1
13.3 59 90 90 24
PERCENT FREQUENCY OF OCCURRENCE
JULY-SEPTEMBER
SPECIES
Euphausia similis
IRI
(rank)
MEAN %
VOLUME (rank)
1037 32 (2) 9 60 (3)
3710 17 (1) 55 40 (1)
34 45 (4) 5 70 (5)
7 60*(3) Included in liah
7 1.76*(3) 22.87 (2)
7.31 (5) 6.42 (4)
0 036 (6) 0.01 (6)
• Benthodesmus sp.
included in fish for ranking
combined IRI = 127.4
OCTOBER-DECEMBER
MEAN %
VOLUME (rank)
34 I 3.7 3 7 18 4 9 2 0.4
PERCENT FREQUENCY OF OCCURRENCE
17 2 23 2 19 3 33 5 17 2 9 2
PERCENT FREQUENCY OF OCCURRENCE
Figure 4. -Index of relative importance (IRI) plots for selected food items of skipjack tuna. The complete data are divided into four 3mo
quarters (I-IV). The food categories are ranked in terms of IRI and mean percent volume.
382
ANKHNHKANPT: R)()I) HAHl'I'S ( )K SKIIMACK Tl'NA
IRI and M\'RM were chub mackerel, Scomber
japonicus. and Thyrsitops lepidopoides*^ (Fig. 3).
Crustaceans other than A\ fiirriilis occurred frequent-
ly in the stomachs (F = 22.6%), but as a relatively
low percentage of the total volume {V = 2.0%).
Cephalopods were usually insignificant in the diet
(see below). Pteropods, siphonophores, beetles,
rocks, and unidentified materials were the consti-
tuents of the miscellaneous category (App. Table 1).
Seasonal Variations
The data were divided into four quarters: January-
March 1982 (I), April-June 1982 (II), July-September
1982 (III), October-December 1981 and 1982 (IV).
The results (App. Tables 2-6) are illustrated in
Figures 4 and 5 both with the IRI and the MVRM of
•^Identified by Y. Matsuura, Universidade de Sao Paulo, Institiito
Oceanografico, Sao Paulo, Brazil, October 1984.
dominant food items in each quarter. Note that items
important in one quarter may be negligible or absent
in another. When evaluated in terms of MVRM, the
prey ranks sometimes did not coincide with those
determined by the IRI (Figs. 4, 5). Based on the IRI,
E. similvi was the dominant food in the first quarter,
followed by other fish and M. muelleri (Fig. 4).
According to the MVRM, other fishes, other crusta-
ceans, and E. similis were ranked first, second, and
third in importance, respectively. The importance of
E. similis in this quarter based on the IRI was exag-
gerated by their high frequencies of occurrence.
Scomber' japonicus and frigate tuna, Auxis thazard,
were secondary in importance to M. muelleri as the
main fish species consumed.
The rankings of the food categories in the second
quarter were the same for both the IRI and the
MVRM (Fig. 4). Euphausia similis and M. muelleri
were the dominant food items, followed by Caranx
ruber.
Figure .5. -Relative importance based on mean volumetric ratio of selected food items for skipjack tuna grouped by length for each quarter
(I-IV) and all months. * indicates a significant difference (P < 0.05) in the mean percent volume of that food item by length when tested with
the Kruskal-Wallis nonparametric one-way analysis of variance.
383
FISHERY BULLETIN: VOL. 83, NO. 3
The principal food item in the third quarter based
on both measurements was M. muelleri (Fig. 4). The
ranks for the other items did not correspond. Eu-
phausia similis was second in importance according
to the IRI, but ranked third next to other fish based
on the MVRM. Scomber japonicus and Benthodes-
mus sp. were the predominant species consumed in
the fish category.
The IRI and MVRM ranks in the fourth quarter
corresponded with the exception of the principal
prey type (Fig. 4). Again, E. similis ranked first ac-
cording to the IRI, but Thyrsitops lepidopoides was
the primary food item based on the MVRM. Cepha-
lopods, mainly Argonauta sp., were consumed in
significant proportions in this quarter {IRI = 31.7,
MVRM = 7.2%).
In summary, M. muelleri and E. similis predom-
inated in the skipjack tuna diet during all quarters
(Fig. 3). With the exception of the second quarter, S.
japonicus was an important food item. Benthodesmus
sp., C. ruber, A. thazard, as well as the cephalopod,
Argonauta sp., also proved important in specific
quarters. The importance of T. lepidopoides in
Figure 3 was exaggerated by its predominance in the
fourth quarter.
Variations with Size
As might be expected, basic dietary changes occur
as the skipjack tuna grow. Nakamura (1965), Alver-
son (1963), Batts (1972), Dragovich and Potthoff
(1972), and Wilson (1982) observed a decrease in the
relative importance of crustaceans and an increasing
importance of fish in the diet, as the skipjack size in-
creased.
To evaluate the relationship between size and food
habits, the skipjack were arbitrarily divided into
seven 5 cm groups (Fig. 2). For each prey category
the MVRMs were stratified by size group and
(quarter (App. Tables 6-10, Fig. 5). Trends reported
in the results for length groups > 70 cm may not
represent feeding habits of skipjack tuna from the
study area because the sample sizes were too small
(Fig. 2. App. Table 6).
There were no significant differences (P < 0.05) in
diet and size in the first quarter except in the amount
of other fish consumed (Fig. 5, App. Table 7). The
MVRM of this category increased from 28.7% in
skipjack 45.0-49.9 cm to 91.7% in fish 75.0-79.9 cm.
In the second quarter the proportions of other fish,
other crustaceans, E. similis, and M. muelleri signi-
ficantly changed with size (Fig. 5, App. Table 8). The
larger skipjack tuna ate more fish {MVRM = 1 .7% in
the 45.0-49.9 cm size class toMVRM = 54.1% in the
75.0-79.9 cm size class) and more M. muelleri
{MVRM = 15.4% to MVRM = 30.3%) than the
smaller skipjack. As their size increased, skipjack
decreased their consumption of E. similis from
MVRM = 76.9% to MVRM = 4.5%. There was a
significant difference between size classes {P < 0.05)
in the MVRM of other crustaceans in the diet, but
this difference seemed uncorrected to increases in
size.
In the third quarter there were no significant dif-
ferences in the diet with increasing size except that
the MVRM of E. similis decreased from 25.0% to
8.0% (Fig. 5, App. Table 9).
Thyrsitops lepidopoides was eaten by the smaller
skipjack (45-59.9 cm) only in the fourth quarter (Fig.
5, App. Table 10). Although there were significant
differences {P < 0.05) in the diets between the seven
size groups during this period, these differences
again seemed unrelated to increasing size.
In summary, when the data on T. lepidopoides
were included with the rest of the fish data, there
were no significant differences between size groups
in the proportions of other fish consumed throughout
the year (Fig. 5, App. Table 6). The MVRM of E.
similis in the diet decreased from 42.5% in skipjack
tuna 45.0-49.9 cm to 0.0% in skipjack 75.0-79.9 cm.
There were significant differences in the percent-
ages of M. muelleri and S. japoniciis between the
size classes. There were no significant differences in
the MVRM of other crustaceans with changes in size.
As reported in the studies of the food habits of
skipjack tuna referred to above, the stomach con-
tents of skipjack from this area indicated the basic
dietary changes associated with increasing size: a
significant decrease in the proportion of E. similis,
the predominant crustacean prey, and an increase in
proportion of M. muelleri, the predominant fish
prey.
DISCUSSION
Several studies have reported that skipjack tuna
feed predominantly on euphausiids and gonostoma-
tids. Dragovich and Potthoff (1972) reported that the
gonostomatid Vinciguerrin nimbario contributed
44.7% by volume to the diet of skipjack tuna from
the Gulf of Guinea. Zavala-Camin (1981) reported M.
muelleri and euphausiids as dominant food items in
36 stomachs of skipjack caught off Brazil. Alverson
(1963) reported skipjack tuna captured in the eastern
tropical Pacific fed primarily on euphausiids (47% by
volume, in 37% of the stomachs), followed in impor-
tance by the gonostomatid Vinciguerria lucetia
(10% by volume). The abundance of euphausiids in
384
ANKKNHKANltT: FOOH HABITS OK SKIIMACK TINA
the stomachs of skipjack, compared with larger
scombrids. may be a result of smaller gill raker gaps
in skipjack (Magnuson and Heitz 1971).
The importance of other fishes as food for western
Atlantic skipjack tuna observed in this study has
been previously reported. Dragovich (1970) found a
predominance of fish in the stomachs of skipjack
caught off the eastern United States and the Carib-
bean. Suarez-Caabro and Duarte-Bello (1961) found
that fishes constituted 75% of the total volume,
followed by squid (23%) and crustaceans (2%), in the
stomachs of Cuban skipjack. Zavala-Camin (1981)
observed that fish constituted 38.9%, crustaceans
22.2%, and mollusks 2.8% of the total stomach
volume of Brazilian skipjack.
CONCLUSIONS
The multiplicity of prey found in this as well as
other studies indicates that tunas are perhaps non-
selective feeders, and stomach contents are probably
determined by prey availability (Hotta and Ogawa
1955; Alverson 1963; Batts 1972; Perrin et al. 1973;
Argue et al. 1983). Therefore, if the larval and
juvenile skipjack were available in significant
numbers, then one would expect them to occur in the
diet of the adults.
Their absence in the diet was caused by two possi-
ble results. First, the young remained among the
unidentified portion of the stomach contents;
however, skipjack tuna have distinctive vertebral
characteristics which were probably not discounted
in the analysis (Potthoff and Richards 1970). Second,
the adults did not spawn in the study area. Young
skipjack should be found in the stomach contents of
spawning adults (Argue et al. 1983). Goldberg and
Au^ found no evidence of spawning in skipjack col-
lected from the Brazilian fishery. These results are
consistent with the absence of larval and juvenile
skipjack in the diet of the adults in this study.
The southernmost distribution boundary for larval
skipjack tuna is the 24 °C surface isotherm (Argue et
al. 1983). Matsuura (1982) found no larval skipjack in
ichthyoplankton surveys south of lat. 21 °S in this
area, where temperatures range from 21° to 24°C
(Evans et al. 1981).
^Goldberg, S. R., and D. W. K. Au. 1983. The spawning
schedule of skipjack tuna from southeastern Brazil as determined
from histological examinations of ovaries, with notes on spawning in
the Caribbean. Prepared for the International Skipjack Year Pro-
gram conference of the International Commission for the Conser-
vation of Atlantic Tunas. June 21-25, 1983, Tenerife, Canary
Islands, Spain, 31 p. Manuscript in preparation; Department of
Biology, Whittier College, Whittier, CA 90608.
These results are consonant with those of Argue et
al. (1983); juvenile skipjack tuna were absent from
samples of adult stomachs taken in subtropical south
Pacific waters. The adult skipjack in this investiga-
tion did not feed on their young. The absence of
cannabilism suggests that larvae and juveniles were
not significantly abundant to serve as forage of the
adults, and therefore probably do not occur in this
cooler southern water.
ACKNOWLEDGMENTS
I wish to thank Ronald Rinaldo for organizing the
collection of stomachs from skipjack tuna landed in
Puerto Rico and Brazil. Silvio Jablonski (SUDEPE,
Brazil), Eugene Holzapfel (NMFS, Puerto Rico), and
their employees were responsible for the collection
and shipment of the skipjack tuna stomachs.
Gareth Nelson, Richard Rosenblatt, Kurt Schaef-
fer, and Betsy Stevens assisted in the identification
of the fishes. The euphasiid was identified by Ed-
ward Brinton. Robert Olson assisted in the identifi-
cation of cephalopod beaks. Angeles Alvarino
assisted in the identification of other invertebrates.
Thanks to Andrew Dizon, John Graves, Ronald
Rinaldo, Robert Olson, and Kurt Schaeffer for their
criticisms and suggestions in reviewing this paper.
LITERATURE CITED
Alverson, F. G.
1963. The food of yellowfin and skipjack tunas in the eastern
tropical Pacific Ocean. [In Engl, and Span.] Inter-Am.
Trop. Tuna Comm. Bull. 7:293-396.
Argue, A. W., F. Conand, and D. Whyman.
1983. Spatial and temporal distributions of juvenile tunas from
stomachs of tunas caught by pole-and-line gear in the central
and western Pacific Ocean. Tuna and Billfish Assessment
Programme Technical Report No. 4. South Pacific Commis-
sion, Noumea, New Caledonia.
Batts, B. S.
1972. Food habits of the skipjack tuna. Katsuwomm pelamis,
in North Carolina waters. Chesapeake Sci. 13:193-200.
Dragovich, A.
1969. Review of studies of tuna food in the Atlantic Ocean.
U.S. Fish Wild!. Serv., Spec, Sci. Rep. Fish. 593, 21 p.
1970. The food of skipjack and yellowfin tunas in the Atlantic
Ocean. Fish. Bull., U.S. 68:445-460.
Dragovich, A., and T. Potthoff.
1972. Comparative study of food of skipjack and yellowfin
tunas off the coast of West Africa. Fish. Bull., U.S. 70:1087-
1110.
Evans, R. H., D. R. McLain, and R. A. Bauer.
1981. Atlantic skipjack tuna: influences of mean environmen-
tal conditions on their vulnerability to surface fishing gear.
Mar. Fish. Rev. 43(6):1-11.
HoTTS, H., AND T. Ogawa.
1955. On the stomach contents of the skipjack, Katsuwomis
pelamis. Bull. Tohoku Reg. Fish. Res. Lab. 4:62-82.
385
FISHERY BI'LLETIN: VOL. 83. NO. 3
Kearney, R. E.
1976. Some hypotheses on skipjack (Katsuwonus pelamis) in
the Pacific Ocean. South Pac. Comm., Occas. Pap. 7, 23 p.
Klawe, W. L.
1961. Young scombroids from the waters between Cape Hat-
teras and Bahama Islands. Bull. Mar. Sci. Gulf Caribb. 1 1 :
150-157.
Magnlfson, J. J.
1969. Digestion and food consumption by skipjack tuna (Kat-
suwonus pelamvi). Trans. Am. Fish. Soc. 98:379-392.
Magnuson, J. J., AND J. G. Heitz.
1971. Gill raker apparatus and food selectivity among mack-
erels, tunas, and dolphins. Fish Bull., U.S. 361-370.
Matsuura, Y.
1982. Distribution and abundance of skipjack (Katsuwonus
pelamis) larvae in eastern Brazilian waters. ICCAT/SCRS/
81/70, Coll. Vol. Sci. Pap. Vol. XVII(SCRS-1981), p. 211-213.
Matsuura. Y., K. Nakatani, G. Sato, and S. T. J. Tamassia.
1978. Exploracao e avaliacao de estoque de peixes pelagicos
no sul do Brasil. Relat. Teen. Conv. FINEP/IOUSP, 46
P-
Matsuura, Y., J. C. Amaral, S. T. J. Tamassia, and G. Sato.
1981. Ocorrencia de cardumes de peixes peligicos e a estru-
tura oceanografica da regiao entre Cabo de Sao Tome (RJ) e
Cananela (SP) em janeiro-fevereiro de 1979. Ser. Doc. Teen.
PDP/SUDEPE 36:1-73.
Miller. G. L., and S. C. Jorgenson.
1973. Meristic characters of some marine fishes of the west-
ern Atlantic Ocean. Fish Bull., U.S. 71:301-312.
Nakamura, E. L.
1965. Food and feeding habits of skipjack tuna {Katsiuronus
pelamvi) from the Marquesas and Tuamotu Islands. Trans.
Am. Fish. Soc. 94:236-242.
NisHiKAWA, Y., S. Kikawa. M. Honma, and S. IIeyanagi.
1978. Distribution atlas of lan,-al tuna, billfishes, and related
species. Results of larval surveys by R/V Shunyo-Maru and
Shoyo-Maru, 1956-1975. Far Seas Fish. Res. Lab., S. Ser.,
9:1-99.
PiNKAS, L., M. S. Oliphant, and L. K. Iverson.
1971. Food habits of albacore, bluefin tuna, and bonito in
California waters. Calif. Dep. Fish Game, Fish Bull. 152,
105 p.
Perrin, W. F., R. R. Warner, C. H. Fiscus, and D. B. Holts.
1973. Stomach contents of porpoise, SteTiella spp., and yellow-
fin tuna, Thunnua nlbacares, in mixed species aggregations.
Fish. Bull., U.S. 71:1077-1092.
POTTHOFF, T., AND W. J. RiCHARDS.
1970. Juvenile bluefin tuna, Thunnus thynnus (Linnaeus), and
other scombrids taken by terns in the Dr>' Tortugas, Florida.
Bull. Mar. Sci. 20:389-413.
Suarez-Caabro, J. A., and P. P. Duarte-Bello.
1961. Biologia pesquera del bonito (Katsuwonus pelamis) y la
albacora (Thunnus atlantieus) en Cuba \. Inst. Cub. Invest.
Tecnol. Ser. Estud. Trab. Invest. 15, 151 p.
Wilson, M. A.
1982. The reproductive and feeding behavior of skipjack tuna,
Katsuwonus pelamis, in Papua New Guinea waters. D.P.I.
Fish. Res. Surv. Br., Papua New Guinea, Rep. 82-4, 38 p.
Wolff, G. A.
1981. A beak key for eight eastern tropical Pacific cephalopod
species with relationships between their beak dimensions and
size. Fish. Bull., U.S. 80:357-370.
Zavala-Camin, L. a.
1981 . Habitos alimen tares e distribuicao dos atuns e afins (Os-
teichthyes - Teleostei) e suas relacoes ecologicas com outras
especies pelagicas das regioes Sudeste e Sul do Brasil. Ph.D.
Thesis, Universidade de Sao Paulo, Sao Paulo, Brasil, 237 p.
1982. Datos historicos de areas de crecimiento de listado (Kat-
suwonus pelamis) obtenidos por medio de examen de conten-
ido estomacal de predadores (informe preliminar). ICC AT/
SCRS/82/48, Coll. Vol. Sci. Pap. Vol. XVII (SCRS-1981), p.
209-210.
APPENDIX
Appendix Table 1. — List of prey items and other ingested nnaterials found in ttie stomacfis of 1,041
skipjack tuna caugtit off souttiern Brazil, from October 1981 to December 1982.
NumI
bers
Vol
ume
Occurrence
Prey items
No.
%
mL
%
No.
%
Crustacea
Stomatopoda
12.0
0.003
4.5
0.024
6.0
0.576
Mysidacea
Eucopiidae
220.0
0.057
42.4
0.226
22.0
2.113
Lophogastridae
24.0
0.006
1.7
0.009
3.0
0.288
Isopoda
1.0
0.000
0.1
0.001
1.0
0.096
Flabellifera
7.0
0.002
2.1
0.011
7.0
0.672
Amphipoda
22.0
0.006
1.5
0.008
20
0.192
Gammaridea
16.0
0.004
5.1
0.027
10.0
0.961
Euphausiidae
139.0
0.036
3.9
0.021
15.0
1.441
Euphausia sp.
50.0
0.013
0.6
0.003
1.0
0.096
Euphausia similis
368,632.0
94.785
4.895.3
26.122
172.0
16.523
Stylocheiron sp.
1.0
0000
0.3
0.002
10
0.096
Caridea
3.0
0.001
2.3
0.012
3.0
0.288
Macrura
Scyllaridae
1.0
0000
0.2
0.001
1.0
0.096
Unid. Ptiyllosoma larvae
1.0
0.000
0.1
0001
1.0
0.096
386
ANKKNBRANnT: FOOD H AMITS OF SKIIMA( 'K Tl'NA
APPENDIX Table ^. — Continued.
Numbers
Volume
Occurrence
Prey items
No.
%
mL
%
No.
%
Brachyura
5.0
0.001
0.7
0.004
1.0
0096
Portunidae
1.0
0.000
0.1
0.001
1.0
0.096
Unid. megalops
102.0
0.026
32.0
0.171
27.0
2.594
Unid zooea
555.0
0.143
30.2
0.161
24.0
2,305
Unid Decapoda
7.0
0.002
0.6
0.003
2.0
0,192
Unid. Crustacea
96.0
0.025
11.0
0.059
26.0
2.498
Mollusca
Gastropoda
1.0
0.000
0.1
0.001
1.0
0.096
Cavolina sp.
101.0
0.026
6.0
0.032
7.0
0.672
Cephalopoda
Teuthoidea
4.0
0.001
26.0
0.139
4.0
0.384
Thysanoteuthldae
2.0
0.001
10.0
0.053
1.0
0.096
Ommastrephidae
35.0
0.009
55.1
0.294
18.0
1.729
Loliginidae
2.0
0.001
10.5
0.056
2.0
0.192
Histloteuthidae
1.0
0.000
1,0
0.005
1.0
0.096
Onychoteuthidae
13.0
0.003
6.0
0.032
2.0
0.192
Octopoda
Argonautidae
Argonauta sp.
20.0
0.005
75.9
0.405
11.0
1.057
Unid. Cephalopoda
4.0
0.001
1.3
0.007
3.0
0.288
Insecta
Coleoptera
2.0
0.001
2.0
0.011
2.0
0.192
Siphonophora
1.0
0.000
0.9
0.005
1.0
0.096
Algalmidae
8.0
0.002
6.6
0.035
8.0
0.768
Pisces
Gonostomatidae
Maurolicus muelleri
13,438.0
3.455
8,619.3
45.994
181.0
17.387
Synodontidae
8.0
0.002
16.0
0.085
3.0
0.288
Paralepididae
1.0
0.000
0.5
0.003
1.0
0.096
IVIyctophidae
43.0
0.011
62.3
0.332
5.0
0.480
Exocoetidae
2.0
0.001
2.0
0.011
2.0
0.192
Exocoetus volitans
1.0
0.000
56.0
0.299
1.0
0.096
Scomberesocidae
Scomberesox saurus
8.0
0.002
105.0
0.560
6.0
0.576
Belonidae
2.0
0.001
5,0
0.027
2.0
0.192
Macrorhamphosidae
5.0
0.001
6.9
0.037
4.0
0.384
Sygnathidae
1.0
0.000
1.0
0.005
1.0
0.096
Holocentridae
3.0
0.001
4.0
0.021
1.0
0.096
Holocentrus sp.
3.0
0.001
9.0
0.048
1.0
0.096
Carangidae
1.0
0.000
1.0
0.005
1,0
0.096
Selene vomer
8.0
0.002
17.0
0.091
8.0
0.768
Decapterus punctatus
2.0
0.001
46.0
0.245
2.0
0.192
Caranx ruber
70.0
0.018
360.0
1,921
17.0
1.633
Mullidae
11.0
0.003
25.0
0.133
6.0
0.576
Sconnbridae
16.0
0.004
2.5
0.013
3.0
0.288
Auxis thazard
474.0
0.122
223.7
1.194
23.0
2.209
Scomber japonicus
1,474.0
0.379
978.7
5.223
77.0
7.397
Sarda sarda
81.0
0.021
127.0
0.678
8.0
0.768
Gempylidae
176,0
0.045
100.7
0.537
20.0
1.921
Thyrsitops lepidopoldes
2,617.0
0.673
2,348.4
12.532
54.0
5.187
Trichiuridae
11.0
0.003
12.0
0.064
4.0
0.384
Benthodesmus sp.
19.0
0.005
80.9
0.432
8.0
0.768
Unid. Perciforms
24.0
0.006
63.7
0.340
16.0
1.537
Balistidae
1.0
0.000
5.0
0.027
1.0
0.096
Monacanthidae
27.0
0.007
198
0.106
19.0
1.825
Ostraciidae
1.0
0.000
0.5
0.003
1.0
0.096
Molidae
Ranzania sp.
3.0
0.001
13.0
0.069
1.0
0.096
Triglidae
1.0
0.000
1.0
0.005
1.0
0.096
Peristedion sp.
1.0
0.000
1.0
0.005
1.0
0.096
Unid. fish
289.0
0.074
163.5
0.872
94.0
9.030
Unid. material
1.0
0000
26.4
0.141
5.0
0.480
Empty
436.0
41.882
Total
388,912.0
18,739.9
1,041.0
387
FISHERY BULLETIN: VOL. 83, NO. 3
Appendix Table 2.— List of prey items and othier ingested materials found in the stomacfis of skip-
jack tuna caught
during (
Juarter \.
Prey items
Numbers
Volume
Occurrence
No.
%
mL %
No. %
Crustacea
f^ysidacea
Eucopiidae
Lophogastridae
Isopoda
Flabellifera
Amphipoda
Euphausiidae
Euphausia simills
Caridea
Brachyura
Unid. megalops
Unid. zooea
Unid. Decapoda
Unid. Crustacea
IVIollusca
Gastropoda
Pteropoda
Cavolina
Cephalopoda
Teuthoidea
Thysanoteuthidae
Ommastrephidae
Loliginidae
Octopoda
Argonautidae
Argonauta sp.
Insecta
Coleoptera
Pisces
Gonostomatidae
Maurolicus muelleri
Belonidae
Holocentridae
Carangidae
Selene vomer
Mullidae
Scombridae
Auxis thazard
Scomber /aponicus
Gempylidae
Unid. Perciforms
Monacanthidae
Ostraciidae
Triglidae
Peristedior) sp
Unid. fish
Unid. material
Total
112.0
0.0076
19.0
0.013
1.0
0.001
1.0
0.001
20.0
0,014
49.0
0.033
44,070.0
97.624
1.0
0.001
80.0
0.054
549.0
0.372
4.0
0.003
47,0
0,032
68.0
0.046
9.3
0.253
1.5
0.041
0.1
0.003
0.1
0.003
0.5
0.014
2.3
0.063
25.9
57.878
0.5
0.014
22.6
0.615
28.6
0.779
0.1
0.003
8.3
0.226
2.2
0.060
8.0
2.658
2.0
0.664
1.0
0.332
1.0
0.332
1.0
0.332
4.0
1.329
34.0
11.296
1.0
0,332
17.0
5,648
19.0
6.312
1.0
0.332
13.0
4.319
1.0
0.332
2.0
0.001
2.0
0.054
2,0
0.664
2.0
0.001
10.0
0.272
1.0
0.332
5.0
0.003
1.1
0.030
2.0
0.664
1.0
0.001
8.0
0.218
1.0
0.332
2.0
0.001
0.3
0.008
2.0
0.664
1.0
0.001
1.0
0.027
1.0
0.332
1,346.0
0.912
838.0
22.815
29.0
9.635
1.0
0.001
3.0
0.082
1.0
0.332
3.0
0.002
4.0
0.109
1.0
0.332
6.0
0.004
9.0
0.245
6.0
1.993
2.0
0.001
8.0
0.218
1.0
0.332
15.0
0.010
1,5
0.041
2.0
0.664
4270
0.289
189.7
5.165
21.0
6.977
504.0
0.342
225.2
6.131
22.0
7.309
76.0
0.051
48.5
1.320
11.0
3.654
9.0
0.006
7.0
0.191
5.0
1.661
13.0
0.009
9.5
0.259
8.0
2.658
1,0
0.001
0.5
0.014
1.0
0.332
1,0
0.001
1.0
0.027
1.0
0.332
1,0
0.001
1.0
0.027
1.0
0.332
137,0
0.093
76.5
2.083
35.0
11.628
1,0
0.001
26.3
0.716
4.0
1.329
147.577,0
3,673.1
301.0
388
ANKKNHRANliT: FOOD HAHITS OK SKIIMACK Tl'NA
Appendix Table 3. — List of prey items and other ingested nnaterials found in the stomachs of skip-
jack tuna caught during Quarter II.
Numbe
rs
Volume
Occurrence
Prey items
No.
%
mL
%
No.
%
Crustacea
Stomatopoda
1.0
0.001
1.0
0.016
1.0
0.345
Mysidacea
Eucopiidae
97.0
0.055
31.9
0.508
9.0
3.103
Lophogastridae
5.0
0.003
0.2
0.003
1.0
0.345
Isopoda
Flabellifera
2.0
0.001
1.5
0.024
2.0
0.690
Amphipoda
2.0
0.001
1.0
0.016
1.0
0.345
Gammaridea
6.0
0.003
0.4
0.006
3.0
1.034
Euphausiidae
2.0
0.001
0.2
0.003
2.0
0.690
Euphausia similis
171.843.0
97.352
2,104.3
33.485
61.0
21.034
Caridea
1.0
0.001
0.8
0.013
1.0
0.345
Macrura
Scyllaridae
1.0
0.001
0.2
0.003
1.0
0.345
Brachyura
Unid. megalops
1.0
0.001
0.5
0.008
1.0
0.345
Unid. zooea
1.0
0.001
0.2
0.003
1.0
0.345
Unid. Decapoda
3.0
0.002
0.5
0.008
1.0
0.345
Unid. Crustacea
30.0
0.017
1.2
0.019
2.0
0.690
Mollusca
Gastropoda
Pteropoda
Cavolina sp.
33.0
0.019
3.8
0.060
6.0
2.069
Cephalopoda
Teuthoidea
Ommastrephidae
6.0
0.003
8.5
0.135
5.0
1.724
Onychoteuthidae
13.0
0.007
6.0
0.095
2.0
0.690
Siphonophora
Algalmldae
8.0
0.005
6.6
0.105
8.0
2.759
Pisces
Gonostomatidae
Maurolicus muelleri
4,287.0 ,
2.429
3,548.0
56.458
38.0
13.103
Synodontidae
8.0
0.005
16.0
0.255
3.0
1.034
Myctophidae
24.0
0.014
61.3
0.975
4,0
1.379
Sygnathidae
1.0
0.001
1.0
0.016
1.0
0.345
Carangidae
Selene vomer
2.0
0.001
8.0
0.127
2.0
0.690
Decapterus punctatus
2.0
0.001
46.0
0.732
2.0
0.690
Caranx ruber
70.0
0.040
360.0
5.729
17.0
5.862
Scombridae
Auxis t hazard
46.0
0.026
30.0
0.477
1.0
0.345
Scomber japonicus
8.0
0.005
6.0
0.095
2.0
0.690
Unid. Perciforms
1.0
0.001
12.0
0.191
1.0
0.345
Balistidae
1.0
0.001
5.0
0.080
1.0
0.345
Monacanthidae
4.0
0.002
4.1
0.065
3.0
1.034
Unid. fish
9.0
0.005
18.1
0.288
6.0
2.069
Total
176,518.0
6,284.3
290.0
389
FISHERY BULLETIN: VOL. H3, NO. '.i
Appendix table 4.— List of prey items and other ingested nnaterials found in ttie stomachs of
skipjack tuna caught during Quarter IN.
Num
bers
Vol
ume
Occurrence
Prey items
No.
%
mL
%
No.
%
Crustacea
Mysidacea
Eucopiidae
10.0
0.046
0.8
0.020
4.0
1.843
Isopoda
Flabellifera
2.0
0.009
0.3
0.007
2.0
0.922
Euphausiidae
88.0
0.401
1.4
0.034
9.0
4.147
Euphausia sp.
50.0
0.228
0.6
0.015
1.0
0.461
Euphausia similis
15,414.0
70.236
196.3
4.796
30.0
13.825
Unid. Crustacea
5.0
0.023
0.4
0.010
4.0
1.843
Mollusca
Cephalopoda
Teuthoidea
1.0
0.005
3.0
0.073
1.0
0.461
Pisces
Gonostomatidae
Maurolicus muellerl
6,239.0
28429
3.289.2
80.369
74.0
34.101
Exocoetidae
2.0
0.009
2.0
0.049
2.0
0.922
Exocoetus volitans
1.0
0.005
56.0
1.368
1.0
0.461
Macrorhamphosidae
2.0
0.009
2.9
0.071
2.0
0.922
Carangidae
1.0
0.005
1.0
0.024
1.0
0.461
Mullidae
6.0
0.027
9.0
0.220
3.0
1.382
Scombridae
Scomber laponicus
45.0
0.205
374.0
9.138
8.0
3.687
Sarda sarda
6.0
0.027
4.0
0.098
2.0
0.922
Trichiuridae
11.0
0.050
12.0
0.293
4.0
1.843
Benthodesmus sp.
19.0
0.087
80.9
1.977
8.0
3.687
Unid. Perciforms
4.0
0.018
35.0
0.855
3.0
1.382
fVlonacanthidae
1.0
0.005
1.0
0.024
1.0
0.461
Unid. fish
39.0
0.178
22.8
0.557
21.0
9.677
Total
21,946.0
4,092.6
217.0
390
ANKKNKKANDT: FOOD HAHITS OK SKIIMACK TINA
Appendix table 5— List of prey items and other ingested materials found in tfie stomachis of skip-
jack tuna caught during Quarter IV.
Num
bers
Volume
Occurrence
Prey items
No.
%
mL
%
No.
%
Crustacea
Stomatopoda
11.0
0.026
3.5
0.075
5.0
2.146
Mysidacea
Eucopiidae
1.0
0.002
0.4
0.009
1.0
0.429
Isopoda
Flabellifera
2.0
0.005
0.2
0.004
2.0
0.858
Amphipoda
Gammaridea
10.0
0.023
4.7
0.100
7.0
3.004
Euphausiidae
Euphausia similis
37,305.0
87.017
468.8
9.996
47.0
20.172
Stylochelron sp.
1.0
0.002
0.3
0.006
1.0
0.429
Caridea
1.0
0.002
1.0
0.021
1.0
0.429
Macrura
Scyllaridae
Unid. Phyllosoma larvae
1.0
0.002
0.1
0.002
1.0
0.429
Erachyura
5.0
0.012
0.7
0.015
1.0
0.429
Portunidae
1.0
0.002
0.1
0.002
1.0
0.429
Unid. megalops
21.0
0.049
8.9
0.190
9.0
3.863
Unid. zooea
5.0
0.012
1.4
0.030
4.0
1.717
Unid. Crustacea
14.0
0.033
1.1
0.023
7.0
3.004
Mollusca
Gastropoda
Pteropoda
Cavoliniidae
1.0
0.002
0.1
0.002
1.0
0.429
Cephalopoda
Teuthoidea
1.0
0.002
21.0
0.448
1.0
0.429
Ommastrephidae
24.0
0.056
455
0.970
11.0
4.721
Loliginidae
1.0
0.002
2.5
0.053
1.0
0.429
Histioteuthidae
1.0
0.002
1.0
0.021
1.0
0.429
Octopoda
Argonautidae
Argonauts sp.
18.0
0.042
75.6
1.612
9.0
3.863
Unid. Cephalopoda
4.0
0.009
1.3
0.028
3.0
1.288
Insecta
Coleoptera
1.0
0.002
1.0
0.021
1.0
0.429
Siphonophora
1.0
0.002
0.9
0.019
1.0
0429
Pisces
Gonostomatidae
Mauroltcus muelleri
1.566.0
3.653
944.1
20.130
40.0
17.167
Paralepididae
1.0
0.002
0.5
0.011
1.0
0.429
Myctophidae
19.0
0.044
1.0
0.021
1.0
0.429
Scomberesocidae
Scomberesox saurus
8.0
0.019
105.0
2.239
6,0
2.575
Belonidae
1.0
0.002
2.0
0.043
1.0
0.429
Macrorhamphosidae
3.0
0.007
4.0
0.085
2.0
0.858
Holocentridae
Holocentrus sp.
3.0
0.007
9.0
0.192
1.0
0.429
Mullidae
3.0
0.007
8.0
0.171
2.0
0.858
Scombridae
1.0
0.002
1.0
0.021
1.0
0.429
Auxis thazard
1.0
0.002
4.0
0.085
1.0
0.429
Scomber japonicus
917.0
2.139
373.5
7.964
45.0
19.313
Sard a sard a
75.0
0.175
123.0
2.623
6.0
2.575
Gempylidae
100.0
0.233
52.2
1.113
9.0
3.863
Thyrsi tops lepldopoldes
2,617.0
6.104
2,348.4
50.074
54.0
23.176
Unid. Percitorms
10.0
0.023
9.7
0.207
7.0
3.004
fVlonacanthidae
9.0
0.021
5.2
0.111
7.0
3.004
Molidae
1.0
0.001
0.5
0.014
1.0
0.332
Ranzania sp.
3.0
0.007
13.0
0.277
1.0
0.429
Unid. fish
104.0
0.243
46.1
0.983
32.0
13.734
Unid. material
0.0
0.000
0.1
0.002
1.0
0.429
Total
42,871.0
4,689.9
233.0
391
FISHERY BULLETIN: VOL. 83, NO. 3
APPENDIX Table 6.— Mean volumetric ratio of selected food items of skipjack tuna divided into 5 cm length
groups for all months. Data are 7 ± SD with (n) in parentheses. Range is 0-100%.
Length cm
Other
Other
Euphausia
Maurolicus
Scomber
Thyrsitops
(n)
fish
crustaceans
similis
muelleri
laponicus
lepidopoides
45.0-49.9(67)
9.51 ±22.5
9.51 ±25.4
42.50 ±48.1
10.35 ±29.5
8.57 ±23.6
16.64 ±36.4
50.0-54.9(155)
10.53 ±27.7
12.62 ±30.9
26.73 ±43.6
13.99 ±33.4
12.44 ±29.5
20.05 ±38.5
55.0-59.9(162)
24.81 ±39.4
11.80 ±29.5
20.40 ±39.5
29.49 ±43.6
5.62 ±19.6
2.70 ±14.2
60.0-64.9(147)
23.48 ±39.2
8.03 ±24.7
18.83±36.5
42.90 ±48.2
2.12±12.2
—
65.0-69.9(55)
42.80 ±47.6
12.43±31.7
4.73±18.7
32.18 ±45.9
0.27 ±2.0
—
70.0-74.9(13)
48.30 ±48.1
9.88 ±27.9
8.57 ±21.9
23.36 ±43.7
2.20 ±79.2
—
75.0-79.9(4)
47.50 ±55.0
27.50 ±48.6
—
25.00 ±50.0
—
—
Total (603)
18.80 ±35.5
10.96 ±28.6
22.22 ±40.0
26.73 ±42.8
6.24±21.1
10.34 ±27.9
APPENDIX Table 7. — Mean volumetric ratio of selected food items of skipjack tuna divided
into 5 cm length groups for Quarter I. Data are 7 ± SD with (n) in parentheses. Range is
0-100%.
Length cm
Other
Other
Euphausia
Mauroiicus
Scomber
in)
fish
crustaceans
similis
muelleri
laponicus
45.0-49.9(12)
28.70 ±33.4
35.15 ±42.5
9.18 ±28.7
7.48 ±25.9
13.89 ±38.4
50.0-54.9(53)
19.87 ±36.8
29.64 ±43.5
24.48 ±43.3
6.09 ± 19.6
16.12±33.5
55.0-59.9(45)
30.23 ±40.9
17.69 ±33.9
20.81 ±38.9
22.96 ±38.1
7.98 ±25.2
60.0-64.9(36)
34.79 ±44.1
16.96 ±35.4
20.14 ±38.9
20.92 ±40.1
19.84 ±46.5
65.0-69.9(4)
48.61 ±56.2
28.24 ±47.9
—
—
3.71 ±7.4
70.0-74.9(3)
91.67± 14.4
8.33 ± 14.4
—
—
—
75.0-79.9(2)
—
—
—
—
—
Total (155)
29.55 ±41.0
23.47 ± 38.9
19.80 + 38.9
14.18±32.1
10.08 ±27.3
Appendix Table 8.— Mean volumetric ratio of selected food items of skipjack tuna divided
into 5 cm length groups for Quarter II. Data are r ± SD with (n) in parentheses. Range is
0-100%.
Length cm
Other
Other
Euphausia
Maurolicus
Scomber
(n)
fish
crustaceans
similis
muelleri
laponicus
45.0-49.9(26)
1.65 ±8.4
5.00 ±20.3
76.92 ±43.0
15.38 ±36.8
—
50.0-54.9(12)
5.82 ± 11,5
14.72 ±33.0
65.71 ±48.6
—
—
55.0-59.9(35)
20.89 ±38.7
18.13±36.4
35.65 ±49.9
14.71 ±33.9
0.14 ±0,80
60.0-64.9(45)
16.33 ±36.2
4.67 ± 18.5
28.92 ±45.7
45.54 ±49,7
0.32 ±2.1
65.0-69.9(23)
54.07 ±49.1
—
4.49 ±20.8
30.29 ±46.8
—
Total (141)
20.02 ±38.1
8.16 + 25.2
38.32 ±48.6
25.96 ±43.3
0.14±1.3
Appendix Table 9. — Mean volumetric ratio of selected food items of skipjack tuna divided
into 5 cm length groups for Quarter III Data are r ± SD with (n) in parentheses. Range is
0-100%.
Length cm
Other
Other
Euphausia
Maurolicus
Scomber
in)
fish
crustaceans
similis
muelleri
laponicus
45.0-49.9(4)
25.81 ±49.5
25.00 ±50.0
24.19 ±48.4
25.00 ±50.0
50.0-54.9(27)
11.17±32.0
1.24 ±6.4
11.21 ±32.0
61.56 ±48.5
14.81 ±36.2
55.0-59.9(36)
24.88±41.3
9.22 + 27.9
3.67 ±16.2
59.05 ±47.0
3.17±16.8
60.0-64.9(31)
24.09 + 40.5
3.39 ± 17.9
16.51 ±29.9
53.76 ±46.6
2.26 ± 12.6
65.0-69.9(17)
31.80 ±46.4
17.65 ±39.3
3.89 ±9.8
46.67 ±48.8
—
70.0-74.9(5)
31.27 ±45.5
—
8.00 ± 17.9
60.73 ±53.8
—
Total (120)
22.87 + 40.1
6.42 ± 23.6
9.6 ±25.5
55.40 ±47.39
5.70 ±22.7
392
ANKKNBRANnTFOdDHAHrrsnFSKnMACKTUNA
Appendix Table 10— Mean volumetric ratio of selected food Items of skipjack tuna divided into 5 cm length
groups tor Quarter IV. Data are r ± SD with (n) in parentheses. Range is 0-100%.
Length cm
Other
Other
Euphausia
Maurolicus
Scomber
Thyrsitops
in)
fish
crustaceans
si mi lis
muelleri
japonicus
lepidopoides
45.0-49.9(25)
5.86 ±13.8
3.43+11.0
25.49 ±39.6
4.26 ± 16.9
12.30±25.1
44.60 ±48.4
50.0-54.9(63)
3.30 ± 13.4
2.77 ±13.0
27.84 ±43.4
2.91 ± 16.3
10.69 + 25.1
49.33 ±47.0
550-59.9(46)
22.45 ±37.5
3.25 ±15.3
21.48 ±40.2
24.01 ±42.9
9.40 ±22.5
9.49 ±25.7
60.0-64.9(35)
20.51 ±35.4
7.29 ±22.1
6.55 ± 19.5
52.48 ±49.9
1.71 ±85.6
—
65.0-69.9(11)
34.11 ±44.1
24.59 ±40.2
8.26 ±27.4
25.45 ±43.9
—
—
70.0-74.9(5)
39.31 ±53.8
20.69 ±44.4
14 29±31.9
—
5.71 ± 12.8
—
75.0-79.9(2)
45.00 ±63.6
5.00 ±7.1
—
50.0 ±70.7
—
—
Total (187)
14.80 ±16.5
5.6 ±19.5
29.17 + 37.8
19.31 ±38.9
8.03±21.2
24.91 ±27.7
393
STOMACH CONTENTS OF
YOUNG SANDBAR SHARKS, CARCHARHINUS PLUMBEUS,
IN CHINCOTEAGUE BAY, VIRGINIA'
Robert J. Medved,^ Charles E. Stillwell,^ and
John J. Casey»
ABSTRACT
nurinp the summer of \WA the stcmiach contents of 414 sandbar sharks captured by j^ll nets, and nnl and
reel fishing gear in Chincoteague Bay, Virginia, were examined. The blue crab, CaUinectes mpidui<, occur-
red in 67.4% of the stomachs and Atlantic menhaden, Brevoortia tyrannus, occurred in 13.3% of the
stomachs. Other species of small crustaceans and fishes were found in < 6.0% of the stomachs, and 17.9%i of
the stomachs were empty. Data collected concerning the amount, stage of digestion, and number of food
items in the stomachs indicated that feeding occurred during relatively short periods of time separated by
long pericKis during which food was digested and no additional food was consumed. Sharks caught in gill
nets were found to be in various stages of the feeding cycle and were more representative of the entire
population than those caught by rod and reel. In the stomachs of these sharks, crustaceans accounted for
nearly twice as much of the mean weight of food as did fish. The mean quantity of food in the stomachs was
0.96% of body weight (BW) and the maximum quantity was 5.28% of BW. The quantity of food in all
stomachs was significantly less than the estimated maximum stomach capacity (13.0% BW). Sharks caught
between 0130 and 0430 were found to contain considerably more food in their stomachs than sharks caught
during other times of the day. The data collected from this study when combined with information concern-
ing gastric evacuation will provide the basis for food consumption estimates in this species.
Traditionally the management of commercially
valuable fisheries has been based on single-species
production models and the concept of maximum sus-
tainable yield (Hennemuth 1979). Although general-
ly accepted as an objective of management, the esti-
mation and application of maximum sustainable yield
have not provided satisfactory results and have, in
fact, led to significant declines of some traditional
and highly valued fisheries (Edwards and Henne-
muth 1975; Hennemuth 1977; Holt and Talbot
1978). The poor results of single-species models in
allocating fishing quotas may be due in part to the
fact that they assume no interactions of the target
species with other components of the ecosystem. In
recent years it has become clear that this assumption
is unrealistic and that variables such as competition,
predation, and abiotic factors should be considered in
any assessment of fishery productivity and potential
yields to man. It has been pointed out(Gulland 1978,
1983; Mercer 1982) that the future success of our
iMARMAP Contribution No. MED/NEFC 84-02.
^University of Rhode Island, Graduate School of Oceanography,
Narragansett, RI; present address: Northeast Fisheries Center
Narragansett Laboratory, National Marine Fisheries Service,
NOAA, South Ferry Road, Narragansett, RI 02882.
^Northeast Fisheries Center Narragansett Laboratory, National
Marine Fisheries Service, NOAA, South Ferry Road, Narragansett,
RI 02882.
attempts at managing fishery resources will depend,
to a large extent, on our ability to develop multi-
species production models that adequately account
for interactions among species. An important compo-
nent of these models is predator-prey interactions. In
fact, collection of data on the diets of the major
predators is considered absolutely necessary for the
progress of multispecies assessment techniques
(Hennemuth 1980^; Mercer 1982). Considering their
position as one of the most abundant apex predators
in the sea, predation by sharks undoubtedly plays a
major role in the exchange of energy in the marine
environment. In fact, a study by Jones and Geen
(1977) has indicated that the spiny dogfish, Squalus
acanthias, in British Columbia waters annually con-
sumes over 5 times the commercial catch of herring
and up to 44% of the total stock. The impact that
sharks have on commercial fisheries can only be
determined by knowing the diversity of prey items
and the biomass of each consumed. While numerous
publications on sharks incorporate lists of items
found in their stomachs, very little is known about
daily ration and the amounts of food consumed an-
nually.
■•Hennemuth, R. C. 1980. Research needs for multispecies
fisheries. Office of Technology Assessment Workshop, Seattle,
WA., 21-23 April.
Manuscript accepted October 1984.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
395
FISHERY BULLETIN: VOL. 83, NO. 3
In most investigations the food consumption of
fishes has been studied by methods that involve
laboratory techniques to estimate various
parameters relating to growth, metabolism, diges-
tion, and excretion (reviews by: Davis and Warren
1971; Mann 1978). These methods, however, are of
limited value for fishes such as sharks that are dif-
ficult to maintain in captivity. An alternate method
for determining food intake that can be applied to
fishes in the wild has been successfully used in
several studies (Bajkov 1935; Swenson and Smith
1973; Eggers 1977; Thorpe 1977; Elliott and
Persson 1978; Jobling 1981; Stillwell and Kohler
1982; Durbin et al. 1983). This approach requires in-
formation concerning the quantity of food found in
the stomachs of fishes sampled at regular intervals
over 24-h periods and the rate at which food is evacu-
ated from the stomach. The objective of the present
study was to obtain the quantitative stomach content
data needed to use this approach to estimate the
daily food ration of the sandbar shark, Carcharhinus
plumbeiis. The sandbar shark was selected for this
study because it is one of the few sharks for which
gastric evacuation data are available (Medved in
press). It is also an abundant, widely distributed
shark (Springer 1960; Casey 1976) known to feed on
commercially valuable species (Medved and Marshall
1981). In addition, it is a member of a large family of
sharks (Carcharhinidae) and data collected for this
species will provide the basis for making preliminary
estimates of food consumption for the other
members of the family.
METHODS
During the summer of 1983, young sandbar sharks
were collected from Chincoteague Bay, VA, for
stomach content analysis. The study area is located
within the summer distribution of this species and
supports a relatively large number of young sandbar
sharks from early June through September. The bay
is about 40 km long and 8 km wide at its widest
point, and the average water depth is 2 m. A tidal
inlet connects the bay with the Atlantic Ocean, and
the tidal range varies from 0.75 to 1.50 m. The area
is also characterized by strong tidal currents, vast
salt marshes, and brackish to seawater salinities.
A 4.9 m outboard motor boat was used as a fishing
platform, and sharks were caught using monofila-
ment gill nets and rod and reel fishing gear. The gill
nets were 91m long, 1.8 m deep, and had a stretched
mesh size of 10.8 cm. They were anchored at both
ends and were buoyed so the foot rope touched the
bottom. Net retrieval was made every 1 to 2 h. The
fishing rods were equipped with Penn^ reels of 3/0
size, and the terminal tackle consisted of two wire
leaders, each with a 4/0 fishing hook baited with
squid. The hooks were set 1 m off the bottom. Both
types of gear were used during all hours of the day.
Upon capture each shark was brought into the boat
where it was sexed, measured, and weighed. The
sharks were then cut open and the stomach contents
were removed and stored on ice in plastic bags.
In the laboratory each food item was identified to
species and a length measurement was made when
possible. Each item in the stomach was also assigned
a stage-of-digestion value ranging from 1 to 6 with a
higher number indicating a greater extent of diges-
tion. The stage-of-digestion scale was based on a
gastric evacuation study (Medved in press) in which
sandbar sharks were fed preweighed meals of either
blue crab, Callinectes sapidus, or Atlantic menhaden,
Brevoortia tyrannus, and were maintained in an
enclosure constructed in the natural environment.
The range of water temperatures in the enclosure
(22.0°-30.0°C) was close to that recorded during the
present study (20.0°-27.3°C). The sharks were
sacrificed at various time intervals after feeding, and
the food remains were weighed and described. The
food item descriptions were used to arbitrarily esta-
blish six stages of digestion that were each one-sixth
of the total evacuation time. Each stage of digestion
was about 12 h long for crustacean prey and 15 h
long for fish prey. After identification of food items
and assignment of digestion values, the stomach con-
tents of each shark were separated into fish and crus-
tacean components that were weighed to 0.01 g
after draining off excess water. Each sample was
then dried at 80 °C to constant weight (about 72 h)
and again weighed to 0.01 g.
RESULTS
During the study 414 sharks were captured for
stomach content analysis. The numbers of sharks
caught by each fishing method and during various
time periods of the day are summarized in Table 1 .
The number of male and female sharks collected was
nearly equal (210 and 204 respectively), and they
ranged in size from 40.0 to 80.0 cm fork length (FL)
(x = 56.1, SD = 6.8). Body weights were obtained
from 369 (89.1%) of these sharks, and ranged from
720.0 to 5,690.0 g (x = 1,885.5, SD = 738.8). The
body weight of the sharks not weighed was esti-
mated from a regression equation derived from the
^Reference to trade names does not imply endorsement by the Na-
tional Marine Fisheries Service, NOAA.
396
MKI)\ Kli KTAL : STOMACH CONTENTS OF SANDBARSHARKS
Table 1. — Number of sharks caught for stomach
content analysis during different time intervals
and by the two capture methods.
Time interval
Rod and reel Gill net Total
2230-0130
0130-0430
0430-0730
0730-1030
1030-1330
1330-1630
1630-1930
1930-2230
Total
19
11
20
21
27
39
18
23
178
33
27
20
27
27
39
30
33
236
52
38
40
48
54
78
48
56
414
animals that were measured and weighed: Wt =
0.0123 (FL)-^'^'" (v = 369, R- = 0.97). Water
temperature during the fishing periods ranged from
20.0° to 27.3°C {n = 172, x = 25.1) but 90% of the
temperatures were between 23.9° and 26.4° C.
Fifteen different food types were identified in the
stomachs (Table 2). A relatively large number of
stomachs (« = 74, 17.9%) were empty, and unidenti-
fiable fish remains occurred in others (n = 21, 5.1%).
The blue crab was the most frequently occurring
food item and was found in 279 (67.4%) of the
stomachs examined and in 82.1% of the stomachs
containing food. Of the food remains that could be
positively identified as individual blue crabs (n =
309), 88.0% of the crabs had recently molted and
were soft. The crabs that could be measured ranged
in size from 1.0 to 14.0 cm between the two points of
the carapace (n = 136, x = 7.4). Although exact
numbers were difficult to determine, it appeared
that less than half of the blue crabs were consumed
whole. The only other prey frequently found was the
Atlantic menhaden, which occurred in 55 (13.3%) of
the stomachs examined and in 16.2% of the
stomachs with food. Of the 61 cases where it was
possible to determine if the fish was consumed whole
or in part, 28 (45.9%) of the menhaden were whole
and ranged in size from 5 to 10 cm total length (TL)
(x = 7.3). The estimated sizes of the partially eaten
menhaden ranged from 5 to 17 cm TL (x = 8.6). All
other prey items were found in < 6.0% of the
stomachs examined.
The distributions of stage-of-digestion values
assigned to the food items in the stomachs of sharks
caught by the two different fishing methods are
shown in Figure 1. The distribution for sharks
caught by rod and reel indicated that 71.8% of the
food items were in either the first or last stage of
digestion. In contrast, food items in the stomachs of
sharks caught by gill nets were divided more evenly
among all the stages of digestion. The two capture
methods also differed in the proportion of sharks
Table 2— Stomach contents found in a sample of 414 sand-
bar sharks.
Stomach content
No. of
stomachs
found in
Percent of
stomachs
found in
Blue crab, Call nee ties sapidus
Empty
Atlantic menhaden, Brevoortia
tyrannus
Summer flounder, Paralichthys
dentatus
Unidentified fish
IVIantis shrimp, Squilla emprisa
American eel, Anguilla rostrata
Spot. Leiostomus xanthurus
Atlantic silverside, Menidia
menldia
Smooth dogfish, Mustelus canis
Northern pipefish. Syngnathus
fuscus
Anchovy, Anchoviella mitchilll
Squid, Loligo pealei
Bluefish, Pomatomus saltatrix
Calico crab, Ovalipes ocellatus
Mummichog, Fundulus
heteroclitus
Northern seahorse.
Hippocampus hudemius
279
74
55
24
21
18
15
14
9
7
6
5
5
3
1
1
1
67.4
17.9
13.3
5.8
5.1
4.4
3.6
3.4
2.2
1.7
1.5
1.2
1.2
0.7
0.2
0.2
0.2
caught with empty stomachs. The percentage of the
178 sharks caught by rod and reel with empty
stomachs (22.5%) was significantly higher than that
found for the 236 sharks caught by gill nets (14.4%;
^-test, P = 0.015).
Of the 414 stomachs examined, 203 contained a
single food item. A stage-of-digestion value of 5 or 6
was assigned to 89 (43.8%) of these items, indicating
that many sharks went at least the time equivalent of
5 stage-of-digestion units between meals (48 to 60 h
for crustacean prey or 60 to 75 h for fish prey).
Multiple food items were found in 137 stomachs.
The difference between the stage-of-digestion values
NET ROD-REEL
^ 50-, N = 338 N = 195
iiiiiii Li
1 2 3 4 5 6
2 3 4 5 6
STAGE OF DIGESTION
FiGt_iRE 1.- Distributions of stage-of-digestion values assigned to
food items present in the stomachs of sharks caught with gill net
and rod and reel.
397
FISHERY BULLETIN: VOL. 83. NO. 3
of the first and last eaten food items within each
stomach was calculated to assess the amount of time
that passed during consumption of multiple item
meals. In 19 stomachs a food item in the sixth stage
of digestion and one in the first stage of digestion
were found. In these cases a time equivalent of 5
stage-of-digestion units had passed between con-
sumption of the two food items, and since a stomach
containing an item in stage 6 of digestion would be
relatively empty, the two food items were considered
to represent two different meals. Excluding the
above 19 stomachs from analysis, the mean differ-
ence between the stage-of-digestion values of the
first and last eaten food items was calculated for
stomachs containing from 2 to 5 items (Table 3). The
overall mean difference was 0.60 stage-of-digestion
units indicating that multiple food items in the
stomachs were in similar stages of digestion.
The quantity of food in each stomach examined
was measured on a wet weight and drj' weight basis.
Excluding empty stomachs from analysis, the total
Table 3.— Number of stomachs for wfilchi tfie stage-of-
digestion value of the first eaten food item minus the stage-
of-digestion value of the last eaten food item was equal to
the given difference. The data are broken down into groups
based on the number of food Items present in the stomachs.
Stomachs that contained an item at stage 1 of digestion and
an item at stage 6 of digestion are not included (see text).
No. of stomachs with
indicated difference between
stage-of-digestion values of
first and last food items eaten
No. of
Difference
Mean
differ-
stomach
0
1 2
3
4
N
ence
SD
2
44
25 9
0
1
79
0.60
0.78
3
13
17 0
0
0
30
0.57
0.50
4
2
3 2
0
0
7
1.00
0.76
5
2
0 0
0
0
2
0
0
Overall
61
45 11
0
1
118
0.60
0.78
dry weight of food (TDW) was found to be linearly
related to the total wet weight of food (TWW) in the
stomachs (TDW = -0.24 + (0.22) TWW; n = 318,
R~ = 0.96). Since the two measurements were highly
correlated (r = 0.98) and wet weight measurements
have frequently been used in similar food studies on
other species, it seemed valid to express the food
quantity results in this paper on a wet weight basis.
Table 4 summarizes the descriptive statistics of the
quantity of food in 414 stomachs examined. The
mean total weight of food found in the stomachs of
sharks caught by gill nets was significantly higher
than that found for sharks caught by rod and reel
(18.91 and 13.09 g respectively; 2-test, P = 0.003).
Similar results were obtained when food quantity
was measured as a percentage of shark body weight
(0.96 vs. 0.76%; z-test, P = 0.043). This result, in
conjunction with the other differences between the
two capture methods mentioned above, suggested
that sharks caught by rod and reel may not have
been representative of the entire population (see sec-
tion on Discussion). Because the primary value of the
stomach content data in this study will be in the esti-
mation of food consumed by the population, the
following results concerning the amount of food in
the stomachs were based on sharks caught by gill
nets since they were probably more representative
of the entire population of young sandbar sharks in
the study area. For sharks caught by gill nets, crus-
taceans accounted for nearly twice as much of the
mean total wet weight of food in the stomachs than
did fish. The mean wet weight of crustaceans in the
236 stomachs (12.37 g) was significantly higher than
the mean of 6.53 g found for fish (z-test, P < 0.001).
Similar results were obtained when food quantity
was expressed as a percentage of shark body weight
(0.65 vs. 0.31%; z-test, P < 0.001). The mean
weights of the two food components in the stomachs
Table 4 —Summary statistics of the amount of food In the stomachs of a sample of 414
sandbar sharks. Sharks were captured with gill nets and rod and reel gear. The z-test
statistic was used to test the equality of the indicated pairs of mean values.
Stomach
contents
Capture
method
Mean
N
SE
mean
Max
Min
z-test
Stat.
P-value
2-tailed
test
Fish (g)
Crustacea (g)
Gill net
Gill net
6.53
12.37
236
236
1.10
1.11
114.80
102.20
0
0
3.74
< 0.001
Fish (% BW)
Crustacea (% BW)
Gill net
Gill net
0.31
0.65
236
236
0.04
0.06
3.93
5.28
0
0
4.84
< 0.001
Total (g)
Total (g)
Gill net
Rod and reel
18.91
13.09
236
178
1.53
1.25
135.68
100.30
0
0
2.95
0.003
Total {% BW)
Total (% BW)
Gill net
Rod and reel
0.96
0.76
236
178
0.06
0.07
5.28
6.92
0
0
2.02
0.043
398
MKDVKl) KT AL.: STOMACH CONTKNTS OK SANDBAR SHARKS
were also calculated for each of eight consecutive 3-h
time intervals of the day (P^ig. 2). The means ranged
from 1.05 to 14.92 g for fish, from 7.51 to 19.72 g for
crustaceans, and from 11.74 to 34.64 g for the total
wet weight of food in the stomachs. When 95% con-
fidence bounds were placed around the means, con-
siderable overlap of the confidence intervals was
observed (Fig. 2). However, the mean total wet
weight in the stomachs of sharks captured between
the time of 0130 and 0430 was considerably higher
than the other means, and the confidence interval for
the mean during this time period overlapped sub-
stantially with only two of the remaining seven inter-
vals. Similar results were obtained when food quanti-
ty was expressed as a percentage of shark body
weight.
During the study one stomach was examined that
contiiined a total wet weight of 444.0 g of food
(10.3% BW (body weight)). This shark was not in-
cluded in the results presented above because the
quantity of food in the stomach was substantially
greater than for any other shark. It is mentioned
here because it does indicate that the stomach
capacity of this species is considerably greater than
the amount of food typically found in the stomach. In
an attempt to estimate maximum capacity, the
stomachs of 23 sharks were removed, ligated, and
filled with water to the point at which they were
about to burst. This point was determined by filling
several stomachs until they burst and noting the
changes that occurred in the stomach wall just before
the bursting point. The average maximum capacity
of the stomachs was found to be 13.0% of BW
(range: 8.04 to 19.8%). For sharks caught by gill nets
the mean quantity of food in the stomachs (0.96%
BW) was 7.4% of maximum capacity and the largest
quantity of food in a stomach (5.28% BW) was
40.6% of maximum capacity.
DISCUSSION
Several investigations conducted in other areas
have reported the sandbar sharks' diet to consist of
small crustaceans and fish (Bigelow and Schroeder
1948; Springer 1960; Clark and von Schmidt 1965;
Bass et al. 1973; Lawler 1977). With the exception of
squid in several stomachs, the prey items of the sand-
bar sharks captured in Chincoteague Bay, VA, were
also found to be small crustaceans and fish (Table 2)
and agree with those reported by Medved and Mar-
shall (1981) for this species in Chincoteague Bay. The
studies above provided little specific information con-
cerning the frequency of occurrence, size, relative
amounts, or physical state of the food items. In the
NUMBER
ou-
40-
— 30-
1
[ 1
<
O 20-
1—
10-
1 . 1
■
.1
0130 0430 0730 1030 1330 1630 1930 2230
0430 0730 1030 1330 1630 1930 2230 0130
TIME INTERVAL
Figure 2. -Amount of food in the stomachs of sandbar sharks
caught by gill nets during various time intervals of the day. Dots in-
dicate mean wet weight in grams, and bars represent 2 standard
errors on each side of the mean. The number of stomachs examined
during each interval is given at the top of the figure.
present study, small blue crabs that had recently
molted were, by far, the predominant food item in
terms of both weight and numbers. Small menhaden
were also found to comprise a significant portion of
the food consumed, but other species appeared to be
of minor importance in the diet of the sandbar shark
in the study area.
The results of this study strongly suggest that the
feeding behavior of sandbar sharks in the study area
was characterized by relatively short periods of feed-
ing activity separated by substantially longer periods
of time during which stomach contents were digest-
ed and no additional feeding occurred. An indication
that this species may go relatively long periods of
time without feeding was the high percentage
(21.5%) of sharks that had a single food item in their
stomach that was in a late stage of digestion (stage 5
or 6). Based on the approximate duration of each
399
FISHERY BULLETIN: VOL. 83, NO. 3
stage of digestion (12 or 15 h depending on prey
type) these sharl<s apparently had gone at least 48 h
without consuming additional food. Another 17.9%
of the sharks captured had empty stomachs. None of
these were found to have an everted stomach, in-
dicating that regurgitation of food was not respon-
sible for the high percentage of empty stomachs.
Additionally, 98 sandbar sharks fed preweighed
meals and released in an enclosure in the natural en-
vironment were not observed to regurgitate food
when recaptured at a later time (Medved in press).
Thus it appears that the sharks with empty stomachs
had not consumed food for a period of time greater
than the time required to evacuate the last meal (at
least 72 h). Given the long duration of gastric evacua-
tion, a shark feeding nearly continuously would have
many food items at various stages of digestion in the
stomach. Multiple food items were found in some
stomachs, but 90.6% of the stomachs contained less
than three food items. Multiple food items in a
stomach were also generally in similar stages of
digestion (Table 3). The sharks with a single food
item in their stomach consumed that meal in a very
short period of time. The mean difference between
the stage-of-digestion values of the first and last prey
item consumed by sharks with multiple items in their
stomach was 0.60 units (Table 3). Considering that
digestion was divided into six stages, the feeding
duration of sharks that consumed a meal of multiple
food items was also very short relative to the time re-
quired for complete gastric evacuation. Observations
made during a study of gastric evacuation in the
sandbar shark also suggested that feeding ceased
after the consumption of a meal (Medved in press). In
that study the stomachs of 98 sharks were lavaged to
remove all food and a preweighed meal was then fed
to each animal. The sharks were released in a large
enclosure in the natural environment that contained
an abundance of prey and were recaptured at various
times after feeding. Of the 54 sharks sacrificed
within 40 h of feeding, only 4 had consumed addi-
tional food. In contrast, of 11 sharks that had their
stomachs lavaged but were not fed a meal before
release all but 2 were found to have food in their
stomachs when sacrificed 24 h later. The results
discussed above indicate that the feeding activity of
sandbar sharks in the study area was intermittent
rather than continuous. Similar models have been
proposed in several other feeding behavior studies on
fishes. Diana (1979) proposed an intermittent feed-
ing model for the northern pike, Esox lucius, and
suggested that such a model was appropriate for
many top carnivores. Longval et al. (1982) have
shown that after captive lemon sharks, Negaprion
brevirostris, have fed to satiation, it takes a few days
for the appetite to become reestablished. Carey et al.
(1982) suggested that the great white shark, Car-
charodon carcharias, may maintain itself for more
than a month on a single large meal. Holden (1966)
and Jones and Geen (1977) indicated that the spiny
dogfish, Squalus acanthias, consumes a meal and
then ceases to feed until digestion is complete.
Observations made by Sano (1959) suggest that this
may be typical of other shark species as well.
The differences observed between the stomach
contents of sharks caught by the two capture
methods are consistent with the model of feeding
postulated above. The majority of sharks caught by
rod and reel had stomachs that were empty or that
contained food items in the first or last stage of
digestion (Fig. 1). The sharks with empty stomachs
had apparently not consumed food for a long period
of time. Those with a food item in the last stage of
digestion had relatively empty stomachs and had also
gone a considerable time without feeding. Finally,
the sharks with a food item in the first stage of diges-
tion had eaten within several hours of being caught.
Assuming that these sharks were actively feeding
since they were inclined to consume the squid used
as bait, it appears that the sharks in a "feeding mode"
were those with relatively empty stomachs that had
not fed for some time and those that had just eaten
but were inclined to consume additional food. The
stomachs of sharks caught by gill nets were empty or
contained a single food item or multiple food items in
similar stages of digestion suggesting, as indicated
above, that feeding was intermittent. However, the
stage-of-digestion values of the food items in the
stomachs were spread more evenly over the diges-
tion scale than for sharks caught by rod and reel, in-
dicating that these sharks were in various stages of
the feeding cycle (Fig. 1). The higher percentage of
empty stomachs and lower mean stomach content
weight found for sharks caught by rod and reel than
for those caught by gill nets also suggested that
sharks caught by red and reel were those in a "feed-
ing mode" and that sharks caught by gill nets were
probably more representative of the entire popula-
tion.
For sharks caught by gill nets the mean quantity of
food in the stomach was 0.96% of BW and the max-
imum quantity was 5.28% of BW (Table 4). Con-
sidering that the mean stomach content was based
on sharks containing food in various stages of diges-
tion, it f)robably is a significant underestimation of
the average meal size of sharks in the area. In con-
trast, the maximum quantity of food found in a
stomach is undoubtedly an overestimate and the
400
MEDVKI) KT AL.: STOMACH CONTENTS OF SANPHAK SHARKS.
average meal size should be considered to have been
somewhere between the two values. It would then
appear that the average meal size of the sharks cap-
tured was substantially less than the estimated
stomach capacity (13.0% BW). The mean stomach
content weights found for various time intervals of
the day in this study suggested that sandbar sharks
contained more food in their stomachs between 0130
and 0430 than during other times of the day (Fig. 2).
The evidence was not overwhelming but these
results do agree with a study by Medved and Mar-
shall (1981), indicating that night hours may be a
period of increased feeding activity for the sandbar
shark.
Although this paper has provided a quantitative
description of the stomach contents of the sandbar
shark, data concerning stomach contents alone are
not sufficient for estimating food consumption. As
pointed out by numerous researchers, the amount of
food in a fish's stomach is a function of both the rate
of ingestion and the rate of gastric evacuation (Eg-
gers 1977; Thorpe 1977; Elliott and Persson 1978;
Jobling 1981). However, when combined with detail-
ed information concerning gastric evacuation, the
results of this study will provide the basis for the con-
struction of an appropriate model of food consump-
tion for the sandbar shark.
ACKNOWLEDGMENTS
We would like to acknowledge the management
and staff of the Wallops Island Marine Science
Center for their cooperation. This study was sup-
ported by the Narragansett Laboratory of the Na-
tional Marine Fisheries Service, the Montauk (New
York) Captains' Association, the National Wildlife
Federation, and the Society of the Sigma Xi. It con-
stitutes a portion of a thesis submitted by the first
author in partial fulfillment of the requirements for
the degree of Ph.D. in oceanography at the Graduate
School of Oceanography of the University of Rhode
Island. Special thanks go to Ann Durbin and Howard
Winn for reviewing the manuscript and to Jim
Donovan. Jeremy Donovan, Brad Thompson, Herb
Morgan, and Todd Stephens for assisting with the
field work.
LITERATURE CITED
Bajkov, a. D.
1935. How to estimate the daily food consumption of fish
under natural conditions. Trans. Am. Fish. Soc. 65:288-289.
Bass, A. J., J. D. D' Aubrey, and N. Kistnasaivtv.
1973. Sharks of the east coast of southern Africa. I. The genus
Carcharhinus (Carcharhinidae). S. Afr. Assoc. Mar. Biol.
Res., Invest. Rep. 33, 168 p.
Hic.ELOW, H. B., and W. C. Schroeder.
1948. Sharks. In A. E. Parr and Y. H. Olsen (editors). Fishes
of the western North Atlantic, Part One, p. 59-576. Mem.
Sears Found. Mar. Res., Yale Univ.
Carey, F. G., J. W. Kanwisher, 0. Brazier, G. Gabrielson, J. G.
Casey, and H. L. PiiATT, Jr.
1982. Temperature and activities of a white shark, Carcharo-
don carcharias. Copeia 1982:254-260.
Casey, J. G.
1976. Migration and abundance of sharks along the Atlantic
Coast. In W. Seaman, Jr. (editor). Sharks and man -a
perspective, p. 13-14. Fla. Sea Grant Program, Rep. 10.
Clark, R., and K. von Schmidt.
1965. Sharks of the central gulf coast of Florida. Bull. Mar.
Sci. 15:13-83.
Davis, G. E., and C. E. Warren.
1971 . Estimation of food consumption rates. In W. E. Ricker
(editor). Methods for assessment of fish production in fresh
waters, p. 227-248. I.B.P. Handbook, No. 3, 2d ed.
Diana, J. S.
1979. The feeding pattern and daily ration of a top carnivore,
the northern pike (Esox lufius). Can. J. Zoo!. 57:2121-2127.
Durbin, E. G., A. G. Durbin, R. W. Langton, and R. E. Bowman.
1983. Stomach contents of silver hake, Merlucciiu? hilinearis,
and Atlantic cod, Gadus nwrhua, and estimation of their daily
rations. Fish. Bull., U.S. 81:437-454.
Edwards, R., and R. Hennemuth.
1975. Maximum yield: assessment and attainment. Oceanus
18(2):3-9.
Eggers, D. M.
1977. Factors in interpreting data obtained by diel sampling
of fish stomachs. J. Fish. Res. Board Can. 34:290-294.
Elliott, J. M., and L. Persson.
1978. The estimation of daily rates of food consumption for
fish. J. Anim. Ecol. 47:977-991.
Gulland, J. A.
1978. Fishery management: new strategies for new condi-
tions. Trans. Am. Fish. Soc. 107:1-11.
1983. Fish stock assessment: a manual of basic methods.
John Wiley, N.Y., 223 p.
Hennemuth, R. C.
1977. Some biological aspects of optimum yield. In H. Clep-
per (editor), Marine Recreational Fisheries 2, Proceedings of
the Second Annual Marine Recreational Fisheries Sympo-
sium, p. 17-27. Sport Fishing Institute, Wash., D.C.
1979. Man as a predator. In G. P. Patil and M. L. Rosen-
zweig (editors). Contemporary quantitative ecologj' and
related econometrics, p. 507-532. International Co-operative
Publishing House, Fairland, MD.
HOLDEN, M. J.
1966. The food of the spurdog, Squalm acanthias (L.). J.
Cons. Perm. Int. Explor. Mer 30:255-266.
Holt, S. J., and L. M. Talbot.
1978. New principles for the conservation of wild living
resources. Wildl. Monogr. 59, 33 p. The Wildlife Stx'iety.
Inc., Washington, D.C.
JOBLlNG, M.
1981. Mathematical models of gastric emptying and the esti-
mation of daily rates of food consumption for fish. J. Fish.
Biol. 19:245-257.
Jones, B. C, and G. H. Geen.
1977. Food and feeding of spiny dogfish (Squalus acanthias)
in British Columbia waters. J. Fish. Res. Board Can. 34:
2067-2078.
Lawler, E. F.
1977. The biology of the sandbar shark, Carcharhinus plum^
401
FISHERY Bl'LLKTlN; VOL. 83, NO. 3
beus (Nardo, 1827) in the lower Chesapeake Bay and adjacent
waters. M.S. Thesis, College of William and Mary, Williams-
burg, VA, 49 p.
LoNGVAL, M. J., R. M. Warner, and S. H. Gruber.
1982. Cyclical patterns of food intake in the lion shark Nega-
prion hreinrostiis under controlled conditions. Fla. Sci. 45
(l):25-33.
Mann, K. H.
1978. Estimating the food consumption of fish in nature. In
S. D. Gerking (editor). Ecology- of freshwater fish production,
p. 250-273. John Wiley and Sons, N.Y.
Medved, R. J., AND J. A. Marshall.
1981. Feeding behavior and biology of young sandbar sharks,
Carcharhimis plumbeus (Pisces, Carcharhinidae), in Chinco-
teague Bay, Virginia. Fish. Bull., U.S. 79:441-447.
Medved, R. J.
In press. Gastric evacuation in the sandbar shark, Carcharhi-
mis plumbeus. J. Fish. Biol. 1985(26).
Mercer, M. C.
1982. Multispecies approaches to fisheries management
advice. Can. Spec. Fuhl. Fish. Aquat. Sci. 59, 169 p.
Sano, 0.
1959. Notes on the salmon shark as a predator of salmon
(Oncorhynchui< spp.) in the North Pacific Ocean. In Data on
salmon predation, No. 3, p. 9-11. Hokuyo Bosen Kyogi Kai,
Japan. (Bur. Comm. Fish. Biol. Lab. (Seattle) Transl. Ser.
No. 32, I960.]
Springer, S.
1960. Natural history' of the sandbar shark Eulamia milberti.
U.S. Fish Wildl. Serv., Fish. Bull. 61:1-38.
Stillwell, C. E., and N. E. Kohler.
1982. Food, feeding habits, and estimates of daily ration of the
shortfin mako (/.sun<,s nxyrinrhus) in the northwest Atlantic.
Can. J. Fish. Aquat. Sci. 39:407-414.
Swenson, W. a., and L. L. Smith, Jr.
1973. Gastric digestion, food consumption, feeding periotiicity,
and food conversion efficiency in walleye {StizoMcdiun I'i^
treum intreum). J. Fish. Res. Board Can. 30:1327-1336.
Thorpe, J. E.
1977. Daily ration of adult perch, Pcrca Jh/riatiltJ^ L. during
summer in Loch Leven, Scotland. J. Fish. Biol. 11:55-68.
402
THE SPAWNING CYCLE OF SOFT-SHELL CLAM, MYA ARENARIA, IN
SAN FRANCISCO BAY
Shelly E. Rosenblum and Thomas M. Niesen'
ABSTRACT
Fi'ur populations Myit urcuaria in San Francisco Bay were studied for 1 year to determine the spawning
cycle. The spawning- cycle was well synchronized among; the four populations. Gametogenesis had com-
menced by late February and spawning occurred uninterrupted from April through summer. Cessation of
spawning occurred from September to October. The protracted spawning period of M. arenaria populations
in San Francisco Bay is f)robably related to the long period of moderate water temperatures (March-
October) which occur there. Size at first reproduction was placed at a shell length of 25 mm. Sex ratios of Af.
arenaria > 25 mm in shell length did not differ significantly from 1 : 1 . No evidence of hermaphroditism was
observed.
The soft-shell clam, Mya arenaria, was once popular
with clam diggers in San Francisco Bay. During the
early 20th century, owners of bay front property
fenced off portions of the mud flats in order to ex-
clude clam predators, thus insuring bountiful
harvests of M. arenaria (Bonnot 1932). Today as the
"trend toward the improvement of San Francisco
Bay water continues, "^ the potential for a recreation-
al shellfishery exists again. Agencies for communi-
ties on the bay have begun to look at this potential.
Recently (1982), the digging of clams in San Fran-
cisco Bay received official clearance for the first time
in 30 yr.3
The spawning cycle of the soft-shell clam has been
studied extensively on the east coast. Ropes and
Stickney (1965) examined populations from the Cape
Cod-New England region. They did not encounter
clams in the ripe stage of gametogenesis until May,
and by September spawning was over. Brousseau
(1978) reported a biannual cycle of spawning forM.
arevjiria from Cape Ann, MA. The first spawning
occurred between March and April and was of short
duration. A separate, second spawning took place
from June through July. Porter (1974) studied M.
arenaria from populations at Skagit Bay, WA. He
noted a single yearly spawning from late May to
early September.
'Department of Biological Sciences, San Francisco State Univer-
sity', 1600 Holloway Ave., San Francisco, CA 94132.
2Jones and Stokes Associates, Inc. 1977. San Francisco Bay
shellfish: an assessment of the potential for commercial and recrea-
tional harvesting. Prepared for the Association of Bay Area
Governments, 171 p.
^Champion, D. 1982. Clam digging OK'd on part of San Fran-
cisco Bay. San Francisco, Chronicle, 27 August 1982, p. 1.
The climate of the San Francisco Bay area, and
hence the seasonal water temperature fluctuations of
San Francisco Bay, are much less extreme than that
of the New England or Washington areas and most
of the other locations from which M. arenaria has
been examined. The question investigated in this
study is whether the spawning cycle of M. arenaria
from San Francisco Bay would differ from that of
other areas reported in the literature.
MATERIALS AND METHODS
Description of Study Sites
Specimens of M. arenaria were collected from
September 1979 through December 1980 from four
sites around central San Francisco Bay (Fig. 1): 1)
Candlestick Point- adjacent to the causeway leading
to the Candlestick Park Stadium (lat. 37°42'32"N,
long. 122°23'28"W); 2) Burlingame Lagoon -just
south of San Francisco International Airport (lat.
37°35'12"N, long. 122°20'10"W); 3) Foster City-
immediately north of the San Mateo Bridge, off
Third Street (lat. 37°34'20"N, long. 122°23'28"W); 4)
Point Isabel -north of the Golden Gate Fields race
track on the eastern shore of San Francisco Bay (lat.
37°53'59"N, long. 122°23'28"W). These areas were
selected because they experience annual variations
in temperature and salinity (Conomos 1979), factors
which are known to affect bivalve spawning cycles
(Loosanoff and Davis 1951; Swan 1952; Matthiessen
1960, Pfitzenmeyer 1962; Stickney 1964). Substra-
tum conditions were classified according to field
observations; no particle size analyses were con-
ducted.
Manuscript accepted October 1984.
FISHERY BULLETIN: VOL. 83. NO. 3, 1985.
403
FISHERY Bl'LLETlN: VOL. ,S3. NO. .S
The Candlestick Point site has a sandy substratum
and is adjacent to a broad expanse of mud flat.
Temperatures and salinities at this site reflect those
of the central San Francisco Bay (Conomos 1979).
Clams were collected high on the sandy beach front
0.6 m above Mean Lower Low Water (MLLW) in the
areas exposed as the tide begins to recede.
Burlingame Lagoon is separated from San Fran-
cisco Bay by a levee with a narrow channel connect-
ing to the open body of the Bay (Fig. 1). Salinity and
temperature can vary dramatically with heavy rains
(8 to 12 ppt) (pers. obs.). The area has a heavy clay-
mud substratum. The collecting site was 0.6 m above
MLLW.
The Foster City site was selected because it
reflects conditions more closely associated with the
south bay (Conomos 1979). The substratum is sandy-
mud with rocks and cobble intermixed. The area juts
into the bay and is exposed to wave action and
temperatures and salinities characteristic of the bay
waters (Conomos 1979). It is adjacent to outflow
from the tidal channel that winds through Foster
City. The collecting site was 0.24 m above MLLW.
The Point Isabel site is on the mud banks of a nar-
row (4 m wide) tidal channel that bisects the Point
Isabel promontory. The substratum is clay-mud with
rock and debris intermixed. Clams were collected
from 0.15 to 0.46 m above MLLW.
The depths of the collection sites (relative to
MLLW) at the four locations were dictated by the
presence of M. arenaria at each site. Mya arenaria
signals its presence by distinct siphon holes at the
surface of the substratum. After an initial excavation
of each collection site to a depth of 10 cm, it became
obvious that clams were present only in the specific
areas clearly marked by their siphon holes. There-
after only these areas were sampled.
Temperature and salinity were recorded with a
field hydrometer (marked at ppt) and thermometer
at each' site each month, beginning in October 1979
and continuing through November 1980.
Collecting Methods
A gardener's hand rake and careful hand digging
was used for excavating the deep-dwelling M.
arenaria. At least 25 clams were collected from each
of the four sites each month for 1 yr (with the follow-
ing exceptions: 4 October- Foster City, 12 collected;
3 November- Foster City, 20 collected; 25 Decem-
ber-Foster City, 24 collected; 2 November- Candle-
stick Point, 20 collected; 24 September- Point
Isabel, 20 collected; 3 November- Burlingame, 7 col-
lected). A total of 1,625 clams were examined in this
study. Clams were collected, placed in a Thermos*
jug of cool bay water, and returned to the laboratory.
Processing Methods
Analysis of gonadal stage was made by micro-
scopical examination of histological preparations
(Ropes and Stickney 1965). The presence and devel-
opment of gametes was used to infer the spawning
stage or readiness of the clam. Specimens were
measured for shell length to the nearest 0.1 mm. The
anterior one-third of the visceral mass (Ropes and
Stickney 1965) was removed, labeled, and placed in
Bouin's seawater fixative. During dissection, tissues
were submerged in cool seawater to prevent drying
or osmotic changes. The time between collection and
preservation was under 3 h to prevent any gonadal
changes.
The tissues were subjected to standard histological
procedures (dehydrated in alcohol and embedded in
paraffin). Embedded tissues were thin sectioned (5 ^A)
on a rotary microtome. Sections were mounted on
glass slides, stained with Harris' hematoxylin and
eosin, and examined using standard light micro-
scopy.
Each slide of gonadal tissue was studied to deter-
mine the presence of male or female gametes and the
condition of the gonadal tissues. This allowed clams
to be placed into one of the five classes of spawning
readiness (inactive, active, ripe, partially spawned,
spent) employed and described by Ropes and Stick-
ney (1965) for M. arenaria.
Categories of Spawning Readiness
(adapted from Ropes and Stickney 1965)
Female Gonads
INACTIVE PHASE. -Ropes and Stickney (1965)
used the term "inactive" to describe this phase.
Brousseau (1978) preferred the term "indifferent"
because cellular activity is continuing although no
gametogenic activity is obvious. The term "inactive"
is employed here and refers to individuals which are
not seen to be producing gametes whether due to
seasonal (quiescence or immaturity. Thus in this
research which presents pooled male and female
datii, the "inactive phase" may contain sexually un-
differentiated individuals along with inactive animals
clearly recognizable as male and female.
Females in the inactive phase exhibit small oocytes
^Reference to trade names does not imply endorsement hy the Na-
tional Marino P^i.shories Service, NOAA.
404
ROSKNHLIM :in<l NIKSKN: SI'AWNINC CYCI.K ()FAfK,4 .4/?^;,V/l/?M
PACIFIC
OCEAN
BURLINGAME LAGOON
FOSTER CITY
10km
Figure 1.- Study sites on San Francisco Bay indicated by circles.
405
FISHERY BULLETIN: VOL. 8.3. NO. 3
at the periphery of alveoli. Follicle cells completely
imbed the oocytes and may fill the lumina of alveoli.
ACTIVE PHASE. -Enlarging oocytes grow be-
tween follicle cells towards the center of alveoli.
Oocytes are irregular in shape but are attached to
the wall of the alveolus by broad cytoplasmic bases.
RIPE PHASE. -In the ripe phase, oocytes appear
as round cells in the lumina of the alveoli as if free of
attachment to the basal membrane, yet they may be
attached by a very slender stalk. The large oocytes
fill the lumina of the alveoli and are usually more
numerous than less developed oocytes.
PARTIALLY SPAWNED PHASE. -Gonadal
tissues contain a few ripe oocytes. Small oocytes are
imbedded in follicle cells at the periphery of an
empty alveolus. Many alveoli are devoid of ripe
oocytes.
SPENT PHASE. - Very few ripe oocytes are pres-
ent, usually darkly staining with obscure nuclei.
Numerous spherical droplets of lipoids and other
products of cytolysis are characteristic. The spent
phase progresses into the inactive phase.
Male Gonads
INACTIVE PHASE. -During the inactive phase,
male tissues contain products of atypical spermato-
genesis (Coe and Turner 1938). Tissues appear quite
active, yet this activity will not result in viable male
gametes. Pycnotic cells and multinucleated cells ap-
pear in the follicles. A few spermatogonia and
primary spermatocytes may be seen at the periphery
of alveoli while aberrant cells can be seen throughout
the alveoli. As indicated in the description of the in-
active phase for female gonads, this phase category
is expanded to include sexually undifferentiated in-
dividuals along with pooled male and female inactive
phase animals.
ACTIVE PHASE. -Proliferating primary sper-
matocytes exist at the basal membrane of the alveoli.
These are small and uniformly sized cells which are
similar to the earliest oocytes. They can be seen
growing between follicle cells, extending toward the
centers of the alveoli. Early stages of meiosis occur
at the periphery of the alveoli, while later spermatids
occur at the alveolar centers where they later form a
distinct mass. Follicle cells eventually disappear.
RIPE PHASE. -Masses of spermatozoa arranged
in more or less radial columns exist in rounded
alveoli with tails oriented toward the center.
PARTIALLY SPAWNED PHASE. -Relatively
few spermatozoa can be seen. Follicle cells start to
refill the alveoli. Some pycnotic cells occur.
SPENT PHASE. -Spent male tissues contain no
or very few spermatozoa in the central alveolar area.
Numerous follicle cells with multinucleated cells and
pycnotic cells from atypical spermatogenic activities
surround small groups of spermatozoa. Tissues lack
cells in the active phase of spermatogenesis. The
spent phase progresses into the inactive phase.
RESULTS
Of the 1,674 clams examined in this study, 1,361
were distinguishable as male or female; the remain-
ing 313 were indistinguishable as to sex. The male:
female ratio (670:691) did not vary significantly from
a 1:1 sex ratio (P = 0.25; x" = 0.294). No hermaph-
rodites were found. The possibility of asynchrony
between males and females was considered. Separ-
ate histograms were prepared for the male and
female data. Upon visual inspection the histograms
showed no clear pattern of asynchrony between the
sexes. As no discernable asynchrony was apparent,
further analysis was considered unnecessary'. The
data for both sexes were pooled and are reported
here.
The clams sampled in this study ranged from 15 to
88 mm in shell length. Of the 28 clams < 25 mm
sampled, only a single 15 mm female in the active
stage could be distinguished, the remainder showing
no gonadal activity of any kind, sex being indistin-
guishable.
No consistent relationship between spawning con-
dition and size could be discerned for clams over 25
mm in length. Correlation coefficients between size
and spawning condition were calculated and sub-
jected to a ^test, but the results were inconclusive.
Clams of all sizes occurred in the various spawning
categories throughout the spawning season. Mean
shell lengths varied from 44.9 to 61.6 mm among the
four populations studied (Fig. 2).
Candlestick Point
Sampling began in September 1979 and it was
apparent that spawning was ending at that time.
While 15% of M. arenaria were still ripe, 65% were
inactive and the remaining 20% partially spawned or
spent (Fig. 3). By late November, 95% of the clams
406
KOSKNBLUM and NIESEN: SPAWNING CYCLE OK A/1 .4 4/ffiN/lftM
CANDLESTICK
25
X = 44.9
SD= 13.0
20-
n = 409
h15-
^"
_
z
lU
o
oc
UJ
"
Q- 10'
-
5-
-
if
Th
ISABEL
X = 57.0
SD = 9.1
n = 447
£
oioomoinowomoiooioow
'-'-CJCVJCOOTt'TtlOinCDCON.h.OOOO
omoiooinoioowomoiooto
T-T-c\JC4COCO^TtlOlO<D<Dr«-N.OOOO
25
20
k151
Z
UJ
o
oc
lU
Q- 101
5-
FOSTER CITY
X = 61.6
SD = 13.3
n = 351
1
Oif)OlOOU)OmOU50U50«)OiO
••-•^C\JCVaC>5CO^Tl-lOU5<D<ON.h.OOCO
BURLINGAME
X = 55.0
SD = 12.3
n =466
J
Ih.
oioou)ou)otoou)ou)oir>oto
•'-•'-ejcMcoco'^'^mmtDtDN.h.oooo
SIZE CLASS
Figure 2. -Size-frequency histograms for the four populations studied. Size classes are (in mm) 10.0-14.9,
15.0-19.9, etc.
sampled were inactive and 5% still showed a few
mature gametes which would probably have been
resorbed. All individuals were inactive by the end of
December 1979.
The first sign of gonadal activity appeared at the
end of January 1980; by March, 82.1% of the clams
sampled were active. In April, all individuals were
either ripe or spawning. Peak spawning occurred
407
FISHERY BULLETIN: VOL. 83, NO. 3
CANDLESTICK POINT
100
z
111
o
cr.
UJ
0
SO N D JFMA
POINT ISABEL
lOOr t— I
LU
O
GC
UJ
FOSTER CITY
100
m
O
tr
UJ
Q.
0"-
S O N D JF M A M JJASOND
BURLINGAME
lOOr
ui
O
GC
UJ
a.
MONTHS
INACTIVE [HO] ACTIVE ^RIPE ^ PARTIALLY SPAWNED | | SPENT
Figure 3. - Percentage of the clams sampled that were in each of the five categories of spawning readiness. Male and
female data are pooled.
408
ROSKNHU'M and NIKSKN: SPAWNINC.CVC'LK OF A/y'.4 ARKNAHIA
during May and June. By the end of June, the sample
was roughly divided into thirds among the partially
spawned, spent, and inactive stages. Some spawning
could still be seen through the end of August, but by
late September 85% were inactive, 10% partially
spawned, and 5% spent.
Foster City
September-October 1979 marked the end of the
Foster City population spawning, with most clams
(70%) being inactive during this period (Fig. 3).
From early November through the end of December
1979, no activity could be found. The late January
1980 sample showed a 90% active:10% spent ratio
with no intermediate stages represented. It is
unclear whether this indicated a rapid maturing and
spawning of a few precocious individuals or an over-
wintering of residual gametes. By mid-March, every
stage was represented, most (50%) being in the ripe
stage. Peak spawning extended from the beginning
of April through May, with a complete maturation-
spawning season extending from late February
through May. From July to late September no appre-
ciable gonadal activity could be discerned. This lack
of activity from mid- to late summer distinguished
the Foster City population by its short spawning
season relative to other populations (Fig. 3).
Burlingame Lagoon
Sampling of the Burlingame Lagoon population
did not begin until November 1979. At the time 85%
of the clams sampled were spent and only 15% were
inactive (Fig. 3). This suggests a protracted spawn-
ing in 1979, similar to that which was seen in 1980.
By December all but 5% were inactive and by 1
January 1980 all were inactive. Gonadal activity ap-
peared again by the end of January 1980. Peak
spawning occurred during May and June; however,
spawning continued well into September and Octo-
ber with a full 30% of the clams of each sample being
in the partially spawned stage. The Burlingame
Lagoon population had the longest spawning season
of the populations examined.
Point Isabel
Sampling of the Point Isabel population began in
September 1979. The September and October sam-
ples still contained ripe individuals (< 10%), but most
of the clams sampled were spent or inactive. By
November, 70% of the clams sampled were inactive
and by the end of December all were inactive (Fig.
3). The 1979 spawning season had ended for the
Point Isabel population by early November.
Gonadal activity had resumed by late January. By
March, 80% of the clams sampled were active. Only
ripe and partially spawned individuals could be found
in mid-April, and by May inactive individuals were
being found (10%). Peak spawning occurred during
May. Spawning continued through June and by July
almost 80% were inactive and 20% partially spawn-
ed or spent. Spawning appeared to be over; however,
the August sample contained almost 35% partially
spawned and 5% ripe individuals. It is tempting to
suggest a possible second spawning in August, but
the May and June samples lacked active or ripe in-
dividuals, which suggest the August observation be
attributed to sampling error. Spawning was still
occurring in late September, as 15% were still in the
partially spawned stage. At this time, however, 60%
were inactive and 25% spent.
The four study sites showed similar trends (Fig. 4)
in temperature and salinity. Temperatures fell from
November through mid-Januar^' and rose from mid-
January through the beginning of April and then
stabilized. Temperature then climbed again from
mid-May through July. The July-September temper-
atures were steadier at the Foster City and Bur-
lingame sites than at Point Isabel or Candlestick
Point, where they dropped markedly during this
period. Salinity followed a similar trend, falling dur-
ing the late winter months, and rising during spring
and summer (Fig. 4). Salinity ranged from 8 to 33
ppt and temperature from 12° to 23°C.
DISCUSSION
The spawning cycle of M. arenaria in San Fran-
cisco Bay in 1980 was an extended one. Gameto-
genesis had begun by late January for three of the
four populations sampled (Candlestick Point, Bur-
lingame Lagoon, and Point Isabel), and by mid-
March all five stages of gonadal development were
represented in the Burlingame Lagoon, Point Isabel,
and Foster City populations. Spawning had begun at
all four sites by April; over 20% of the individuals
from each sample were in the partially spawned or
spent stages. The number of clams in these spawning
stages reached a maximum during May and June
1980. Spawning continued through September and
October and then ceased.
Only a single clam < 25 mm in length was found to
have active gonads. This suggests that 25 mm might
be generally recognized as the size at first repro-
duction for San Francisco Bay M. arenaria.
409
FISHERY BULLETIN: VOL. «3. NO. 3
T
E
M
p
E
R
A
T
U
ft
E
26H
24
2>
20*
!••
U*
12
26<
24-
22<
20-
!••
!«•
U<
12<
26«
24«
22«
20*
!••
16*
14<
12
26<
2«
2>
2C^
IS*
lb*
I4<
^ g '^
L_1_SL
ISABEL
FOSTER CITY
BURLINGAME
^^1 CANDLESTICK
N
M
M
JASON
36
32
>2t
•24
20
>16
>12
••
F36
32
>2t
•24
•20
>16 ppt
•12
>•
36
•32
•2t
•24
•20
•16
•12
>•
t
A
L
I
N
I
T
V
Figure 4. -Temperature and salinity variations during the collection period for the four collection sites, 1979 and 1980.
Although no growth or age measurements were per-
formed in this study, the 25 mm shell length in-
dicating a lower limit to sexual maturity corresponds
to the east coast M. arenaria found to be late in their
first year (Brousseau 1979).
Of the 313 clams that were indistinguishable as to
sex, only 28 were < 25 mm in length, therefore we
cannot attribute this lack of discernable sex to im-
maturity. Furthermore, clams of indeterminate sex
were seen only during the fall and winter months
(September-March) when most clams were found to
be in the inactive stage. During the period of March-
September or spring-fall when the active, ripe, par-
tially spawned, and spent stages were well
represented, all clams could easily be determined to
be male or female. The difference between inactive
male and female gonads is obvious and was seen in
many clams, yet many clams which were larger than
25 mm in length and should have been sexually
mature showed no signs of sexually distinguishable
tissue at all. No evidence of even small oocytes or
atypical spermatogenesis was seen in these clams.
For the sake of simplicity, these clams were placed in
the inactive stage. Perhaps this condition was a kind
of "gonadal exhaustion" due to the prolonged spawn-
ing period.
The four study populations were dominated by
clams ranging from 40 to 75 mm in length (P^ig. 2).
This size range corresponds to the 1.5 to 4.0 year
classes determined by Brousseau (1979) for M.
arenaria from Gloucester, MA. While total corres-
pondence in growth rates between Massachusetts
410
ROSKNBLUM and NIESEN: SPAWNINC CVCl.K OF An'/l /IftAW/IWM
and San Francisco Bay populations cannot be as-
sumed, the age classes can be used as a first estimate
of approximate age with size.
Studies of the spawning cycle of soft-shell clams
from the east and west coasts of the United States
reveal both similarities and differences in spawning
pattern. Spawning on both coasts begins in early
spring as the water warms from the lower winter
temperatures. The majority of east coast populations
studied show two separate spawnings each year,
while populations studied on the west coast show a
single more protracted spawning. Differences in the
length of spawning and the number of separate
spawning episodes are probably partially related to
the phenology of water temperature change and the
difference in the range of water temperatures that
occur on either coast.
Mya arenaria in San Francisco Bay, studied dur-
ing the 1979-80 season, began ripening earlier than
M. arenaria of the New England region studied
previously. Ropes and Stickney (1965) encountered
active clams in eastern Maine by late January;
however, ripe clams were not discovered until mid-
May, and at that time none appeared to have spawn-
ed. Clams from their Booth Bay Harbor samples
showed the earliest ripening, which was in April and
May; by September spawning was over.
Brousseau (1978) reported a biannual cycle of
spawning for M. arenaria from Cape Ann, MA. The
first spawning at Cape Ann occurred as early as that
in San Francisco Bay (March); however, it was of
short duration, being over by April. A separate sec-
ond spawning took place during June through July.
Brousseau's figures indicate water temperatures
began to rise from a low of 1°C around Cape Ann as
early as mid-February, but did not rise above 10° C
before May. It is possible that the increase in
temperature triggered an early spawning, but the
continuing, relatively cold temperature prevented an
adequate build-up of mature gametes to sustain a
prolonged spawning. Once spawning had taken
place, the clams may have had to undergo another
period of gametogenesis prior to a second spawning.
Brousseau (1978, page 159) stated, "The presence of
cytolyzed unspawned gametes in the summer
samples suggested that the same individuals had also
been ripe earlier in the year. Thus the observed
spawning pattern was due to repeated spawning by
the same individuals rather than asynchronous
spawning of individuals within the population."
Pfitzenmeyer (1962) also reported two annual
periods of spawning in M. arenaria at Solomons,
MD. He noted that "The first umbone larvae of the
year usually were found in May after the surface
waters rise above 15°C or a mean temperature of
16.7°C." Salinities which remained constant
throughout the spring remained near 10 ppt. This
corresponds to the March temperature-salinity pat-
terns in San Francisco Bay. During March, San
Francisco clams were just beginning to spawn. Pfit-
zenmeyer also noted the disappearance of larvae
from the Maryland waters as the temperature rose
above a mean of 21.4° C. The larvae did not reappear
until temperatures had fallen below this point. He
concluded an optimal temperature range exists dur-
ing which spawning may occur. In San Francisco
Bay, temperatures rose to or above 21 °C only in the
following instances: Foster City- 11 April - 23° C, 2
July - 21°C, 25 August - 21°C; Candlestick Point-
9 April - 23°C, 30 June - 23°C; Point Isabel- 10
April - 23°C (Fig. 4).
Porter (1974) noted a single yearly spawning from
late May to early September among M. arenaria
from Skagit Bay, WA. This is a shorter spawning
season than seen among San Francisco Bay M.
arenaria and may be a result of lower temperatures
(4.8°-15.7°C) encountered in Washington.
Simel^ reported a single spawning from late March
through April for soft-shell clams from Humboldt
Bay, CA. Generally, this more northerly part of
California has a cooler climate than the San Fran-
cisco Bay area. Simel indicated that the later stages
of gametogenesis corresponded with a peak in the
phytoplankton abundance.
Studies of the spawning cycles of M. arenaria
from the east and west coasts of the United States
suggests a pattern of spawning behavior. Spawning
begins as the water temperature rises in the spring.
Pfitzenmeyer's (1962) work suggests M. arenaria's
optimal spawning range falls between 15° and 21 °C.
Differences between the spawning cycle of M.
arenaria from San Francisco Bay and that of M.
arenaria from New England, Canada, Washington,
and northern California may be explained as the
logical result of the different seasonal warming pat-
terns and extremes encountered in the different
areas. San Francisco Bay does not cool to the same
temperatures as the other areas and has a much
longer period of moderate water temperatures, ex-
tending from late March through summer and into
September and October. Consequently, M.
arenaria's spawning season is equally protracted in
San Francisco Bay.
^N. Simel, Humboldt State University, Areata, CA 94542, pers.
commun. 1982.
411
FISHERY BULLETIN: VOL. 83, NO. 3
ACKNOWLEDGMENTS
We thank James Sutton of the California Academy
of Sciences for his assistance with the selection of
our study sites.
LITERATURE CITED
BONNOT, P.
1932. Soft shell clam beds in the vicinity of San Francisco Bay.
Calif. Fish Game 18:64-66.
Brousseau, D. J.
1978. Spawning cycle, fecundity, and recruitment in a popula-
tion of soft-shell clam, Mya armaria, from Cape Ann, Massa-
chusetts. Fish. Bull. U.S. 76:155-166.
1979. Analysis of growth rate in Mya arenaria using the Von
Bertalanffy equation. Mar. Biol. (Berl.) 51:221-227.
CoE, W. R., AND H. J. Turner, Jr.
1938. Development of the gonads and gametes in the soft-shell
clam (Mya arenaria). J. Morphol. 62:91-111.
CONOMOS, T. J.
1979. Properties and circulation of San Francisco Bay waters.
In T. J. Conomos (editor), San Francisco Bay, the urbanized
estuary, p. 47-84. Pac. Div., Am. Assoc. Adv. Sci. Allen
Press, Lawrence, KS.
LOOSANOFF, V. L., AND H. C. DAVIS.
1951. Delaying spawning of lamellibranchs by low tempera-
ture. J. Mar. Res. 10:197-202.
Matthiessen, G. C.
1960. Observations on the ecology of the soft clam, Mya
arenaria, in a salt pond. Limnol. Oceanogr. 5:291-300.
Pfitzenmeyer, H. T.
1962. Periods of spawning and setting of the soft-shelled clam,
Mya arenaria, at Solomons, Mary'land. Chesapeake Sci. 3:
114-120.
Porter, R. G.
1974. Reproductive cycle of the soft-shell clam, Mya arenaria,
at Skagit Bay, Washington. Fish. Bull., U.S. 72:648-656.
Ropes, J. W., and A. P. Stickney.
1965. Reproductive cycle of Mya arenaria in New England.
Biol. Bull. (Woods Hole) 128:315-327.
Stickney, A. P.
1964. Feeding and growth of juvenile soft-shell clams, Mya
arenaria. Fish. Bull., U.S. 63:635-642.
Swan, E. F.
1952. The growth of the clam Mya arenaria as affected by the
substratum. Ecology 33:530-534.
412
RECRUITMENT PATTERNS IN
YOUNG FRENCH GRUNTS, HAEMULON FLAVOLINEATUM
(FAMILY HAEMULIDAE), AT ST. CROIX, VIRGIN ISLANDS'
W. N. McFarland,2 E. B. Brothers.^ j. C. Ogden," M. J. Shulman,^
E. L. Bermingham," and N. M. Kotchian-Prentiss'
ABSTRACT
During 1979 and 1980 the settlement of postlarval ji^runts (mostly French grunts, Haemulon flarolinentuw)
from the plankton to inshore areas in Tague Bay, St. Croix, Virgin Islands, was monitored. Settlement
occurred at all times of the year, but showed two distinct maxima during May-June and October-November.
Summer settlement rates were approximately one-third the peak rates, whereas winter settlement rates
were low but always present. A dominant, semilunar periodicity in the settlement of the postlarvae was
clearly present, but smaller interspersed weekly peaks occurred. Calculation of the fertilization dates of
recently settled postlarval grunts, derived from otolith ages, also established a dominant 1 5-day periodicity,
but again interspersed with smaller weekly fertilization peaks. The phase of settlement and fertilization is
most strongly associated with the quarter moons and/or intermediate daily excursions of the tides; the
smaller weekly peaks are more closely associated with new and full moons. The pelagic existence of French
grunts is about 15 days, suggesting that fertilizations that lead to successful recruitment to inshore areas
precede settlement by 15 days. Two hypotheses -semilunar shifts in spawning versus a more constant daily
rate of reproduction -are discussed as possible explanations of the dominant semilunar rhythm observed in
the settlement patterns.
Community structure is primarily determined by
predation, competition, environment, and patterns
of reproduction and recruitment (Ricklefs 1979). In
most marine fishes the larval stages are planktonic, a
circumstance especially true for tropical reef fishes
(Breder and Rosen 1966; Sale 1980; Thresher 1984).
In general, larger reef species produce numerous but
relatively small eggs, which at spawning are dis-
persed into the plankton; whereas smaller reef
species produce fewer but larger demersal eggs,
which are guarded until hatching when the larvae
also "escape" into the offshore plankton community
(Johannes 1978; Barlow 1981). The potential
significance of this widespread reproductive strategy
to affect coral reef fish assemblage structure is wide-
ly recognized (see Helfman 1978 and Sale 1980 for
reviews). Most ecologists have assumed that
^Contribution No. 70 of the West Indies Laboratory.
^Section of Ecology and Systematics, Division of Biological
Sciences, Cornell University, Ithaca, Wi 14853.
^Section of Ecology and Systematics, Division of Biological
Sciences, Cornell University, Ithaca, NY 14853; present address: 3
Sunset West, Ithaca, Wi 14850.
"•West Indies Laboratory, Fairleigh Dickinson University, Chris-
tiansted, St. Croix, VI 00820.
^Department of Zoology, University of Washington, Seattle, WA
98195.
^Department of Biology, University of Massachusetts, Boston,
MA 02125.
'Department of Zoology, University of Maine, Orono, ME 04473.
Manuscript accepted October 1984.
FISHERY BULLETIN; VOL. 83, NO. 3, 1985.
planktonic larval fishes provide an extensive reser-
voir of potential recruits that settle to the reef
whenever space becomes available (Sale 1977, 1978;
Dale 1978; Smith 1978). Virtually all recent studies,
however, emphasize that we know little of the
ecology of larval fishes at sea and of their patterns of
recruitment to benthic juvenile habitats (McFarland
in press; McFarland and Ogden in press). Until more
quantitative information on the early life history of a
variety of species of reef fishes is available, models
that "explain" fish community structure remain, at
best, first approximations. Here we describe spatial
and temporal patterns of recruitment in the French
grunt, Haeviulonflavolin£atum, a dominant western
Atlantic tropical reef species.
MATERIALS AND METHODS
Recently settled postlarval French grunts and
white grunts, H. plumieri, standard length (SL) ca.
8.5 mm, are commonly observed in schools over
grass beds or associating with coral clumps and
gorgonians in Tague Bay, St. Croix, VI. Single in-
dividuals and larger aggregations associate with
structure and/or intermix with schools of mysids
(McFarland and Kotchian 1982). There is little diffi-
culty in recognizing and counting these very small
grunts in the field because they lack the body colora-
413
tion patterns of slightly larger postlarvae (see table 1
in McFarland and Kotchian 1982). Postlarval grunts,
however, cannot be identified by sight at the species
level. We will refer to these smallest postlarvae as
PL-1 grunts. These recently settled postlarvae are
diurnal plankton feeders (McFarland 1980) as,
presumably, is the preceding pelagic larval stage.
Although the postlarvae show strong social tenden-
cies to school during daytime, they are solitary at
night (Helfman et al. 1982); the same pattern is
found in older juveniles and adults (Ogden and
Zieman 1977). The typical stereotyped twilight
migrations of older juvenile and adult grunts (Hob-
son 1968; Ogden and Ehrlich 1977; McFarland et al.
1979), however, are not present, nor are the agonis-
tic behaviors typical of all later stages (McFarland
and Hillis 1982).
During collateral studies on the population dyna-
mics of grunts, on agonistic behavior in juveniles
(McFarland and Hillis 1982), and age determinations
of grunts (Brothers and McFarland 1981), we noted
that recently settled PL-l's appeared in pulses. To in-
vestigate this periodicity, an extensive area of bot-
tom in Tague Bay and a series of shallower discrete
reef sites were censused repeatedly for PL-l's. In
addition, subsamples of PL-l's were collected
throughout the census period for size and age deter-
minations.
Tague Bay Census Measurements
Sixteen flagged iron stakes were set 10 m apart
along the bottom of Tague Bay parallel to the bay's
barrier reef at a depth of ca. 5m. The bottom was
characterized by sandhills produced by the burrow-
ing activity of thalassinid shrimps, with stands of the
seagrasses Thalassia testudinum, Syringodium
filiforme, and Halodole wrightii between the
mounds. Censuses of the total number of postlarvae
were made using scuba, recording the numbers of
grunts encountered along a 5 m wide transect. The
census included all postlarval grunts observed over
an area of 800 m^ of bay bottom. Because almost all
juvenile grunts in the immediate vicinity were
French grunts, we presume the census data mostly
represent this species. Of 85 PL-l's collected on
this site, all were identified as French grunts. The
census began on 25 February 1979, and was con-
tinued at variable intervals through 31 August 1980.
Although numbers of older grunts were also record-
ed, here we report only the numbers of the smaller
and youngest postlarvae (mean SL = 8.5 mm). This
census is hereafter referred to as the "sandhill"
site.
FISHERY BULLETIN: VOL. 83, NO. 3
Reef Census Measurements
A series of 20 individual sites in a shallow sandy
area (1-3 m depth) along a 200 m stretch of the
Tague Bay barrier backreef were monitored for post-
larval settlement. The sites varied somewhat in size
and structure, but were composed of small clumps of
Montastrea annularis and/or Porites porites. Six-
teen of the sites were in depths of 1 to 2 m; four were
in 2 to 3 m depth. Reef areas varied from 0.1 to 8 m^;
vertical relief from 20 cm to 1.5 m. Daily censuses
were obtained as often as possible from 25 April
1980 through 25 May 1981. The census schedule was
intensified especially from 6 May through 27 Decem-
ber 1980 (172 censuses over 236 d). Counts on each
site on each census day included the total numbers of
PL-l's, older postlarvae, juvenile grunts (see McFar-
land and Kotchian 1982), damselfishes (all species
lumped), and the common sea urchin, Diadema an-
tillarum, within the spines of which the middle-sized
juveniles often seek refuge (see Helfman et al. 1982).
In this reef area, which is surrounded by coral sand
and lacks seagrass beds, juvenile white grunts were
never encountered, only French grunts. We con-
clude therefore that recruits were all French
grunts.
Reproductive Activity and
Aging of French Grunts
Spawning in grunts has not been observed or
reported in the literature (Breder and Rosen 1966;
Hobson 1968; Johannes 1978; Lobel 1978; our per-
sonal observations and field observations of P. Colin
and of E. S. Hobson). An indirect method was used
to provide information on whether grunts spawned
in some periodic manner, as so many reef fishes do
(Johannes 1978; Lobel 1978; Colin 1982).
The age of French gnmts can be established in
days, for example, by counting the number of micro-
structural growth increments laid down in the
lapillus (Brothers and McFarland 1981). The method
is especially useful for aging the younger life history
stages (< 100 d). By ascertaining the actual age of an
individual grunt in days, it becomes possible to
establish the specific date on which it was spawned.
The method requires a correction, however, because
the first "daily" growth increment deposited in the
otolith does not coincide with fertilization of the egg.
Our best "estimate" for the age at formation of the
first distinct increment in the otoliths of French
grunts is the third day after fertilization (for details
see Brothers and McFarland 1981; this revised esti-
mate is based on laboratory-reared porkfish, the con-
414
McFAKl.ANI) KT Al,.; KKCRUITMKNT PATTERNS IN FRKNCll CKUNTS
familial Anisotremus virginicus, of known age, sup-
plied by Martin Moe). Thus, to each "otolith age" ( =
total increments counted) 2 d were added to establish
the "absolute" daily age of an individual fish.
This method was applied to postlarval French
grunts, collected throughout the year in the vicinity
of the 20 discrete census sites. On most census days
individual PL-l's were collected with a fine mesh net
and fixed and preserved in 95% ethanol. Each post-
larva was measured (SL) and the otoliths were
removed and placed in immersion oil. The number of
growth increments was counted and corrected ( -i- 2
d) to the actual date of fertilization.
Tides
A tidal gauge (NOAA, Ocean Survey #9751224)
operates at the West Indies Laboratory dock, about
0.5 km from our Tague Bay study site. Hourly tidal
heights for the year 1980 were obtained from
NOAA. Missing, due to malfunction of the gauge,
are records from 26 June to 9 September 1980.
These missing values were approximated from calcu-
lated tidal data for San Juan, Puerto Rico. The phase
of the tides in Puerto Rico matched closely the tides
at Tague Bay (comparisons of dates before and after
the missing records), but the actual excursion of the
tides was less at St. Croix than calculated for Puerto
Rico.
RESULTS
Tague Bay Sandhill Study Site
During 1979, 27 censuses were executed during
300 possible days of sampling (25 February to 21
December). The mean interval between censuses
was 1 1 .2 d ± 6.6 ( 1 SD), the intervals ranging from 4
to 23 d. Five population peaks were recorded, with
the number of PL-l's counted between peaks often
declining to < 100 individuals. The 1979 census
clearly indicated that settlement was represented by
a series of pulses, but the sampling intervals were
too long to resolve periodicities of much less than 1
mo. Therefore, in 1980 the sampling resolution was
improved by increasing the number of censuses to 47
over a possible 325 sampling days (6 February to 26
December 1980); mean sampling interval was 7.0 d
±7.7, the shortest interval being 1 d and the longest
interval 49 d (i.e., the first interval). Eleven peaks, of
which 8 are distinct, establish that the postlarvae
settle in pulses, with the population numbers on the
bay bottom often decreasing to 0 between pulses
(Fig. 1). Although the pulses in population numbers
1950
Figure 1.- Numbers of recently settled postlarval grunts observed
over 800 m of bottom on the sandhill site area of Tague Bay, St.
Croix, V.I.
are suggestive of a semilunar periodicity, the peaks
do not coincide more closely with either quarter
moons or with the new and full moons than do the
population declines.
Individual Barrier Reef Study Sites
The mean sampling interval on the 20 individual
census sites from 6 May to 27 December 1980 (possi-
ble 236 sampling days) was 1.37 d ± 0.7 (1 SD). This
shorter sampling interval vividly reveals the period-
icity in the appearance of PL-l's on the sites (Fig. 2).
Coincidence between these peaks and the peaks for
the sandhill study sites is quite good (compare
Figures 1 and 2) and indicates that the timing of the
settlement of PL-l's is general over the entire area.
Also, as in the sandhill area, the numbers of PL-l's
declined to 0 between most pulses. Furthermore, the
pooled data for the 20 sites indicate a bimodal
seasonal influx of PL-l's, one in late spring and a sec-
ond increase in fall, as seen also in the sandhill study
site (compare Figures. 1 and 2). The summer settle-
ment pulses involved about one-third the number of
individuals associated with the bimodal peaks.
Winter settlement was very low; only small numbers
of PL-l's were observed during January and
February 1981.
Age and Reproductive Activity
A total of 2,353 postlarvae from 141 collections
spread over 391 d were captured between 20 Febru-
ary 1980 and 16 March 1981 (Fig. 3). From each of
these 141 samples 15 PL-l's were measured and
aged, or fewer if the collected samples contained
415
FISHERY BULLETIN: VOL. 83, NO. 3
CO
cc
o
100 -
jl.jllll I
Jl j| A| SI O
J
7 -(4)
ill I I
14 - (2)
11 - (11)
nH dH
DC 900
J
yk
15^
Figure 2. - Numbers of recently settled postiarval grunts observed on the individual census sites located in the shallows along the backreef of
Tague Bay barrier reef. The three upper graphs represent the recruitment of PL- I's to specific sites?, 11, and 14. Numbers in parentheses to
the right of the hyphens indicate on how many sites a similar seasonal pattern of settlement was observed. Three of the 20 census sites were
like 7 or 14, but also recruited grunts in summer ( not shown). The lower graph represents the pooie<l data from all 20 sites. Values for census
gaps have been estimated by calculating running averages (open bars). Numbers indicate the weaker but definitive weekly influxes of post-
larvae. Additional weekly peaks probably occur but are less certain. Note the bimodal seasonal increase in recruitment during May-June and
October-November: This coincides with the modal and bimodal peaks in gonadal development of several Caribbean reef species (Munro et al.
197.3).
416
McFARLANP F.T AL.: KKCKI'ITMKNT I'AITKRNS IN FKP:N('H CRUNTS
CO
DC
O
CC
<
SAMPLING DATES
15 -
o
\j\y
Q.
20
U.
O
10
QC
LU
CQ
0
1980
Fkjure 3. - Relationship (if fertilization dates of recently settled postlarval grunts to time of the year. Upper graph represents the dates and
the numbers of postlarvae collected for aging from the backreef of Tague Bay barrier reef. Lower graph represents the frequencies for back-
calculated dates of fertilization of the collected samples in the upper graph.
fewer postlarvae (Fig. 3). The actual day of fertiliza-
tion for each of these 1,478 French grunts indicates
that recently settled individuals were spawned with
a consistent periodicity (Fig. 3) that is similar to the
settlement periodicity (Fig. 2). These derived spawn-
ing data suggest, however, the presence of a more
pronounced short cycle.
Periodic Analysis, Times of
Settlement and Reproductive Activity,
and Patterns of Settlement
Periodic Analysis
To evaluate the periodicity of postlarval settlement
and of fertilization times of recently recruited
French grunts (Figs. 2. 3), we used a Rayleigh-test
(see Batschelet 1965). The method involves a Fourier
transform of sequential data (see McFarland and
Kotchian 1982 for details). A data set is first sequen-
tially summed for a specified period, and these pool-
ed data are used to evaluate the degree of deviation
from a nonperiodic random distribution. By compar-
ing dimensions of the mean vectors obtained for dif-
ferent specified periods, the most dominant period is
usually revealed (Fig. 4).
Analysis of the 1980 settlement and fertilization
data reveals that a rhythm with a period of about 15
d dominates (Table 1). Examination of the census
and fertilization data (Figs. 2, 3) indicates that weak
secondary appearances of PL-l's and different ferti-
lization dates may occur. Indeed, their presence (e.g.,
4 peaks in Fig. 2) hints at a weekly rhythm super-
imposed on the semilunar periodicity. It is difficult to
assess this possibility with periodic analysis,
however, because a natural harmonic of the domi-
nant 15-d rhythm can occur at about 7.5 d, even if a
weekly rhythm does not exist (Fig. 4).
With less mathematical elegance the periodicity in
the data sets can be estimated by averaging intervals
between peaks. Both the 1980 census data for the 20
discrete study sites (Fig. 2) and the fertilization date
data (Fig. 3) provide similar estimates of about 13.9
d and 15.1 d (Table 2), which do not differ significant-
ly from the mean semilunar period of 14.64 d that ac-
tually occurred. The possible presence of a weekly
rhythm often interspersed between the biweekly
rhythm is revealed by 5 obvious short-period pulses
417
FISHERY BULLETIN: VOL. 83, NO. 3
Figure 4. -Variation in the len^h of vectors derived
from a circular distribution test for different
periodicities in the settlement and fertilization data
presented in Figures 2 and 3 (upper graph). Note that a
period of about 15 d provides the largest vector value
beyond a 1-d period (Rayleigh test statistic z = 28.2 for
settlement and 10.8 for fertilization, where 2(p^Q qi) =
4.6). Lower graph is a plot of vector values from ar-
tificial data generated by repeating the analysis for 2, 4,
and 8 cycles (artificial data were 0, 0, 0. 0, 25, 50, 75,
100, 75, 50, 25, 0, 0, 0, 0). Note how an increased
number of cycles or periods narrows the peak for the
dominant 15-d period and introduces more harmonics.
The settlement and fertilization data (upper graph)
represent 16 cycles for a period of 15 d. The height of
the harmonics after 15 d probably reflects basic sam-
pling noise and the presence of smaller weekly peaks
(see Figs. 2, 3).
•— FERTILIZATION
O— SETTLEMENT
10 15 20
PERIOD IN DAYS
25 30
Table 1.— Dominant periods derived from a circular distribution test of the settlement
and fertilization data presented in Figures 2 and 3. Significance symbols are ** = P<
0.01; z values are Rayleigh test statistic (Batschelet 1965).
Type of
data
Date of
samples
Dominant
period
(days)
z value
No.
days
No. cycles
analyzed based on
dominant period
Settlement
Fertilization
30 Aug.-31 Dec.
2 May-31 Aug.
30 Aug. -31 Dec.
2 May-31 Dec.
2 May-31 Aug.
30 Aug.-31 Dec.
14.9
15.3
17.0
14.8
14.6
15.5
26.5**
19.2**
31.6**
10.7**
8.7**
2.8 n.s.
244
122
124
244
122
124
16.4
8.0
7.3
16.5
8.4
8.0
for settlement and at least 9 short-period pulses for
fertilization (Table 2).
Timing of Settlement and Fertilization
To estimate the phase of settlement and of fertili-
zation to the lunar cycle, the delay in days from the
nearest full or new moon was determined for each
event (Table 2). The mean phase delay for fertiliza-
tion was 5.4 d, and for settlement 7.3 d. Clearly both
fertilization and settlement are more often associ-
ated with the quarter moons than they are with the
full or new moons. The overall relation to the lunar
cycle is revealed more clearly by matching each in-
418
McFARLAM) F.T AI..: RPX'Rl'ITMENT I'ATrKRNS IN FRFCNCH CRUNTS
Table 2. — Comparisons of fertilization and settlement dates for recently recruited postlarval French)
grunts with the lunar cycle and the state of the tides. F and N are full and new moons; S and N are spring
and neap tides; It and U are rising and falling tides of intermediate amplitude between a spring and a neap
tide. The peak date for settlement represents the maximum influx of postlarvae, which occurred on
average 3 d before the maximum number of French grunts appeared on a site. Values are the sums from all
20 census sites. Rows are aligned so that the most likely fertilization date precedes each settlement date.
Vertical lines and summed numbers for days between peaks are best estimates of weekly peaks to yield
the dominant biweekly peaks (see mean values at bottom of table).
Fertilization
Settlement
No.
No. days
Moon
Total no
No. (
days
Moon
Peak
PL-I's
between
phase
Tidal
Peak
PL-1's
between
phase
Tidal
date
in peak
peaks
+ days
state
date
in peak
peaks
+ days
state
_
_
4/7
'18
—
F + 7
U
—
4/22
'13
15
N + 8
li
—
—
5/7
360
15
F + 7
li
—
—
—
'5/14
383
7
13
N + 0
s
5/4
49
—
F + 4
S
5/20
723
6
N + 6
li
—
—
—
'5/26
29
6
13
N+12
It
5/19
48
15
N + 5
11
6/3
930
7
F + 5
li
5/30
18
11
F+ 1
s
6/18
224
15
N + 6
li
6/19
21
20
N + 7
li
7/3
195
15
F + 5
li
^6/28
20
9
14
F + 0
s
—
—
—
—
—
7/3
34
5
F + 5
u
7/17
317
14
N + 5
li
'7/7
21
4
14
F + 9
It
—
—
—
—
—
7/17
19
10
N + 5
u
8/4
324
18
F+10
It
'7/25
16
8
19
F + 0
s
—
—
—
—
—
8/5
18
11
F+ 11
It
8/20
255
16
N+ 10
It
'8/10
8
5
15
N + 0
11
9/2
45
13
F + 9
It
8/20
12
10
N + 10
It
—
—
—
—
—
'8/30
24
10
F + 5
s
9/12
226
10
N + 3
N
9/3
15
4
13
F + 9
s
'9/20
100
8
N + 11
li
'9/12
17
9
N + 3
It
—
—
—
18
—
—
9/16
18
4
N + 7
It
9/30
280
10
F + 6
s
'9/21
11
5
15
N + 12
li
—
—
—
—
—
9/27
20
6
F + 3
It
—
—
—
—
—
'10/2
21
6
11
F + 8
1
10/15
462
15
N + 7
s
10/8
15
5
N + 0
1
'10/21
82
7
17
N + 13
N
'10/14
19
6
12
N + 6
s
10/31
917
10
F + 8
1
10/25
17
6
F+2
1
'11/8
100
8
16
N+ 1
1
'11/2
5
11
F+10
N
11/16
50
8
N + 9
1
11/19
17
8
14
N + 12
N
12/5
199
19
F+13
1
'11/25
5
6
N + 3
1
—
—
—
—
—
12/1
6
6
N + 6
N
—
—
—
—
—
Mean
day
s between peah
;s
inci
uding weel
<ly peak!
3
7.6 ± 1.4 (2 SE)
11.5
± 1
.8 (2 SE)
exc
luding wee
kly peak
S
13.9 ± 1
.6 (2 SE)
15.1
± 1
.1 (2 SE)
Mean
day
s from
F or N
moon
5.5 ± 1
.5 (2 SE)
7.3
± 1.5(2 SE)
'These two peaks are from sites adjacent to the 20 study sites and were abandoned after April.
'The peaks for these dates approximate weekly fertilization and recruitment pulses interspersed be-
tween the biweekly peaks for recruitment (see also Fig. 6).
dividual settlement date and fertilization date to the
time of full moon (Fig. 5). Several features stand out:
1) The settlement data are less noisy than the fertili-
zation data; this is explained, in part, by the more
strongly expressed weekly patterns in the fertiliza-
tion data. 2) Although settlement is clearly associ-
ated with the quarter moons, it does occur during
other periods of the lunar cycle as well (see also
Table 2, Fig. 2). 3) Fewer PL-l's are present on the
sites during full moons than during new moons.
The relation of settlement pulses to daily tidal ex-
cursions (Fig. 6) indicates that settlement was most
often associated with rising or falling (intermediate)
stages of the tidal cycle than with spring or neap
tides. A more extensive evaluation of the results
reveals that out of 22 identifiable settlement pulses,
17 occurred during intermediate tides, 3 with spring
highs, and 2 during neap tides. Also, out of 26 fertili-
zation periods, 16 occurred during intermediate
tides, 7 on spring highs, and 3 during a neap tide.
If a specific state of the moon, such as the quarter
moons, is the significant environmental factor that
determines the timing of fertilization and/or settle-
ment of French grunts, then the state of the tides
419
FISHERY BULLETIN: VOL. 83, NO. 3
Figure 5. -Lunar phase relationships of settlement
and fertilization dates for French grunts. Data repre-
sent the totals obtained from Figures 2 and 3 summed
with reference to the days before and after full
moons. The settlement data are the sum of peak
numbers of PL-l's on all census sites. Actual settle-
ment rates (maximum rate of influx) were maximal 2
to 3 d before the figured peaks. The fertilization data
clearly reveal weaker weekly periods of spawning (see
text for details).
3
O
C
CO
3
o
_l
<
>
cc
<
2000
1500
1000
500
SETTLEMENT
CO ^
O 14
^ 100 I-
u.
O
CC
UJ
50
10
10 14
n FERTILIZATION
I
5
T
0
(-) 14 10 5 0 5 10
DAYS FROM FULL MOON
14 (+)
should be unimportant. This condition would prevail
because the tidal states (springs, neaps, intermediate
conditions) change phase relative to the lunar cycle
as the year progresses (Fig. 6). In contrast, if a par-
ticular state of the tide served as a primary trigger
for fertilization and/or settlement then the moon's
state would be unimportant. To test for the impor-
tance of tidal and lunar state the data were analyzed
using a log likelihood statistic (g-test, Table 3) by
grouping the 22 settlement and 26 fertilization peaks
into the 9 possible combinations of tidal and lunar
state (e.g., spring, neap, and intermediate tides and
full, new, and quarter moons). Clearly both the lunar
cycle and tidal state have significant effects on
settlement and fertilization, but their interaction,
although large, is nonsignificant. Because 60 to 80%
Table 3. — Summary of comparisons of lunar cycle and tidal state for fer-
tilizations and settlement pulses of Frencfi grunts during 1980. Data from
Table 2. Log likelihood test from Sokal and Rohlf (1981).
g-value and associated chi-square
Category
Settlement data
Fertilization data
Total G'
Moon alone'
Tide alone'
Moon-tide'
36.7
11.3
18.0
>x'
001(8)
.01(2)
> X' .001(2) = 1 3.8
7.4 ns < x' .05(4)
= 26.1 22.5 > x' 01(8) = 20.1
= 9.9 7.3 > x' 05(2) = 6.0
10.2 > x' .01(2) = 9-9
= 9.5 4.9 ns < x' 05(4) = 9.5
'Single classification of all categories.
'Single classification of moon or tidal state alone.
'Two-way classification, moon phase versus tidal state.
420
MiFAKLANI) KT AI, : KKCKl'ITMKNT I'AITKRNS IN FRKNCH CRrNTS
DAYS BEFORE AND AFTER FULL MOON
5 14 10 5 0 5 10 15
-»- J I I I I I I I I I \ I I I I I I I I I I ' I I ' ' I I ' I
CO
<
lu
>
I-
o
LU
CO
O
o
1
2
3
4
5
6
7
8
9
10'
[7\
yS>
A
M
©
.<^^
^
f^
1 — I — I — rrr
w
©
O
f
w
•
1
2
~3
^v
4
5
6
\. y z
7
8
•
9
J
10
I — I — I 1 A I 1 — I — I
o
MOON PHASE
T 1 TXT — I — r
T
1 — I — r
P'iGiiRE 6. - Relation between the periodic settlement pulses of postlarval grunts during 1980, the phases of the moon, and the procession of
spring and neap tides. Shaded areas represent relatively uniform series of neap or spring tides; unshaded areas are either increasing or
decreasing intermediate tides (see Table 2). The sequence of days reads from left to right across each row. The first day of each calendar
month is indicated by the letters, e.g., A at top = April 1980 J = January 1981. Closed circles represent the large and intermediate-sized
pulses (> 100 PL-l's); open circles are settlement pulses with < 100 individuals (see Table 2). Closed and open circles with the letter w are
weekly recruitment pulses interspersed between the more common biweekly peaks (see Table 2). The two abruptly changing vertical lines in-
dicate the actual dates of the quarter moons at different times of the year, as determined from the Nautical Almanac for 1980. The mean
deviations of those pulses most closely associated in each month with the quarter moons are: first quarter moon = 1.7 d + 1.9 (SD). third
(juarter moon = 0.9 d + 0.8 (SD). Maximum tidal excursions for spring tides occurred in May and June, and in October and November, as did
the maximum recruitment of PL-l's to the census sites (Fig. 2, Table 2).
of the settlement pulses and fertilizations were
associated with quarter moons and intermediate
tides (Table 2), attempts were made to isolate the
significant categories by combining the data (springs
-I- neaps versus intermediate tides; full + new moons
versus quarter moons). Nonsignificance occurred in
all combinations with the exception of tides and
settlement (g-test = 9.91 > x^,.:,,,, = 3.84).
The relationship between fertilization and settle-
ment of French grunts and the state of the tides and
lunar cycle is obviously complex and difficult to
unravel without ambiguity. Larger sample sizes
(data over several years) would help, but perhaps
more important would be specific data on current
regimes at actual spawning sites and in the general
vicinity of settlement sites. The highly significant but
independent effects of moon and tidal state likely
point at the importance of favorable currents to
successful larval recruitment.
Settlement of Postlarvae in Space and Time
From May through December 1980, when the cen-
sus frequency was high, there were 16 consecutive
quarter-moon periods. On the 20 census sites, there-
fore, a total of 320 separate pulses (16 x 20) could
have been observed if settlement did occur during
the quarter moons. During this period 161 pulses
were actually observed on the 20 sites during
quarter moons. When the number of PL-l's settling
was high, most sites recruited fish (90% for May-
June, 75% for October-November). In winter, when
the number of fish settling was low, recruitment
nevertheless occurred on at least 4 or more sites dur-
ing the quarter moons.
The periodic appearance of PL-l's on 11 of the 20
sites was virtually continuous at each quarter moon,
and similar in general pattern to that depicted by the
pooled data (e.g., site 11, Fig. 2). On 4 sites,
421
FISHERY BULLETIN: VOL. 83. NO. 3
however, PL-l's settled in spring-summer or in
summer-fall. These differences in the pattern of
settlement between the census sites are highly signi-
ficant (P « 0.001, "distribution-free" nonparametric
test; Hollander and Wolfe 1973, p. 139-146). The
patterns were so consistent, however, that we were
soon able to predict with considerable success not
only when, but which sites would attract PL-l's. We
can provide no correlations with depth or area of a
site, nor with the species of corals and other major
residents (fishes, sea urchins, etc.), as to why some
sites consistently "attracted" postlarval grunts and
others varied, even though it is known that post-
larval settlement can be partly governed by priority
effects on reefs (Shulman et al. 1983). To understand
the characteristics of a site that make it highly
"attractive" to settling postlarval grunts will require
sophisticated field manipulations.
DISCUSSION
The most conspicuous features concerning the
recruitment of French grunts from the plankton are
the rhythms in settlement and fertilization dates
(Figs. 2-4). The continuing and short 15-d periods of
these rhythms over an entire year contrast with
other coral reef fishes where settlement, although
rhythmic, is concentrated mostly around a particular
period of the year (Williams and Sale 1981). Settle-
ment in reef fishes is often episodic; it may show a
lunar periodicity (Johannes 1978), it may be monthly
but not coupled to a particular phase of the moon
(Williams 1983 -mixed guild of pomacentrids), or a
rhythm may not be conspicuous (Victor 1982, 1983 -
Thalassoma bifasciatum).
The short period between fertilization and settle-
ment implies that pelagic existence in French grunts
is of short duration (about 2 wk; Brothers and
McFarland 1981). To estimate the days spent in the
plankton, the average age for the smallest 100
PL-l's was calculated from the sample of 1,478 fish
that were used to estimate the actual day of fertiliza-
tion [mean age = 15.7 d ± 2.1 (SD). range = 13-20;
mean length (SL mm) = 6.9 ± 0.67 (SD), range =
5.9-8.5]. If each of these fish had settled from the
plankton over the previous day, then pelagic exist-
ence (about 15 d) agrees with the periodicity of ferti-
lization and settlement (Table 3, Fig. 4). In contrast,
the pelagic existence of most other coral reef fishes
investigated exceeds 15 d (Randall 1961; Johannes
1978; Sale 1980; Bariow 1981). This has been veri-
fied by results for age at settlement as determined
from otoliths (Victor 1982, 1983; Brothers et al.
1983; Brothers and Thresher in press and unpublish-
ed; Thresher and Brothers in press). Most of these
fishes settled at various ages: Thalassoma bifascia-
tum, 40-72 d; Paragobiodon melanosoma, 39-47 d;
Gobiodon sp., 27-38 d; several unidentified scarids,
34-58 d; and lab rids, 21-56 d. Direct aging of new
recruits or otolith counts to presumed settlement
marks rarely yield ages as low as found for the
French grunt. Examples of species with pelagic
phases of 20 d or less include the angel fish, Holacan-
thus paru (Brothers and Thresher in press); several
damselfishes, Glyphidodontops rollandi, Pomacen-
fyits amboinensis, P. popei, and P. wardii; the blenny
Petroscirtes mitratus; the nemipterid Scolopsis
dubiosus (Brothers et al. 1983); and the goby Gobio-
soma prochilos (Brothers, unpubl. data). These may
be exceptional cases; all or at least most of these
species represent families characterized by having
larval durations moderately to considerably longer
than found in grunts. At the family level, therefore,
only the haemulids, and perhaps the lutjanids, pro-
vide evidence of a short pelagic existence. In support
of this conclusion is the lack of haemulids or lutjanids
amongst the larval fishes collected offshore through-
out the Caribbean (Richards 1981, footnote 8). Are
haemulids programmed for short larval lives? We
cannot be sure, but out of the 1,478 recently settled
French grunts we have aged, not one exceeded 20 d
from fertilization. Such a developmental process
would be crucial in their survival; if they do not drift
over suitable substrates on which to settle after 2
wk, they would perish offshore.
Our observations of a strong semilunar periodicity
in French grunt recruitment, coupled with what
seems to be a relatively fixed or invariant larval
duration, could be the result of a number of different
combinations of spawning and survivorship. Because
we can only determine fertilization dates for indivi-
duals that have successfully recruited, we cannot be
certain whether the apparent periodicity in spawn-
ing is an accurate representation of the temporal pat-
tern of grunt reproduction. At the other extreme, it
may be the result of relatively continuous spawning
activity, the products of which survive differentially
with respect to semilunar environmental variables.
Surprisingly, for such common fishes, little is
known about spawning in haemulids. They produce
pelagic eggs and larvae (Breder and Rosen 1966;
Saksena and Richards 1975). Recently, paired
spawning has been described for Hapalogenys
mucronatus in aquaria (Suzuki et al. 1983). On six
*W. Richards, Southeast Fisheries Center, National Marine
Fisheries Service. NOAA. 75 Virjcinia Beach Drive, Miami. P^L
33149-1099, pers. commun. October 1980.
422
McFARLANP ET AI..: RKCKl'ITMENT PATTERNS IN FRENCH GRUNTS
specific attempts to validate spawning in French
grunts in the sea at St. Croix, two of us (McFarland
and Shulman) failed to observe reproductive activity
during dusk, but we did observe what appeared to be
sporadic spawning by small groups of tomtate
grunts, Haemulon aurolineatum, within large
schools of these fish. These limited data suggest that
grunts, like many reef fishes, cast pelagic eggs into
the water column at dusk. We emphasize, however,
that there are no data about their daily spawning
habits.
Two hypotheses offer explanations for the domi-
nant semilunar periodicity of fertilization and settle-
ment.
Hypothesis 1. Assumption: Spawning follows a
semilunar rhythm with breeding peaks closely cou-
pled to the quarter moons (and/or intermediate
monthly tides). If reproductive activities in French
grunts follow a semilunar cycle, and pelagic life is
programmed for 15 d, then settlement should occur
most often during the quarter moons and interme-
diate monthly tides, which it does (see Table 3, Fig.
6). This hypothesis, however, does not account for
the weekly peaks in settlement and fertilization
(Table 3; Figs. 2, 3, 5), which contradict the assump-
tion of the hypothesis.
Hypothesis 2. Assumption: Spawning is relatively
constant from day to day, and larval existence
restricted to about 15 d. Consistent daily reproduc-
tive effort could produce a continuous pool of grunts
in the plankton. As a result, only those larvae that
are favored by "correct" currents that disperse them
inshore around 15 d will settle, and/or successful
recruitment may also depend on favorable currents
dispersing the eggs at the time of reproduction. At
St. Croix we suspect that current conditions are
most favorable to settlement during the quarter
moons and intermediate tides. The weekly peaks
that are associated with full and new moons (Table 3)
could represent recruitment in less favorable cur-
rents than occur around the quarter moons. These
currents, nevertheless, must allow some larv^ae
through the "filter screens" that all recruits must
pass through to join a reef community (Smith 1978).
The semilunar rhythm of fertilization and settlement
observed in settling grunts would, under this hypo-
thesis, be explained by semilunar rhythms in cur-
rents favorable to settlement.
The time of day when settlement occurs and, espe-
cially, the amount of darkness at night may also
relate to successful settlement. Although data are
scarce, some reef fishes settle from the plankton at
night (e.g., acanthurids- Randall 1961; McFarland,
unpubl. data). We do not have similar direct observa-
tions for French grunts, but we suspect settlement is
nocturnal because the number of PL-l's remained
fairly constant on most census sites throughout each
day. Nocturnal settlement behaviors would tempora-
rily remove recruits from the attack of reef pisci-
vores, especially if accomplished during the dark of
the moon. During full moons, recruits presumably
would be subject to higher rates of predation by
planktivores than during other phases of the moon
(Hobson et al. 1981). The number of grunts settling
during full moons should be low, which it is (Fig. 4).
In contrast, if length of darkness is a dominant factor
to successful settlement, then the highest influx of
recruits should coincide with the new moons, and
intermediate numbers with quarter moons, which
they do not (Fig. 4). The recruitment dynamics,
nevertheless, indicate higher influxes of PL-l's when
some degree of darkness occurs during each night
(Fig. 4). We hypothesize that recruitment is depen-
dent primarily on favorable currents, with predation
possibly acting as a secondary selective force.
Reversals in surface currents and oppositely flow-
ing currents in the upper 30 m, which could affect
the dispersal of larvae, are known to occur at St.
Croix and at Puerto Rico (Gladfelter et al. 1978; Lee
et al. 1978; Molinari et al. 1980). Their local patterns,
however, remain unknown. Eddy formation to the
west of the island of Barbados, produced by Karmen
trails as the generally west-setting current passes
the island, has also been postulated to retain the pela-
gic stages of inshore species (Emery 1972). It is
reasonably well established that seasonal shifts in
local current gyres in the vicinity of Hawaii favor the
settlement of various species of reef fishes (Sale
1970, 1980; Johannes 1978). In addition, spawning is
often synchronized to disperse eggs and lan-ae away
from reefs and into offshore currents (Johannes
1978; Lobel 1978). But specific currents do not
always trigger spawning, as Colin (1982) reported
for several reef fishes at Puerto Rico. In these in-
stances, rhythmic spawning often can be related to
the lunar cycle, but significantly, some species spawn
every day. Depending on the time of spawning,
dispersal routes for fish eggs and larvae can vary
over short-time periods because of reversals in cur-
rents.
The daily behaviors and distributions of grunts at
sea are unknown. Do larval grunts passively drift
with currents? Or do they seek different depths at
different times of the day? Active behaviors that
would utilize differences in currents have been in-
voked to explain the retention of pelagic larval fishes
and invertebrates close to the island of Oahu (Leis
1982). Similar activities by larval French grunts
423
FISHERY Bl'LLETIN: VOL. 83, NO. 3
could explain their absence in collections taken off-
shore (Richards 1981).
We have provided substantial evidence that
French grunts recently recruited from the plankton
are fertilized about 15 d earlier, and that these pro-
cesses most closely correlate with the quarter moons
and intermediate tidal excursions. Is this a general
pattern that occurs throughout the Caribbean and
western Atlantic where French grunts are most
abundant? Or is the lunar-tidal correlation the result
of local conditions? We have no answer at present,
because it requires repeating the investigation in
other localities. Different current regimes and local
hydrographic conditions in other regions might elicit
different recruitment patterns. The much weaker
weekly fertilization and settlement patterns, for ex-
ample, that are associated with full and new moons
(Table 3) might dominate recruitment in other
locales.
There is a seeming order in the rain of young
French grunts from the plankton. Over the period of
this study young grunts following a semilunar time-
table appeared on over half of the census sites 70%
of the time (range 59 to 94%). Although we could not
discern any special characteristics of these sites that
attracted grunts, the sites were never preoccupied
by other species. Settlement certainly did not appear
to be a random phenomenon. The recurrent order in
the occupation of space by settling French grunts,
however, may reflect only their high abundance in
the reef communities at St. Croix (Gladfelter and
Gladflelter 1978). Large populations produce large
numbers of offspring and this alone might swamp
available sites. In this regard we stress that the cen-
sus settlement sites are not main reefs, but isolates
adjacent to them. Indeed, large coral domes in the
census area which sustained large populations of
older juvenile French grunts never sustained popula-
tions of PL-l's. Without manipulative studies of
grunts on the settlement sites, however, it is impossi-
ble to ascertain to what extent recruitment is in-
fluenced by a resident population (Shulman et al.
1983). We can conclude only that the recruitment of
French grunts from the plankton has high temporal
and spatial predictability at St. Croix.
Fishes in the family Haemulidae represent a domi-
nant component of the tropical reef fish community
and constitute a major part of the trap fishery in
western Atlantic and Caribbean waters (Dammann
1980; McFarland 1980). The findings presented in
this study provide insights that are critical to the
management of any fishery for grunts. For example,
the relatively short larval existence in French
grunts, which also occurs in white and tomtate
grunts (Brothers and McFarland 1981), implies that
dispersal does not occur over very long distances.
Whether local populations of grunts are self-sustain-
ing or dependent on interisland transport is
unknown. Answers will require precise knowledge of
spawning habits of each species of grunt, careful
analysis of local and general current regimes, and, if
possible, the behavior of the larvae. If local popula-
tions are self-sustaining, then overly lenient limits on
the harvest of adult grunts could seriously limit
recruitment. In contrast, if recruitment shows large
spring and fall peaks in other species of grunts, as it
does in French grunts, and the seasonality in recruit-
ment is geographically widespread (e.g. Munro et al.
1973), then closure of a grunt fishery for a few mon-
ths during periods of peak recruitment would prob-
ably assure maintenance of the local populations.
ACKNOWLEDGMENTS
We thank Jack Sobel for his technical help in con-
tinuing the daily census routines when we could not
be present, and Kim Benson who assisted in the
otolith analysis. Numerous students at the West In-
dies Laboratoiy assisted as diving buddies; we thank
them all. This project was supported by National
Science Foundation Grant OCE-7918569.
LITERATURE CITED
Barlow. G. W.
1981. Patterns of parental investment, dispersal and size
among coral-reef fishes. Environ. Biol. Fishes 6:65-8.5.
Batschelet, E.
1965. Statistical methods for the analysis of problems in
animal orientation and certain biological rhythms. Am. Inst.
Biol. Sci., Wash., DC, 57 p.
Breder, C. M., and D. E. Rosen.
1966. Modes of reproduction in fishes. Nat. Hist. Press,
Garden City, NY, 941 p.
Brothers, E. B., and W. N. McFarland.
1981. Correlations between otolith microstructure, growth,
and life history transitions in newly recruited French grunts
[Haemulon flavolmeatum (Desmarest), Haemulidae]. Rapp.
P.-v. Reun. Cons. Perm, int Explor. Mer 178:369.374.
Brothers, E. B., and R. E. Thresher.
In press. Pelagic duration, dispersal and the distribution of
Indo-Pacific coral-reef fishes. NOAA Symp. Ser. Undersea
Res., Vol. 3.
Brothers, E. B., D. McB. Williams, and P. F. Sale.
1983. Length of larval life in twelve families of fishes at "One
Tree Lagoon", Great Barrier Reef Australia. Mar. Biol.
(Berl.) 76:319-324.
Colin, P. L.
1982. Aspects of the spawning of Western Atlantic reef
fishes. NOAA Tech. Memo. NMFS-SEFC-80, p. 69-78.
Dale, G.
1978. Money-in-the-bank: a model for coral reef fish existence.
Environ. Biol. Fishes 3:103-108.
424
McFARLAND ET AL.: RECRUITMENT I'A'ITERNS IN FRENCH GRfNTS
Dammann, a. E.
1980. Caribbean reef fish: fish traps and management. Proc.
Gulf Caribb. Fish. Inst. 32:100-105.
Emery, A. R.
1972. Eddy formation from an oceanic island: ecological
effects. Caribb. J. Sci. 12:121-128.
Gladfelter, W. B., and E. H. Gladfelter.
1978. Fish community structure as a function of habitat struc-
ture on West Indian patch reefs. Rev. Biol. Trop. (Suppl. 1)
25:65-84.
Gladfelter, W. B.. E. H. Gladfelter, R. K. Monahan, J. C.
Ogden, and R. F. Dill.
1978. Environmental studies of Buck Island Reef National
Monument. U.S. Dep. Inter., Rep. Natl. Park Serv., 124 p.
Helfman, G. S.
1978. Patterns of community structure in fishes: summary
and overview. Environ. Biol. Fishes 3:129-148.
Helfman, G. S., J. L. Meyer, and W. N. McFarland.
1982. The ontogeny of twilight migration patterns in grunts
(Pisces: Haemulidae). Anim. Behav. 30:317-326.
HOBSON, E. S.
1968. Predatory behavior of some shore fishes in the Gulf of
California. U.S. Fish Wildl. Serv., Res. Rep. 73, 92 p.
HoBsoN, E. S., W. N. McFarland, and J. R. Chess.
1 98 1 . Crepuscular and nocturnal activities of Calif ornian near-
shore fishes, with consideration of their scotopic visual pig-
ments and the photic environment. Fish. Bull., U.S. 79:1-30.
Hollander, M., and D. A. Wolfe.
1973. Nonparametric statistical methods. John Wiley and
Sons, Inc., N.Y., 503 p.
Johannes, R. E.
1978. Reproductive strategies of coastal marine fishes in the
tropics. Environ. Biol. Fishes 3:65-84.
Lee, T. N., R. S. C. Munier, and S. Chiu.
1978. Water mass structure and variability north of St. Croix,
U.S. Virgin Islands, as observed during the summer of 1977
for OTEC assessment. Rosenstiel Sch. Mar. Atmos. Sci.,
Univ. Miami, Tech. Rep. 78004, 81 p.
Leis, J. M.
1982. Nearshore distributional gradients of larval fish (15
taxa) and planktonic crustaceans (6 taxa) in Hawaii. Mar.
Biol. (Berl.) 72:89-97.
Lobel, p. S.
1978. Diel, lunar, and seasonal periodicity in the reproductive
behavior of the pomacanthid fish, Centropyge potteri, and
some other reef fishes in Hawaii. Pac. Sci. 32:193-207.
McFarland, W. N.
1980. Observations on recruitment in haemulid fishes. Proc.
Gulf Caribb. Fish. Inst., 32:132-138.
In press. Overview: the dynamics of recruitment in coral reef-
organisms. NOAA Symp. Ser. Undersea Res., Vol. 3.
McFarland, W. N., and Z.-M. Hillis.
1 982 . Observations on agonistic behavior between members of
juvenile French and white grunts-family Haemulidae. Bull.
Mar. Sci. 32:255-268.
McFarland, W. N., and N. M. Kotchian.
1982. Interaction between schools of fish and mysids. Behav.
Ecol. Sociobiol. 11:71-76.
McFarland, W. N., and J. C. Ogden.
In press. Recruitment of young coral reef fishes from the
plankton. NOAA Symp. Ser. Undersea Res., Vol. 3
McFarland, W. N., J. C. Ogden, and J. N. Lythgoe.
1979. The influence of light on the twilight migrations of
grunts. Environ. Biol. Fishes 4:9-22.
MoLiNARi, R. L., D. K. Atwood, C. Duckett, M. Spillane, and
I. Brooks.
1980. Surface currents in the Caribbean Sea as deduced from
satellite tracked drifting buoys. Proc. Gulf Caribb. Fish.
Inst, 32:106-113.
MtiNRO, J. L., V. C. Galt, R. Thompson, and P. H. Reeson.
1973. The spawning seasons of Caribbean reef fishes. J. Fish
Biol. 5:69-84.
Ogden, J. C, and P. R. Ehrlich.
1977. The behavior of heterotypic resting schools of juvenile
grunts (Pomadasyidae). Mar. Biol. (Berl.) 42:273-280.
Ogden, J. C, and J. C. Zieman.
1977. Ecological aspects of coral reef - seagrass bed contacts
in the Caribbean. In D. L. Taylor (editor), Proc. Third Int.
Coral Reef Symp., Vol. 1, p. 378-382. Rosenstiel Sch. Mar.
Atmos. Sci., Univ. Miami, Miami, F^L.
Randall, J. E.
1961. A contribution to the biology of the convict surgeonfish
of the Hawaiian Islands, Acanthurus triostegns sandvicensis.
Pac. Sci. 15:215-272.
Richards, W. J.
1981. Kinds and abundance of fish larvae in the Caribbean
Sea. Rapp. P.-v. Reun. Cons. Perm. int. Explor. Mer 178:
240-241.
Ricklefs, R. E.
1979. Ecology. 2d ed. Chiron Press, N.Y., 966 p.
Saksena, V. P., and W. J. Richards.
1975. Description of eggs and larvae of laboratory- reared
white grunt, Haem.ulon plumi£ri. (Lacepede) (Pisces, Poma-
dasyidae). Bull. Mar. Sci. 25:523-536.
Sale, P. F.
1970. Distribution of larval Acanthuridae off Hawaii. Copeia
1970:765-766.
1977. Maintenance of high diversity in coral reef fish commu-
nities. Am. Nat. 111:337-359.
1978. Coexistence of coral reef fishes- a lottery for living
space. Environ. Biol. Fishes 3:85-102.
1980. The ecology of fishes on coral reefs. Oceanogr. Mar.
Biol., Annu. Rev. 18:367-421.
Shulman, M. J., J. C. Ogden, J. P. Ebersole, W. N. McFarland,
S. L. Miller, and N. G. Wolf.
1983. Priority effects in the recruitment of juvenile coral reef
fishes. Ecology 64:1508-1513.
Smith, C. L.
1978. Coral reef fish communities: a compromise view.
Environ. Biol. Fishes 3:109-128.
SoKAL, R. R., and F. J. ROHLF.
1981. Biometry. The principles and practice of statistics in
biological research. W. H. Freeman and Co., San Francisco,
859 p.
SuztJKi, K., S. HiOKi, Y. Tanaka, and H. Kitazawa.
1983. Spawning and early life historj' of Hapalogenys mucro-
natus (EYDOUX et SOULEYET) (Pisces: Pomadasyidae) in
an aquarium. J. Fac. Mar. Sci. Technol., Tokai Univ. 16:183-
191.
Thresher, R. E.
1984. Reproduction in reef fishes. T.F.H. Pub!., Neptune
City, NJ, 399 p.
Thresher, R. E., and E. B. Brothers.
In press. Reproductive ecology and biogeography of Indo-
West Pacific angelfishes (Pisces: Pomacanthidae). Evolu-
tion.
Victor, B. C.
1982. Daily otolith increments and recruitment in two coral-
reef wrasses, Thalassoma bifasciatum and Halwkoeres biint-
tatus. Mar. Biol. (Beri.) 71:203-208.
425
FISHERY BULLETIN: VOL. 8:^. NO. 3
1983. Recruitment and population dynamics of a coral reef Williams, D. McB., and P. F, Sale.
fish. Science (Wash.. DC) 219:419-420. 1981. Spatial and temporal patterns of recruitment of juvenile
Williams, D. McB. coral reef fishes to coral habitats within "One Tree Lagoon",
1983. Daily, monthly and yearly variability in recruitment of a Great Barrier Reef. Mar. Biol. (Berl.) 65:245-253.
guild of coral reef fishes. Mar. Ecol. 10:231-237.
426
THE HARBOR PORPOISE, PHOCOENA PHOCOENA, IN
FISH HARBOUR, NEW BRUNSWICK, CANADA:
OCCUPANCY, DISTRIBUTION, AND MOVEMENTS
David E. Gaskin and Alan P. Watson^
ABSTRACT
The distribution, movements, and relative population abundance of harbor porpoises were studied in the
Fish Harbour region of New Brunswick, Canada (lat. 44°59'30"-45°0r00"N, long. 66°54'00"-66°57'00"W),
from 1970 to 1978. In any given year numbers of this species were highest in the region between late July
and early September. This is also the period during which surface temperatures attain a maximum
(10°-12°C) and the largest herring, Clupea harengus, catches are usually made. During July-September the
porpoise population of the inner (western) part of the study area contained 63% mothers with calves.
Changes in relative population abundance were most strongly related with time of year (increasing from
early July), tidal amplitude (most present when amplitude is 6.5 m or less), and wind phase (most present
during onshore winds). Observation of recognizable individuals revealed consistent specific "territories" and
patrolling patterns. A marked decrease in relative abundance in the latter half of the 1970s was noted. This
decrease was coincident with a decline in mean midsummer surface temperature over 1974-78 of about 1°C.
Unfortunately it was not possible to determine from existing data if major changes in availability of prey
species also occurred in the inner Quoddy region during the same period.
Literature concerning ecology of the harbor por-
poise, Phocoena phocoena, has been largely restricted
to reports of nonquantitative or casual observations
(Scheffer and Slipp 1948; M<)hl-Hansen 1954; Amun-
din and Amundin 1974), although more recently
Gaskin (1977), Prescott et al. (1981),^ Flaherty and
Stark (1982),3 Kraus et al. (1983)," and Taylor and
Dawson (1984) have presented information from
surveys and some population estimates for limited
areas of both east and west coasts of North America.
A population estimate for the Copper River area of
Alaska was provided by Matkin and Fay (1980).
Habitat indices, relating occurrence of animals in
coastal waters to various environmental factors have
been given by Smith and Gaskin (1983) and Watts
'Department of Zoology. Universitv of Guelph, Guelph, Ontario
NIG 2W1, Canada.
2Prescott, J. H., S. D. Kraus, P. Fiorelli, D. E. Gaskin, G. J. D.
Smith, and M. Brander. 1981. Harbor porpoise (Phocoemi
phocoena): Distribution, abundance, survey methodology and
preliminary notes on habitat use and threats. Final report to U.S.
Department of Commerce, NOAA, National Marine Fisheries Ser-
vice Contract 80-FA-d-00009, 61 p.
^Flaherty, C, and S. Stark. 1982. Harbor porpoise (Phocoena
phocoena) assessment in "Washington Sound". Final report for
Subcontract 80-ABA-3584, NOAA, NMFS, National Marine
Laboratory, Seattle, WA, 84 p.
^Kraus.'S. D., J. H. Prescott. and G. S. Stone. 1983. Harbor
porpoise, Phocoena phocoena, in the U.S. coastal waters of the Gulf
of Maine. A survey to determine seasonal distribution and abun-
dance. A report to the National Marine Fisheries Service, Woods
Hole, Massachusetts, July 1983, 15 p.
Manuscript accepted October 1984.
FISHERY BULLETIN: VOL. 83. NO. 3. 1985.
and Gaskin (in press), and some radiotelemetric
studies of distribution and movements by Gaskin et
al. (1975) and Read and Gaskin (1983, in press).
In order to gain insight into the nature of local
distributions and movements of P. phocoena over an
extended period, we selected a semi-enclosed area of
limited size in southern New Brunswick, Canada.
Preliminary observations had already shown that the
species was common in the area, and locality (about 8
km- maximum) bounded approximately by lat.
44°59'30"-45°59'00"N, long. 66°54'00"-66°57'00"W
on the east coast of Deer Island (Fig. 1) was easily ac-
cessible for research and relatively sheltered. We
were also aided by the occurrence in the area of
several recognizable porpoises with surface
disfigurements, large blemishes, or distinctive
pigmentation patterns visible at some distance in
favorable light; several of these animals were pres-
ent in successive seasons.
CHARACTERISTICS OF
THE STUDY AREA
(Figure 1)
Average depths range from about 8 m in Lords
Cove to about 22 m in Simpson's Passage (respective
maxima 20 m and 60 m) at mean low water. The
region is subject to anomalistic, semidiurnal tides of
427
FISHERY BULLETIN: VOL. 83, NO. 3
Figure 1. -The Fish Harbour region on the east coast of Deer Island region, New Brunswick, Canada (see inset). Legend: Straight solid lines
indicate approximate limits of study area. Stipple indicates shallow shelf area (low water mark to 5 m); widely spaced vertical lines indicate
areas of relatively gentle slope; narrowly spaced bars indicate steep scarps or slopes terminating in cliffs and the white areas (other than
within island boundaries) are relatively deep basins and channels. Broken line shows regular track of boat with watch-stations 1 and 2. Place
names are those used in the text. Scale = 1 km.
5.6-8.3 m (mean about 6.3 m) (Forrester 1960).
Water turbidity is high (Secchi disk reading in July-
August about 2 m). Most tidal flow from the area is
by the northern end of Simpson's Passage. Salinities
in the whole Quoddy region (Trites 1962) range from
29.57oo (March-May) to 32.3%o (September). Lower
salinities in shallow inshore waters occur after heavy
rain and may last for several days. While some year-
to-year changes in mean surface temperature were
recorded (Trites 1962, fig. 11), one of the most com-
plete series (for 1978) provides a typical sequence of
the relative changes from spring to autumn. Late
May-early June surface temperatures ranged from
6.0° to 7.1°C, mid-July from 8.4° to 9.6°C, and mid-
August-early September from 10° to 11.2°C. By
early December the waters were 7°C again. Peak
summer values of 11.3°-14.5°C were only obtained
in mid-August at the head of Lords Cove in shallow
water (< 5 m). At any given time surface tempera-
tures were 0.5°-1.0°C warmer than those at 12 m
despite the tidal mixing which obviously occurred. A
general pattern of temperature profiles could be
recognized in midsummer: The inner (western) part
of Fish Harbour was vertically well-mixed through-
out, but a rather steep horizontal gradient of about
1.0 °C was maintained at all depths on the outer
margin of this zone. In the central region (near Fish
Island) the direction of water movement showed up
to 90° variation at different depths at any given time
of rapid tidal flow. The outer parts of Fish Harbour,
and Simpson's Passage, tended to be well-mixed ver-
tically, but were always about 0.5° cooler at the sur-
face on the ebb. North of Adam Island there was a
shift from horizonal gradients on flood to vertical
gradients on the ebb. The inshore water is probably
"trapped" in the bight of the harbor, i.e., with an ex-
tended residency time, while movement of water in
and out the northern and southern entrances prob-
ably creates some mixing in the outer and central
part of Fish Harbour. More detail of the static and
dynamic characteristics of the study area and adja-
cent regions is provided by Smith et al. (1984).
428
GASKIN and WATSON: HARBOR PORPOISE
METHODS
Most observations were made from a 5 m two-
seater kayak (weather permitting), which appeared
to exercise a negligible effect on the behavior of
animals even at short distances (Watson 1976). A
small fishing boat was used above Beaufort wind
force 2, but this craft lacked the silent
maneuverability of the kayak. Few publishable
photographs were obtained because this species is an
exceedingly difficult photographic subject. The
method of making and maintaining contact was con-
sistent throughout the study period (1 June 1970-10
September 1978). A central route from the head of
Lords Cove was followed (Fig. 1); unless weather
was too poor for optimal sighting in Simpson's
Passage, or there was specific intent to track a group
within Fish Harbour, the boat continued on track to
watch-station 2 (Fig. 1). If no animals were present
in Fish Harbour and conditions were less than Beau-
fort wind force 2, the boat would remain in the vicin-
ity, but if the animals were already within Fish Har-
bour, the boat usually returned to watch-station 1 in
outer Fish Harbour, from which point most of the
study area normally used by porpoises could be kept
under eye or binocular surveillance. As weather per-
mitted, or presence and movements of animals dic-
tated, this search pattern was usually repeated dur-
ing the day at invervals of several hours. When
porpoises were located either visually or from the
sound of their expirations, the position of the boat
and the initial positions of animals relative to the
vessel were recorded to within a few tens of meters
by taking 3-5 bearings from the many surrounding
landmarks. Subsequent positions were noted in those
cases when movements were tracked for extended
periods, providing the animals surfaced long enough
for accurate bearings to be taken and had moved to a
significant distance (ca. 100 m) from the previous
location. The time, location, size, and apparent com-
position of each porpoise group was recorded on and
later transcribed from tape. The particular problems
of quantifying sightings of this small cetacean have
been considered by Gaskin (1977), Prescott et al.
(footnote 2), Taylor and Dawson (1984), Kraus et al.
(footnote 4, 1983), and Watts and Gaskin (in press).
During the present study we used only data obtained
in Beaufort Sea state 0-1, when visibility was
unlimited within the study area and lighting was
direct or diffuse, but uniform. In these ideal condi-
tions some porpoises can be detected even from the
air (250 m) at 650 m, although this is the least satis-
factory method for sighting this species (Kraus et al.
1983). In a simultaneous comparison of effectiveness
of stationary, mobile, and aerial observers (Kraus et
al. 1983) the former, whether on land or stationary
vessel, not only saw far more animals than the
observers in the aircraft, but could detect them using
binoculars in calm water at 1,000 -(- m. The prob-
bability of contact is enhanced when animals tend to
surface repeatedly. The present authors found that
porpoises working near the Nub close to the Simp-
sons Island (Fig. 1) could be clearly seen with binocu-
lars from watch-station 1, at a distance of > 1 km in
optima] conditions.
Some natural constraints on distribution of por-
poises within the study area reduced the effective
survey region to only 4 km-. Virtually no animals
ventured farther inshore than the shallow shelf edge
(ca. 5 m) even during high water. Almost all ingress
and egress was between Bean and Fish Islands (Fig.
1). Very few animals left by the southern passage
from Lords Cove, and only two were ever noted to
enter this way. Only one group of animals consistent-
ly visited Lords Cove in any case. No movement was
noted through the narrow gut west of Hardwood
Island, and only infrequent movement (< 5%)
through the passage north of Fish Island.
Harbor porpoises in the Quoddy region appeared
generally indifferent to boat traffic (Watts and
Gaskin in press), with no noticeable attraction bias as
noted for Phocoenoides dalli by Kasuya and Jones
(1984). Because of the small size of the study area,
the impossibility of making random transects, the
highly clumped distributions, and nonrandom move-
ments of animals (see latter), any kind of line-
transect approach was inappropriate. From a
combination of the initial strip census search and the
stationary observations, we concentrated on obtain-
ing a "best estimate" of the mean number of animals
present during each observation period with
reference to each hour of the day and each tide sub-
phase within that period. All are minimum estimates
because some animals were probably missed at the
seaward periphery of the study area. We tried to
avoid inclusion of repeat sightings in these estimates
which would lead to an upward bias, except where
we calculated simple sightings of individuals per
hour. The "best estimate" data were used to give
relative abundance with respect to various en-
vironmental conditions, while sightings per hour
were more appropriate for time-based comparisons
such as relative abundance from year to year.
When sighting conditions were particularly favor-
able, the movements of specific groups were plotted,
either by observation from one or other watch-
stations which commanded a wide view with many
landmarks, or by discreetly following them in the
429
FISHERY BULLETIN: VOL. 83. NO. 3
kayak on a parallel course at distances of 50-150 m.
If only one observer was present in the kayak, these
periods were only included in the main data base
if very few animals were known to be in the study
area.
STATISTICAL ANALYSIS
For statistical analyses of these data we con-
sidered the potential application of log-linear and
multivariate models, principle component analysis
(PCA), factor analysis (FA), and a categorical data
(x^) procedure. Considerable differences in the
magnitude of x-variate variances would make results
from PCA or FA suspect (Maxwell 1977, ch. 4). Log-
linear and multivariate approaches were initially
attractive, but both have disadvantages. Tests for in-
dependence of x-variates are difficult in the latter,
and while these are facilitated by the former, results
obtained from log-linear models are often difficult to
interpret (SAS Institute Inc. 1979, p. 222). Further-
more, statistical advisers noted that use of the whole
data base was contraindicated in either method
because 1) there was of necessity inclusion of linear,
nonlinear, and enumeration data types, and 2) there
were significant numbers of empty data cells usually
resulting from poor weather when operation would
have been pointless. The consultants recommended
use of the categorical data procedure, not only for
the reasons outlined above, but also because the very
nature of the x-variates (e.g., lunar cycle and tidal
cycle) precluded the existence of complete indepen-
dence. From the ecological point of view it was con-
sidered more important to relate one dependent
variable (relative abundance of porpoises) to a group
of variables one at a time than to test for indepen-
dence in the latter when the result would likely be
spurious.
We first determined (P = 0.13 -^ ) that no data set
from any x-variate was significantly associated with
one part of the "range" of any other by a series of
simple paired x^ tests. The main analyses were then
carried out on an IBM^ 360 mainframe computer
using the PROC FREQ program (SAS Institute Inc.
1979) which used a generalized least squares model
to generate x^ values for combinations of the
categorical levels between variables. In this case the
relative abundance was related to date, time of day,
tidal amplitude, tidal phase, lunar phase, extant wind
direction, and wind direction 24 h previously.
To examine changes in spatial distribution within
^Reference to trade names does not imply endorsement by the Na-
tional Marine Fisheries Service, NOAA.
the Study area, the location of 669 porpoise sightings
collected in 1973-75 were plotted with respect to
chronological time and time of tide. To avoid repeat
sightings only the initial sighting was used in this
context. To examine possible changes in distribution
by depth and location, the study area was divided in-
to three zones based on subsurface features: shallow
shelving areas, subsurface slopes and scarps, and
relatively deep basins and channels (Fig. 1). Such
data cannot be used to deduce actual patterns of
movement, but we were able to obtain some informa-
tion on these through selective observations of iden-
tifiable individuals. Five of these were known to be
females (consistently accompanied by calves), one a
male (seen briefly copulating with a known female),
and one of unknown sex. Each recorded sequential
position was plotted for movements within a specific
observation period, and for four of the known
females data on all observations were plotted and the
apparent ranges in consecutive seasons examined. In
each case the master sheets had a grid with ordinates
100 m apart.
RESULTS
Hours of Observation of Porpoises in
Fish Harbour Region
About 550 h of observation were made between
June 1970 and September 1978, and 324 h of this
were during an "intensive" study phase encompass-
ing the summers of 1973-75. Estimates of changes in
relative abundance with respect to environmental
parameters were based on 181 h in optimal sighting
conditions in this period (see section on Methods).
Sporadic observations were maintained by our
research group subsequent to 1975 or by auxilliary
observers from Marine Research Associates of Lords
Cove in most months except for late-December to
mid-January.
Changes in Relative Abundance
During the Year
From low relative abundance in the spring and late
fall months, numbers of porpoises were highest dur-
ing August or September in each year of the study
period (Table 1). Highest values in ideal conditions
were 8.00/h in Fish Harbour and 7.72/h in Simpson's
Passage in September 1973 and August 1974 respec-
tively. Observations by Marine Research Associates
over the period 1971-77 in the same area, although
largely of a casual nature, confirmed the animals can
occur in small numbers in any month between Octo-
430
(lASKIN ami WATSON: HARBOR POKCOISK
Table 1. — Sightings of harbor porpoises per hour in the Simpson's Passage and Fish Harbour areas, southern New Brunswick,
1970-78.
Month
1970
1971
1972
1973
1974
1975
1976
1977
1978
Simpson's Passage
Anril 'O
2
May
0.61 ±'0.07
0
0
—
—
—
—
—
June
0
0.90 ±0.20
0.50 ±0.15
0
—
—
—
0
0.94 ±0.40
July
2.63 ±0.30
1.91 ±0.20
3.55 ±0.40
3.55 ±0.55
1.97 ±0.65
1.68 ±0.30
2.11 ±0.30
0.76 ±0.40
1.70 ±0.25
August
4.42 ±0.75
3.34 ± 0.60
6.44 ±0.55
4.50 ± 0.60
7.72 ±0.40
6.55 + 0.40
3.37 + 0.45
1.60 ±0.25
1.93 ±0.40
September
—
7.46± 1.15
6.33 ±0.50
—
—
—
—
4.44 ±1.00
7,47 ±0.50
October
—
—
—
—
—
—
—
—
4.24 ±0.02
November
—
—
—
—
—
—
—
—
0
Fish Harbour
May
0
0
—
0
—
—
—
—
—
June
—
0
0
0.70 ±0.01
—
—
—
0
0
July
0.93 ± 1.70
0.18 ±0.05
3.44 ±0.45
0.21 ±0.04
0.46 ±0.03
0.26 ±0.04
0.92 + 0.08
0.36 ±0.15
0.22 ±0.01
August
4.00 ±0.78
1.04 ±0.40
6.45 ±0.40
4.48 ±0.62
2.08 ±0.70
1.94 ±0.50
2.05 ±0.30
1.17±0.30
0.66 ±0.08
September
—
2.41 ±0.35
—
8.00 ±1.80
5.22 ±0.60
—
—
3.08±1.12
0.89 ±0.05
October
—
—
—
—
—
—
—
—
0
November
—
—
—
—
—
—
—
—
0
'No animals
recorded.
'No search effort.
^Standard error
of the mean.
ber and May, but probably rarely enter Fish Harbour
(see next section).
Arrival and Departure of Porpoises
Each Year in Relation to
Sea Temperatures
First sightings in Fish Harbour were usually made
in mid-late July when surface temperatures attained
about 9°C, and never in Lords Cove until about mid-
August despite 9°-ll°C being reached at the surface
in mid-late July. First regular sightings in Simpson's
Passage varied from mid-May to late June. Deter-
mining the date of departure of the majority of
animals from either sector was difficult because
strong autumnal winds invariably interfered with
observations from mid-September onwards when
relative abundance was still high. In both 1977 and
1978, porpoises were still present in Fish Harbour
until the last week of September and in Simpson's
Passage until at least 15 October. Occasional animals
may venture into the latter area in any month of the
year since a very small population usually over-
winters in the Quoddy region (Gaskin 1977), and one
animal was sighted outside Fish Island on 7 Decem-
ber 1982 (B. M. Braune^ and D. E. Gaskin, pers.
obs.).
We could find no evidence that the distribution of
porpoises was directly or indirectly influenced by the
rather small daily local variations in sea tempera-
tures within Fish Harbour. The most frequently
^B. M. Braune, Department of Zoology, University of Guelph,
Guelph, Ontario NIG 2W1, Canada.
observed known animal and her consorts would
regularly traverse the width of the area (see Figure.
9) and their preferred locations appeared to have
specific topographic rather than temperature charac-
teristics.
Estimating Relative Abundance
Because the species does not make long dives
(mean submergence 1 min 44 s, Watson and Gaskin
(1983)), the required minimum period of observation
needed to search the study area was not excessive.
From our records we selected 3 wk in August
1972-75, when the probability of animals being pres-
ent was high. In a random sample of 40 (i.e., above
the minimum size for a "large" statistical sample
(Bailey 1959)) search periods in optimum conditions
of varying length (5 min to 2 h), the percentage of
time that one or more animals was recorded in-
creased from 50% for 10-min periods to well over
80% for 15-min periods. All observations of < 15 min
were therefore discarded from the data set. If we
were only interested in presence or absence, as in the
case of simple locations at a given time of day or tide,
observations from shorter periods or in Beaufort
wind force 2 + were still of some value.
We have already outlined the methods for obtain-
ing our "best estimates"; it is worth noting that
various characteristics of the animals (e.g., short dive
times, stereotyped movements, recognizable individ-
uals) and of the study area (limited search area
because of shallow water, many landmarks, shelter,
and limited entry and exit points for animals) were of
great assistance in reducing repeat sightings to a
minimum.
431
FISHERY BULLETIN: VOL. 83, NO. 3
Changes in Relative Abundance
Between 1970 and 1978
Table 1 gives sightings of individuals per hour by
month for each year from 1970 to 1978. As some
observation periods were eliminated (see above) the
results sometimes differ slightly from values given
by Gaskin (1977) for the earlier years. Results sug-
gest a decline in relative abundance from 1972 on-
wards in Fish Harbour and from 1974 onwards in
Simpson's Passage. Because the 1970 values were
based on a relatively short series of observations, the
apparent rise from 1970 to 1971 may be spurious.
The slight increase in 1978 is also suspect as most
observers were less experienced than the teams used
in 1970-77. The overall trend however, seems unmis-
takable. Furthermore, a decline in each month of the
July-September period is evident when data for the
whole study area are pooled (Fig. 2).
Results of the categorical data procedure tests for
relative abundance of porpoises against the set of en-
vironmental parameters are presented in Table 2
(Fish Harbour) and 3 (Simpson's Passage). As might
be expected, large x^ and significant P values were
generated from the sharp drop in overall numbers
sighted per observation period (regardless of its
length) from 1972 to 1975, and from the great in-
crease occurring each year between July and
September. Time of day appeared to exert no in-
fluence on relative abundance in either section (P =
0.45, 0.20), nor was any statistically significant rela-
tionship noted between relative abundance and
0)
c
i
1 1 \
1 1 >
1 >
1 !
s ■
1
1
1
t
1
1
\
i
\
\
1
1
1
1 ;
-'-'rC^'^. Sept
i. *\ ^ v^
1
^ \
, »
Aug. \
i !
.■n
July
Oct.
Figure 2. -Comparison of sightings per hour of
porpoises in good condition in the Fish Harbour
study area (Fish Harbour + Simpson's Passage),
1970-78 by month, from July to September. Octo-
ber and November values available for 1978 only.
Vertical dots and bars represent standard error
about the means.
- Nov. 2
-. »
1970 1971 1972 1973 1974 1975 1976 1977 1978
Year
432
GASKIN and WATSON: HARBOR I'ORF'OISE
Table 2.— Results of categorical data procedure tests for
observed numbers of fiarbor porpoises In comparison to ex-
pected numbers withi different environmental parameters In
thie FIsfi Harbour region of souttiern New Brunswick,
1972-75. 1. FIsfi Harbour -(- Lords Cove (see Figure 1). n =
observation periods; x^ = two-way table statistic.
Parameter
measured
n
df
Years (1972-75)
Time of year'
(July to early September)
Time of day^
(0600- -I- 1900)
Tidal amplitude'
Tidal pfiases"
(Start of falling tide to
end of rising tide)
Lunar phiase*
(New moon to full moon)
Wind extant^
(On sfiore, coastwise, or
offshore)
Wind 24 ti previous^
249
249
249
249
249
3
2
4
3
39.57 0.0001*
63.69 0.0001 •
3.67 0.4520
7.80 0.0500*
3.31 0.8450
249 3 5.38 0.1450
249 2 17.58 0.003
249 2 12.22 0.0094
'Categorical division of ttiree periods (July, first 3 wk of
August, last 1 V2 wk of August -1- early September) to balance
effort.
^Four periods of 3 h eacti, post-1900 observations amal-
gamated.
^Four subpfiases (> 5.5, 5.6-6.5. 6.6-7.5, ^ 7.6 m).
'Thie eigfit subptiases given In Figure 4 were used.
^Three subdivisions used. More subdivision tfian thiese
resulted in many empty data cells.
^Four subdivisions used. More subdivision tfian tfiese
resulted In many empty data cells.
*Statistically significant at 0.05 level or better.
Table 3.— Results of categorical data procedure tests for
observed numbers of harbor porpoises in comparison to ex-
pected numbers with different environmental parameters In
the Fish Harbour region of southern New Brunswick,
1972-75. 11. Simpson's Passage, n ~ observation periods;
X^ - two-way table statistic.
Parameter
measured
n
df
Years (1972-75)
Time of year'
(July to early September)
Time of day^
(1600- -I- 1900)
Tidal amplitude'
Tidal phases"
(Start of falling tide to
end of rising tide)
Lunar phase*
(New moon to full moon)
Wind extant^
(Onshore, coastwise or
offshore)
Wind 24 h previous^
132
132
132
132
132
3
2
4
3
7.58 0.050*
16.99 0.0002*
5.98 0.201
2.54 0.468
9.97 0.190
132 3 7.38 0.061*
132 2 0.95 0.620
132 2 0.93 0.628
'Categorical division of three periods (July, first 3 wk of
August, last 1 V2 wk of August -1- early September) to balance
effort.
^Four periods of 3 h each, post-1900 observations amal-
gamated.
'Four subphase (> 5.5, 5.6-6.5, 6.6-7.5, > 7.6 m).
"The eight subphases given in Figure 4 were used.
^Three subdivisions used. More subdivision than these
resulted in many empty data cells.
*Four subdivision used. More subdivision that these
resulted In many empty data cells.
'Statistically significant.
**Close to significance at 0.05 level.
magnitude of tidal amplitude in Simpson's Passage.
In shallower, semi-enclosed Fish Harbour however,
significantly more porpoises were present (P = 0.05)
at low tidal amplitudes (< 6.5 m) than high
amplitudes (^ 6.6 m). Data for the most commonly
sighted individual (a female with a large dorsal scar)
corroborated this general finding; about 78% of all
sightings of this animals were made when the ampli-
tude was 6.5 m or less.
Relative abundance did not alter (P = 0.84, 0.19)
in either zone of the study area during the tidal cycle.
Similarly no significant change occurred relative to
the lunar phase in Fish Harbour, although in Simp-
son's Passage the x^ value approached the arbitrary
0.05 level of significance (P = 0.061; n = 249). No
relationship between extant or previous wind direc-
tion was evident in Simpson's Passage {P = 0.62,
0.63; n = 132), but there appeared to be a significant
association between wind direction and relative
abundance of porpoises in Fish Harbour (P =
0.0003, 0.009; n = 249). In both cases far more
animals were present during onshore wind directions
than when winds were coastwise or offshore.
Distribution and movements of porpoises on the
fine scale is likely to be correlated with the presence
or absence of food species which, in the Quoddy
region, consist largely of juvenile herring, Clupea
harengiis; mackerel; and small gadoids (Smith and
Gaskin 1974). The dispersal of the former in this
region is greatly influenced by current velocities
(Jovellanos and Gaskin 1983). Unfortunately the
beam width of available equipment was far too nar-
row to permit us to cover the study area by acoustic
survey thoroughly, or even representatively, at any
given time or tide phase. Because one of our major
aims at the outset of the study was to avoid disturb-
ing normal behavior of the porpoises, it was also
rarely possible to acoustically scan in their immedi-
ate vicinity. We were however able to infer feeding
behavior from diving patterns (e.g., "pattern B") car-
ried out consistently in one location (Watson and
Gaskin 1983). Sometimes fish were seen jumping at
the surface in such areas (Fig. 3), and these zones
were acoustically scanned on an opportunistic basis.
Fish schools, recorded during bottom topographic
acoustic mapping runs, tended to be concentrated at
several locations in which porpoises were often
sighted. Usually these traces were of herring school-
type. While this species predominates in the Quoddy
region in the summer months (Jovellanos and Gaskin
433
FISHERY BULLETIN: VOL. 83, NO. 3
Figure 3. - Locations in Fish Harbour at which fish were detected visually or by sonar in 1973-78; opportunistic records only. Stipple: species
not identified; vertical bars: Atlantic mackerel: diagonal bars: Atlantic herring; circles: one or more porpoises simultaneously present with
record; arrows: direction of fish movement. The size of hatched areas indicates approximate size of the school.
1983), some could have been of harbor pollack, which
are also taken by this species.
Changes in Distribution Within
the Fish Harbour Region
No differences in distribution of the 669 recorded
sighting positions for 1973-75 could be detected
when they were plotted either by four or eight time
periods from 0600-2200, but considerable differences
were evident when they were plotted against eight
subphases (slack low, slow flood #1, fast flood, slow
flood #2, slack high, slow ebb #1, fast ebb, and slow
ebb #2) of the tidal cycle. This analysis ignores for
the moment the fact that many animals move in a
rather regular manner through the study area, since
useful information can be obtained simply from
noting where they are at any given time of tide. The
results (Fig. 4) showed that up to 80% of porpoises
were congregated over the shallow shelf margins,
slopes, and scarp areas between the onset of flood
tide and high water. Conversely, about the same pro-
portion became concentrated over the basin and
channel areas between onset of the ebb, and slack
low water.
The Nature of Movements Within
the Fish Harbour Region
It became evident that when the recognizable
animals returned each year they reestablished
"specific ranges" (for lack of a better term) in virtu-
ally the same locations in Fish Harbour each summer
(Figs. 5-8). There is some evidence that these
"ranges" shifted progressively further east of Deer
Island between 1973 and 1975, especially in the case
of the scarred female mentioned earlier. Each of
these areas in Fish Harbour, of which we were able
to measure nine approximately, appeared to be about
1.0-1.5 km^ in extent. Even the most distinctive
animals would disappear from the study area for ex-
tended periods and then reappear again, just as
Gaskin et al. (1975) noted for a female carrying a
radiotelemetric package. The scarred female was
once observed with a calf off the eastern coast of
Simpson's Island, and on another occasion between
Minke Ledges and Tinker Island, which lie between
1 and 3 km south of the main study area. This speci-
men was present in the Fish Harbour region for
about half the days of excellent visibility in 1973-75,
was well known to all observers, and yet was only
434
GASKIN and WATSON: HARH( )K fOKPOISE
100
Figure 4. -Distributions of 669 harbor
porpoises in Fish Harbour 1973-75 over
subsurface topographic features, by eight
subphases of the tide: Slack low water (SL),
slow flood 1 (SFi), fast flood (FF), slow
flood 2 (SF2), slack high water (SH), slow
ebb 1 (SEj), fast ebb (FE), and slow ebb 2
(SE2). Solid line shows percentage over
shallow shelf, scarps, and slopes; dotted
line, percentage over basins and channels.
20
10-
SFi FFi SF2 SH SEi FE SE2
Subphases of tide
SL
seen on the two above occasions during simultaneous
surveys outside the present study area.
Only in the case of this particularly distinctive
animal were we able to obtain enough observations
to map some of her patterns of movement over ex-
tended periods. On 17 August 1973, for example, we
tracked her for 2 h 12 min (57 position fixes. Fig. 9),
noting that she tended to stay close to the slopes of
the main basin-channel, with one foray around the
small basin in Lords Cove. This kind of point-to-point
travelling interspersed with short periods of
submergences in one location is quite typical of this
species. This animal repeated almost identical range
movements on 13 and 29 August 1974. On 1 and 30
August 1974 (1 h 4 min and 3 h 3 min respectively)
this animal spent far longer periods in relatively
restricted locations (Fig. 10). Submergences were
again of the "pattern B" type, and no surface resting
was recorded. On 1 August many herring were seen
jumping at the surface immediately after each
submergence by the female. Her calf was often left
at the surface during these bouts.
"Systematic patrolling" of small areas, often in the
lee of ledges or small islets was also recorded (Fig.
10). The movements illustrated were carried out by a
school of three medium-sized animals accompanied
by one small one on 2 August 1974. The group
sychronously dove repeatedly while moving back and
forth in one restricted scarp location, then abruptly
travelled to the second location shown and repeated
the pattern.
DISCUSSION
The distribution of some small odontocetes is
known to be correlated with sea surface tempera-
tures (Gaskin 1968; Wiirsig and Wiirsig 1980), but
the relationship is almost certainly indirect, the
result of influences exerted one or more levels fur-
ther down the food chain. The entry of the main sum-
mer population of harbor porpoises into the study
area not only coincides with 9°-10°C surface
temperatures, but also with the arrival of large
numbers of juvenile herring which feed in the Quod-
dy region during the summer months (Battle et al.
1936; Jovellanos and Gaskin 1983). Although trans-
port of relatively small fish into the study area might
be expected to be at a maximum during spring tides,
435
FISHERY BULLETIN: VOL. 83. NO. 3
Figure 5. -Broken lines encompass all sightings of recognizable animal (#1, scarred mother). 1973; solid wedges; 1974: open wedges; 1975:
dots. The solid triangle, open triangle, and solid circle respectively represent the center of the "range" as determined by the mean of the
latitudes and longitudes of each position, excluding single isolated sightings. Arrows indicate number of times this animal (and any consorts)
were observed leaving the "range". In each case they were swimming at 4 + knots and outdistancing the kayak.
Figure 6. - Broken lines encompass all sightings of known animal #2 (clipped fin). 1 974: dotted lines; 1974: dashes. Open circle and closed cir-
cle for 1974 and 1975 respectively, and arrows indicating animal leaving the area are as in Figure 5.
436
GASKIN anil WATSON: HAKHOK PdKI'OISK
Figure 7. - Broken lines encompass all sightings of known animal #3 (Simpson's Passage mother) except for single 1977 sighting. 1973: dot-
ted line; 1974: dashed line. Other symbols as in Figure 5.
1974.
ir
\ 'z:^-'";--'..
74
• . • ' • .
• 75
I
8
Figure 8. - Broken lines encompass all sightings of known animal if 4 (Light brown mother). 1974: solid wedges; 1974: open wedges. Other
symbols as in Figure 5.
437
FISHERY BULLETIN: VOL. 83 NO. 3
Figure 9. - Movements of scarred mother during 2 h 12 min period of 10 August 1973 accompanied by calf (57 position fixes). On some occa-
sions they resurfaced close to an immediately previous position; about 75 surfacings are represented by these positions. Reverse arrow in-
dicates initial contact point (just outside Lords Cove), solid arrow point where tracking was abandoned, and white circles position of a medium-
sized animal which briefly joined the pair.
we found relative abundance of porpoises conversely
to be greatest during neap tides. About 63% of the
sightings in 1973-75 were of mothers and calves.
Possibly these animals stay out of semi-enclosed
areas during periods of maximum water transport,
especially in areas with turbulent shallows such as
the Fish Harbour region. On the other hand, if there
are larger numbers of herring schools moving into
the outer part of the Quoddy region it may not be
necessary to forage in inshore waters. Once the
animals are in the study area however, the observed
changes in distribution during the tidal cycle confirm
the earlier subjective comment (Watson 1976) that
porpoises seemed to move inshore with the flood tide
and offshore with the ebb.
The distribution of porpoise activity in the region
appeared to be closely related to subsurface
topography, particularly the margins of the basins
and channels in areas of restricted water flow, the
lee of islets, especially Fish Island and the Nub, and
blind trench heads such as that just north of Hath-
away Head. Because our meager acoustic records
revealed fish traces in all these sites at one time or
another (Fig. 3), we speculate that these may be
areas of fish accumulation which the porpoises have
learned to exploit. Each may have subsurface eddies
or areas of relatively slack water against the lee side
of the slope or near the bottom, in which fish can
shelter from strong currents, and in which zooplank-
ton might also accumulate. In such areas fish could
not only avoid being carried further inshore, but
could also feed (Hamner and Hauri 1977). Dispersal
from offshore areas into the coastal belt is likely to be
augmented by onshore winds, which can increase
significantly the flow of water in the immediate sur-
face layers. Local fishermen believe that offshore
winds serve to hold "feed" away from the coast, while
coastwise winds might reduce the possibility of entry
into Fish Harbour by increasing surface flow past
the relatively narrow passages. We conclude that
light or moderate winds are unlikely to affect any
small cetacean directly; when winds were strong
enough that behavior might conceivably be affected,
we were not usually operating.
Large variation always occurs in data such as
these, and it is to a large extent unpredictable. Such
variation in relative abundance can be explained
quite simply; these animals are large, highly mobile
predators with sophisticated adaptations both for ac-
tive and passive acoustic scanning for their equally
438
GASKIN and WATSON: HARBOR PORI'OISE
FiGl'RE 10. -Movements of scarred female on 30 August 1974 (solid circles at left of figure) and 29 August 1974 (solid circles in center of
tlgure). Solid squares show "patrolling" behavior of school of four animals recorded on 2 August 1974. Qualifying comments on position fixes
and surfacings in Figure 9 apply here also.
mobile prey. That the harbor porpoises in this area
can shift tens of kilometers in a few hours cannot be
questioned (Read and Gaskin in press); if few fish are
present in one area, they may well move in a loosely
synchronized group to forage in other localities. This
degree of mobility and scanning ability is highly
adapted not only to the mobility of their prey species,
but also to the patchy nature of the distribution pat-
terns of such fish; there is probably a significant ran-
dom element in the dispersal of juvenile herring in
the Quoddy region (Jovellanos and Gaskin 1983). The
type of porpoise movement shown in Figure 9 was
presumed to indicate that prey were dispersed, since
the animal spent little time in any one location. In the
other movement pattern (Fig. 10) the same animal
was believed to be encountering prey in local concen-
trations that merited prolonged submergences in one
area.
We have little evidence that the region might be
significant either as a mating area or a calving
ground. Females appear to have their calves off-
shore, since, although the latter may be very small in
late June and July, they already accompany females
sighted in the outer part of the Quoddy region (Smith
and Gaskin 1983). Many females with calves appear
to remain on tidal convergence streaks up to 20 km
offshore in the outer Quoddy region (Read 1983) and
may not move into the coastal zone at all. It seems
more likely that the study area functioned as a signi-
ficant feeding area for this species rather than being
a zone favoured for reproductive activity.
The demonstrated existence of "specific ranges"
and annual returns by individual harbor porpoises in
this study is not surprising. Rather similar patterns,
although sometimes on very different geographical
scales, have been recorded for Delphinus delphis by
Martin et al. (1971), Orcinus orca by Bigg (1982),
Tursiops trun^.atus by Wells et al. (1980) and Wiirsig
and Wiirsig (1979), and Lagenorhynchus obscurtis by
Wiirsig and Wiirsig (1980). Periodic disappearances
and abrupt reappearances of T. truncatics were also
recorded by Wiirsig (1978), while studying the
animal.
With respect to the progressive decline in relative
abundance in the peak part of summer, lack of con-
sistent observations through late September-late
October (because of high winds) prevented us from
determining whether or not this resulted from a real
population decrease in the area, or simply a shift of
peak abundance from mid-August to mid-September
during the decade. Consequently we adopted an in-
direct approach to the problem, plotting sightings
439
FISHERY BULLETIN: VOL. 83. NO. 3
per hour for each month of summer for each year
with sufficient data (Fig. 2). This suggests that the
decline resulted from a combination of both factors,
with a general overall decline in relative abundance
since about 1973 and a progressive retardation of the
peak of numbers since about 1975. Unfortunately
there is insufficient information in Department of
Fisheries and Oceans records to decide if any change
in food supply could have occurred during those
years, especially with respect to juvenile herring
abundance (T. D. Iles^). Nevertheless, our surface
temperature records for the inner Quoddy region
reveal a consistent decline in the mean summer value
(centered on mid-August) from above 12°C in 1971
to below 11°C in 1977 (Gaskin et al. 1979). The
temperature curve is compared with the pattern of
relative abundance in Figure 11; there is close cor-
respondence from 1972 onwards. Such a decline
might result from increase in relative dominance of
''T. D. lies, Biological Station, Department of Fisheries and
Oceans, New Brunswick, EOG 2X0, Canada, August 1980.
Nova Scotia current water in the Bay of Fundy
(Sutcliffe et al. 1976) and perhaps a significant
decline in the availability of zooplankton prey of
juvenile herring. Alternatively the slightly cooler
waters might be marginally less suitable for young
porpoise calves.
ACKNOWLEDGMENTS
The authors are very grateful to J. Hines and G.
Darlington of the Department of Mathematics and
Statistics at the University of Guelph for much
assistance and advice during the analysis of the en-
vironmental data. G. J. D. Smith and A. J. Read of
the Department of Zoology read the manuscript in
its several drafts, and along with two anonymous
referees gave much useful and constructive advice
regarding improvements. Many former and current
assistants and graduate students, too numerous to
name, helped to collect the laboriously obtained field
data. Marine Research Associates of Lords Cove and
the late R. Thurber of St. Andrews, N.B., provided
7-
6-
C
4-
CO
Figure 1 1 .- Comparison of midsummer (late
•July-early September) sightings per hour of har-
bor porpoises in the Fish Harbor region of New
Brunswick between 1970 and 1978 with surface
temperatures based on 8 stations (n = about
60/annum): Solid circles and dashed line (sight-
ings per hour), open circles and dotted line (°C).
Vertical dots and bars represent the standard
error about the mean.
12.0
.9
.8
.7
.6
.5
.4
.3
.2
.1
1 1.0-
.9
.8'
I. \
I . \
\ ?.
< .
■ I
9
2.
4.
: \
■■•, y
■»
6
T. \
i'-
11
— I 1 1 1 — I 1 —
1970 1971 1972 1973 1974 1975
— I I
1976 1977
1978
Year
440
GASKIN and WATSON: HARBOR PORF'OISE
valuable logistic support. The program was funded
through Natural Sciences and Engineering Research
Council of Canada operating grant A8563 through-
out, and in later stages by a subvention from
Fisheries and Oceans Canada and a grant from the
Canadian National Sportsmen's Fund.
LITERATURE CITED
Amundin, M., and B. Amundin.
1974. On the behavior and study of the harbour porpoise,
Phocoena phocoena, in the wild. In G. Pilieri (editor). Inves-
tigations on Cetacea, Vol. V, p. 317-328. Berne, Switzer-
land.
Bailey, N. J. T.
1959. Statistical methods in biology. Engl. Univ. Press, Ltd.,
Lond., 200 p.
Battle, H. I., A. G. Huntsman, A. M. Jeffers, G. W. Jeffers,
W. H. Johnson, and M. A. McNairn.
1936. Fatness, digestion and food of Passamaquoddy young
herring. J. Fish. Res. Board Can. 2:401-429.
Bigg, M.
1982. An assessment of killer whale (Orcinus orca) stocks off
Vancouver Island, British Columbia. Thirty-second Rep. Int.
Whaling Comm. SC/Jn81/KW4, p. 655-666.
Forrester, W. D.
1960. Current meaisurements in Passamaquoddy Bay and the
Bay of Fundy 1957 and 1958. J. Fish. Res. Board Can. 17:
727-729.
Gaskin, D. E.
1968. Distribution of Delphinidae (Cetacea) in relation to sea
surface temperatures off eastern and southern New Zealand.
N.Z. J. Mar. Freshw. Res. 2:527-534.
1977. Harbour porpoise Phocoena phocoena (L.) in the western
approaches to the Bay of Fundy 1969-75. Rep. Int. Whaling
Comm. 27:487-492.
Gaskin, D. E., G. J. D. Smith, and A. P. Watson.
1975. Preliminary study of movements of harbour porpoises
{Phocoena phocoena) in the Bay of Fundy using radiotele-
rnetn,-. Can. J. Zool. 53:1466-1471.
Gaskin, D. E., K. I. Stonefield, P. Suda, and R. Frank.
1979. Changes in mercury levels in harbour porpoises from
the Bay of Fundy, Canada, and adjacent waters during
1969-1977. Arch. Environ. Contam. Toxicol. 8:733-762.
Hamner, W. M., and I. R. Hauri.
1977. Fine-scale surface currents in the Whitsunday Islands,
Queensland, Australia: Effect of tide and topography. Aust.
J. Mar. Freshw. Res. 28:333-359.
Jovellanos, C. L., and D. E. Gaskin.
1983. Predicting the movements of juvenile Atlantic herring
(Clupea karengus harengus) in the SW Bay of Fundy using
computer simulation techniques. Can. J. Fish. Aquat. Sci.
40:139-146.
Kasuya, T., and L. Jones.
1984. Behavior and segragation of the Dall's porpoise in the
Northwestern Pacific Ocean. Sci. Rep. Whales Res. Inst.
No. 35, p. 107-128.
Kraus, S. D., J. R. Gilbert, and J. H. Prescott.
1983. A comparison of aerial, shipboard, and land-based
survey methodology for the harbor porpoise, Phocoena
phocoena. Fish. Bull., U.S. 81:910-913.
Matkin, C. 0., and F. H. Fay.
1980. Marine mammal-Fishery interactions on the Copper
River and in Prince William Sound, Alaska, 1978. U.S. Dep.
Commer., N.T.I.S. Rep. PB80-159536, Springfield, VA, 81 p.
Maxwell, A. E.
1977. Multivariate analysis in behavioural research. Chap-
man and Hall, Lond., 164 p.
M6HL-HANSEN, U.
1954. Investigation of reproduction and growth of the por-
poise {Phocoena phocoena (L.)) from the Baltic. Vidensk
Medd. Dan. Naturhist. Foren. Khobenh. 116:369-396.
Read, A. J.
1983. Movements and distribution patterns of harbour por-
poises {Phocoena phocoena) in the western Bay of Fundy.
M.S. Thesis, University of Guelph, Guelph, Ontario, 87 p.
Read, A. J., and D. E. Gaskin.
1983. The application of radio tracking techniques to the study
of harbour porpoises {Phocoena phocoena) in the Bay of
Fundy. Proceedings of the 5th International Conference on
Wildlife Telemetry, Halifax, N.S., Canada, August 1983, 7 p.
1985. Radio tracking the movements and activities of harbour
porpoise, Phocoena phocoena (L.), in the Bay of Fundy, Can-
ada. Fish. Bull. U.S. 83(2).
S.A.S. Institute, Inc.
1979. SAS User's Guide. Edited by J. T. Helwig and K. A.
Council. SAS Institute Inc., Raleigh, NC, 494 p.
Scheffer, V. B., AND J. W. Slipp.
1948. The whales and dolphins of Washington State wdth a
key to the cetaceans of the west coast of North America.
Am. Midi. Nat. 39:257-337.
Smith, G. J. D., and D. E. Gaskin.
1974. The diet of harbour porpoises {Phocoena phocoena (L.))
in coastal waters of eastern Canada, with special reference to
the Bay of Fundy. Can. J. Zool. 52:777-782.
1983. An environmental index for habitat utilization by female
harbour porpoises with calves near Deer Island, Bay of
Fundy. Ophelia 22:1-13.
Smith, G. J. D., C. L. Jovellanos, and D. E. Gaskin.
1984. Near-surface biooceanographic phenomena in the Quod-
dy region, Bay of Fundy. Can. Tech. Rep. Fish. Aquat. Sci.
1280, 124 p.
SuTCLiFFE, W. H., Jr., R. H. Loucks, and K. F. Drinkwater.
1976. Coastal circulation and physical oceanography of the
Scotian Shelf and Gulf of Maine. J. Fish. Res. Board Can.
33:98-115.
Taylor, B. L., and P. K. Dawson.
1984. Seasonal changes in densit>' and behavior of harbour
porpoise {Phocoena phocoena) affecting census methodology
in Glacier Bay National Park, Alaska. Thirty-fourth Rep.,
Int. Whaling Comm., p. 479-483.
Trites, R. W.
1962. Temperature and salinity in the Quoddy region of the
Bay of Fundy. J. Fish. Res. Board Can. 19:975-978.
Watson, A. P.
1976. The diurnal behavior of the harbour porpoise {Phocoena
phocoena) in the coastal waters of the western Bay of Fundy.
M.S. Thesis, LTniversity of Guelph, Guelph, Ontario, 94 p.
Watson, A. P., and D. E. Gaskin.
1983. Observations on the ventilation cycle of the harbour por-
poise Phocoena phocoena (L.) in coastal waters of the Bay of
Fundy. Can. J. Zool. 61:126-132.
Watts, P. W., and D. E. Gaskin.
In press. Habitat index analysis of harbour porpoise {Phocoena
phocoena L.) in the southern coastal Bay of Fundy, Canada
J. Mammal. 64.
Wells, R. S., A. B. Irvine, and M. D. Scott.
1980. The social ecology of inshore odontocetes. In L. M.
Herman (editor). Cetacean behavior: mechanisms and func-
441
FISHERY HULLETIN: VOI,. H3, NO. 3
tions, p. 263-317. Wiley-Interscience Publications, N.Y. stops truncatm, in the South Atlantic. F'ish. Hull., U.S. 77:
WUKSIG, B. 399-412.
1978. Occurrence and group organization of Atlantic bottle- 1980. Behavior and ecology of the dusky dolphin, La(;(?nor%rir
nose porpoises {nirsiops trurwatus) in an Argentine hay. chus obsmrus, in the South Atlantic. Fish. Bull., U.S. 77:
Biol. Bull. (Woods Hole) l.'')4:348-359. 871-890.
WURSIG, B., AND M. WURSIC.
1979. Behavior and ecology of the bottlenose dolphin, Tur-
442
NOTES
THE RELATIONSHIP BETWEEN TILEFISH,
LOPHOLATILUS CHAMAELEONTICEPS,
ABUNDANCE AND SEDIMENT COMPOSITION
OFF GEORGIA
Elucidation of the relationship between physico-
chemical factors and fish abundance has long been of
interest to fisheries biologists. For example, water
temperature frequently exerts a strong influence on
the abundance of many pelagic marine fishes (Rado-
vich 1961; Laurs et al. 1977; Barkley et al. 1978;
Moyle and Cech 1982), and this effect has been noted
also for freshwater species (Magnuson et al. 1979;
Moyle and Cech 1982). For benthic marine fishes,
however, substrate composition may be a more im-
portant factor affecting fish abundance and distribu-
tion. Associations between abundance and substrate
composition have been noted for a diverse group of
fishes: agonids, bothids, cottids, pleuronectids, scor-
paenids, and steichaeids (Day and Pearcy 1968;
Powell and Schwartz 1977; Marliave 1977; Barton
1982). Where detectable, however, these associa-
tions vary substantially in intensity. This is probably
due to the fact that many physicochemical factors
are intercorrelated and most fishes probably respond
to intercorrelated suites of variables rather than to
single factors alone.
In this note we quantify the relationship between
catch rate of a demersal species, the tilefish, Lopho-
latilus chamaeleonticeps, and substrate composition.
This species is commercially exploited throughout
most of its range (Grimes et al. 1980; Low et al.
1983; Turner et al. 1983), although, prior to this
study, tilefish resident to the continental slope off
Georgia appeared to have been subjected to minimal
exploitation (D. Harrington'). The elucidation of a
substrate-abundance relationship for tilefish should
aid in the management and harvest of this species.
Methods
A total of 19 bottom longline sets and 19 sediment
samples were obtained during daylight hours, be-
tween 5 May and 22 November 1982. Fourteen long-
line sets, each comprising 1.6 km of line, and 12 sedi-
ment samples (Table 1) were obtained from the RV
Georgia Bulldog (University of Georgia Sea Grant
Program vessel). Five sets(X ± 1 SD length = 0.31
± 0.09 km) and seven sediment samples were col-
lected aboard the RV Delaware II (National Marine
Fisheries Service vessel). At least one of the authors
was present during collections.
Bottom longlining on the Georgia Bulldog was con-
ducted using snap-on gangions (~ 0.5 m in length)
spaced about 4 m apart, along a 6.3 mm diameter
galvanized aircraft cable groundline. Gangions were
equipped with 4/0 or 5/0 circle hooks and baited with
either fish or squid. A similar system was employed
on the Delaware II except that a much shorter
groundline of 6.3 mm diameter hardlaid nylon was
used (Table 1), with hook sizes ranging from 3/0 to
8/0.
Substrate Analysis
Substrate samples were collected with a 25 x 30
X 37.5 cm box dredge suspended from a power
winch. The dredge was lowered to the bottom and
then dragged across the substrate (typically for < 5
min). After retrieval, 1.2-2.0 kg of sediment were
removed from the dredge and stored in plastic bags.
It is assumed that these samples accurately reflect
the composition of surface sediments.
Sediment samples varied in their proximity to
longline sets. Fourteen samples were taken at the
end of longline sets. Of the remaining five samples,
one was taken from the midpoint of a set, three were
taken alongside sets within a distance of 0.2 km, and
one was taken alongside a set at a distance of 0.6 km.
The general area sampled (see Table 1 for loran C
coordinates) has a relatively homogenous, low-relief
bottom topography, and large variations in substrate
composition probably do not occur over short
distances (V. J. Henry^).
To determine the fraction of each sample compos-
ed of sand and silt-clay, a known amount of sediment
(i.e., enough to yield a dry weight of between 60 and
100 g) was dried in a forced-air oven at 98°C until a
constant weight was reached. The sample was then
moistened with water which contained ~ 2 g of
Calgon^ as a dispersant, and washed through a sieve
which retained particles > 0.0625 mm (4^) (U.S.
standard seive #230). Sediments retained by the
sieve were then oven-dried to a constant weight to
'D. Harrington, University of Georgia Marine Extension Service,
Brunswick, GA 31523, pers. commun. 1983.
^V. J. Henry, Dept. of Geology, Georgia State University, Atlan-
ta, GA 30303, pers. commun. 1983.
^Reference to trade names does not imply endorsement by the Na-
tional Marine Fisheries Service, NOAA.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
443
Table 1.— Sediment composition and catch data for longline sets used to establish the relationship be-
tween catch rates and sediment composition off Georgia.
Minimum and
Percent
maximum
Groundline
Number
Soak
Tilefish
Percent
silt-
Loran C
depths (m) of
length
of
time
per 100
sand
clay
Date
coordinates
longline sets
(km)
hooks
(h)
hook-h-1
(»4|)
(<A^)
5-5-82
45086.1
60777.3
5-29-82
45092.9
60743.2
5-29-82
45093.8
60729.9
5-30-82
45088.0
60869.4
5-30-82
45080.8
60864.2
5-30-82
45076.8
60854.7
5-30-82
45073.0
60847.0
5-30-82
45069.6
60841.0
6-29-82^
44736.5
61531.7
7-1-82^
45039.6
60974.6
7-2-82^
45065.4
60868.6
7-12-82^
26979.6
39551.5
{9960-chain)
7-24-82
45109.8
60548.5
7-25-82
45101.0
60549.0
8-13-82
45076.0
60842.6
8-14-82
45085.6
60735.0
8-17-82
45093.8
60555.9
11-22-82
45097.8
60720.5
11-22-82
45095.8
60716.0
187-190
1.61
242
3.3
2.11
'58
42
193-194
1.61
390
4.3
1.72
53
47
^196
1.61
348
5.3
3.29
'49
51
140-143
1.61
284
3.5
0
85
15
164
1.61
330
4.2
0
69
31
182-185
1.61
247
4.0
0.41
64
36
203
1.61
254
3.6
0
64
36
219
1.61
298
2.9
0.57
79
21
No data
0.18
50
2.5
0
88
12
199
0.35
100
2.0
0
69
31
No data
0.35
100
1.0
0
80
20
216-223
0.35
103
1.0
0
98
2
186-187
1.61
258
3.2
3.56
'40
60
217-219
1.61
241
4.0
3.80
48
52
195-201
1.61
266
3.0
0.50
74
26
230
1.61
352
3.7
2.98
57
43
255-258
1.61
245
3.9
1.67
55
45
186
1.61
311
3.5
3.95
'48
52
189-191
1.61
250
2.9
5.34
52
48
'Substrate samples were taken during a different cruise, however, samples were always taken within
65 d of each other.
^A single depth measurement means that only one reading was taken during the longline set. This
depth is an approximation of longline depth.
^Samples taken from the Delaware II.
determine the percentage of sand and larger par-
ticles in the sample. The silt-clay fraction was obtain-
ed by subtraction. Replicate subsamples were taken
from six collections to establish the technique's preci-
sion. The mean difference in percent silt-clay frac-
tion among the six replicates was 2.5% (s = 1.4%). A
t-test for paired samples indicated that significant
differences did not exist among replicate determin-
ations for a given sample {t = 0.30, df = 5, P > 0.7).
Statistical Analysis
To determine the relationship between tilefish
444
catch rate and sediment composition, we used the
silt-clay fraction of each substrate sample as an in-
dependent variable (X) and catch rate (i.e., tilefish
caught/100 hook-h per soak time) as the dependent
variable (Y). Exponential and polynomial regression
models were fit to the data using the SAS statistical
programs (SAS Institute Inc. 1982). The best poly-
nomial model was compared with the nonlinear ex-
ponential model using R^ as the criterion for model
performance. Similar patterns of variation were
observed in plots of residuals from all models, hence
R^ values are a reasonable criterion for model selec-
tion.
Results
The size structure of tilefish caught off Georgia
was typical of unexploited to lightly exploited tilefish
stocks (Grimes et al. 1980; Turner et al. 1983). This
size structure remained relatively constant for ~ 10
mo, after which a slight decrease in catch rates and a
possible truncation of size structure were observed
(authors' unpubl. data). These results confirm verbal
reports that little exploitation has occurred off
Georgia (Harrington footnote 1). Hence, the data
used in this analysis were probably not influenced by
prior exploitation.
A total of 323 tilefish were taken on 19 longline
sets (Table 1). Catch rates ranged from 0 to 5.34 tile-
fish/100 hook-h. Parameter estimates for linear and
quadratic terms of the polynomial regressions were
significantly different from zero (Table 2). Inclusion
of a cubic term, however, did not significantly im-
prove {F = 0.75, P > 0.40) the fit which was obtained
using a second-degree polynomial. The second-
degree polynomial yielded a higher K~ value than the
nonlinear exponential model (Table 2) and hence was
deemed to be the model of best fit. The ?/-intercept of
this model also was not significantly different than
zero (Table 2, Fig. 1) which contributes to its biolog-
ical realism. Using this equation, 74% of the varia-
tion in catch rate could be accounted for by substrate
composition alone.
(O
Table 2.— Comparison of regression models.
Either F-tests (b-,), f-tests (too), or asymptotic
confidence intervals (exponential model) were
used to test the significance of parameters.
Model
'1
'0
/?2
y = 0.087X - 1.496 ** * 0.64
y = 0.155{e0058X) • ps 0.68
y = 0.002X2 _ 0.050X + 0.122 *** ns 0.74
ns = nonsignificant
* = P < 0.05
** = P< 0.001
*** = P< 0.0001
8 6
x:
-
Y=.002X2-
r2=747o
049X-^.
122 •
X 4
-
%/
§3
-
-
JC 1
•
-1 it
•
!• 1 1 1 1 1
p°0
10 20 30
Percent Sill
40 50 6(
-Clay
Figure 1.- Relationship between the silt-clay fraction of the
sediments and tilefish catch rates off Georgia, U.S.A.
Discussion
Tilefish abundance, as estimated by catch rates off
Georgia's continental slope, was strongly correlated
with the silt-clay fraction of the substrate. This rela-
tionship was nonlinear, and based on W- values, a
second-degree polynomial regression provided the
best fit to the data. Off the northeastern United
States, tilefish also were most abundant on fine-
grain sediments (Able et al. 1982), although they
were also found in horizontal burrows in the sides of
submarine canyons (Warme et al. 1977), and in
boulder fields (Valentine et al. 1980). Because tilefish
construct vertical burrows in the substrate (Able et
al. 1982), they require sediments which possess suffi-
cient stability to prevent the collapse of their bur-
rows. It would appear that bottom areas off Georgia
which contain a sand fraction > 60% do not support
substantial tilefish densities (Table 1, Fig. 1). It is
likely that such substrates are not stable enough to
allow tilefish to construct burrows. Thus, the ob-
served correlation between catch rate and substrate
composition has a biologically realistic explanation:
substrates with high silt-clay fractions are conducive
to the construction and maintenance of tilefish bur-
rows, while substrates with high sand fractions are
not. A similar explanation, based on submarine
observations, has been proposed by Able et al. (1982)
to explain tilefish distributions off the northeastern
United States. Although we have not observed tile-
fish burrows off Georgia, they have been identified in
soft bottom areas off South Carolina (R. Jones'*).
While the relationship between catch rates and
sediment composition is quite strong, several poten-
tial sources of error exist in our data. First, catch
rate data were collected from two different vessels
using different gear. Pooling data from the different
vessels, however, would tend to obscure the relation-
ship between catch rates and sediment composition.
Hence, if differences in sampling methods did have
an effect on our data, it would make the estimates of
the catch rate-sediment relationship conservative.
Second, only one substrate sample was collected
with each longline set. While quantification of
*R. Jones, Harbor Branch Foundation, Fort Pierce, FL 33450,
pers. commun. 1983.
445
geographical variation in substrate composition was
beyond the scope of this project, low relief areas off
Georgia generally do not display large variations in
substrate composition (Henry footnote 2). Evidence
to substantiate this point is presented in Table 1, as
substrate samples from areas with similar loran coor-
dinates typically possessed similar substrate com-
positions.
Third, while a seasonal component to catch rate
has been observed off New Jersey (Grimes et al.
1980), our data for this analysis do not strongly
display this trend (Table 1).
In addition, because the area fished did not display
evidence of significant prior exploitation, our results
were not affected by the potentially confounding in-
fluence of commercial fishing.
In conclusion, approximately three-quarters of the
variation in tilefish catch rate off Georgia could be
attributed to variation in a single physicochemical
factor: the silt-clay fraction of the substrate. At pres-
ent, however, the generality of this relationship is
unknown with respect to other geographical areas or
locations with different exploitation histories. In
addition, temperature also has been shown to affect
the distribution of tilefish off the northeastern
United States (Grimes et al. 1980). It is likely that
within areas possessing suitable thermal regimes,
substrate composition is a major factor affecting tile-
fish abundance. While a variety of associations be-
tween fish abundance and physicochemical factors
have previously been identified (Moyle and Cech
1982), to our knowledge, none approach the intensity
of the relationship described herein. We believe that
identification of this relationship will aid fisheries
biologists in the identification and demographic
quantification of tilefish stocks as well as the location
of new fishing grounds.
ACKNOWLEDGMENTS
We appreciate the assistance of the captains and
crews of both the Georgia Bulldog and the Delaware
II, without whom this work would not have been
possible. The following individuals either reviewed
the manuscript or aided in other aspects of the study:
K. Able, C. Barans, P. Bartlett, E. Chin, D. Beau-
mariage, D. Daniels, D. Erickson, M. Freeman, S.
Floyd, C. Grimes, E. Guthertz, D. Harrington, V.
Henry, J. Hill, B. Low, L. Parker, L. Pittman, M.
Rawson, D. Stouder, G. Ulrich, and C. Wenner.
Facilities and logistic support for this study were
graciously provided by the University of Georgia
Marine Extension Service at Brunswick. We also
wish to acknowledge the continued support of our
research by the Georgia Sea Grant College Program
under contract #NA80AA-D-00091. The manuscript
was ably typed by Bonnie Fancher.
LITERATURE CITED
Able, K. W., C. B. Grimes, R. A. Cooper, and J. R. Uzmann.
1982. Burrow construction and behavior of tilefish, Lophola-
tiltis chamaeleonticeps, in Hudson Submarine Canyon. En-
viron. Biol. Fishes 7:199-205.
Barkley, R. a., W. H. Neill, and R. M. Gooding.
1978. Skipjack tuna, Katsuwonis pelamis, habitat based on
temperature and oxygen requirements. Fish. Bull., U.S. 76:
653-662.
Barton, M.
1982. Comparative distribution and habitat preferences of two
species of stichaeoid fishes in Yaquina Bay, Oregon. J. Exp.
Mar. Biol. Ecol. 59:77-87.
Day, D. S., and W. G. Pearcy.
1968. Species associations of benthic fishes on the continental
shelf and slope off Oregon. J. Fish. Res. Board Can. 25:
2665-2675.
Grimes, C. B., K. W. Able, and S. C. Turner.
1980. A preliminarj' analysis of the tilefish, Lopholatibus
chamaeleonticeps, fisherj' in the Mid-Atlantic Bight. Mar.
Fish. Rev. 42(11):13-18.
Laurs, R. M., H. S. H. Yuen, and J. H. Johnson.
1977. Small-scale movements of albacore, Thunnus alalunga,
in relation to ocean features as indicated by ultrasonic track-
ing and oceanographic sampling. Fish. Bull., U.S. 75:347-
355.
Low, R. A., Jr.. G. F. Ulrich, and F. Blum.
1983. Tilefish off South Carolina and Georgia. Mar. Fish.
Rev. 45(4-6):16-26.
Magnuson, J. J., L. B. Crowder, and P. A. Medvick.
1979. Temperature as an ecological resource. Am. Zool. 19:
331-343.
Marliave, J. B.
1977. Substratum preferences of settling larvae of marine
fishes reared in the laboratory. J. Exp. Mar. Biol. Ecol. 27:
47-60.
Moyle, P. B., and J. J. Cech, Jr.
1982. Fishes: an introduction to ichthyology. Prentice Hall,
Englewood Cliffs, NJ, 593 p.
Powell, A. B., and F. J. Schwartz.
1977. Distribution of paralichthid flounders (Bothidae: Para-
lichthys) in North Carolina estuaries. Chesapeake Sci. 18:
334-339.
Radovich, J.
1961. Relationships of some marine organisms of the north-
east Pacific to water temperatures. Particularly during 1957
through 1959. Calif. Dep. Fish Game, Fish. Bull. 112, 62 p.
SAS Institute Inc.
1982. SAS user's guide, stat SAS Institute Inc., Gary, NC.
Turner, S. C, C. B. Grimes, and K. W. Able.
1983. Growth, mortality, and age/size structure of the fish-
eries for tilefish, Lapholatilits chximaeleonticeps, in the
Middle-Atlantic-Southern New England region. Fish. Bull,
U.S. 81:751-763.
Valentine, P. C, J. R. Uzmann, and R. A. Cooper
1980. Geologj' and biology of Oceanographer Submarine Can-
yon. Mar. Geol. 38:283-312.
Warme, J. E., R. a. Slater, and R. A. Cooper.
1977. Bioerosion in submarine canyons, /w D. J. Stanley and
446
G. Kelling (editors), Submarine canyon, fan and trench sedi-
mentation, p. 65-70. Hutchinson and Ross, Dowdon, U.K.
Gary D. Grossman
Michael J. Harris
Joseph E. Hightower
School of Forest Resources
University of Georgia
Athens, GA S0602
THE DEVELOPMENT AND OCCURRENCE OF
LARVAE OF THE LONGFIN IRISH LORD,
HEMILEPIDOTUS ZAPUS (COTTIDAE).
The subfamily Hemilepidotinae, endemic to the
North Pacific Ocean, is one of the more generalized
subfamilies within the Cottidae (Peden 1978).
According to Peden (1978), the subfamily is compos-
ed of three subgenera: 1) Calycilepidottcs which in-
cludes Hemilepidottcs spinostts; 2) Hemilepidotus
which includes H. hemilepidotus, H. jordani, H.
zapus, and H. gilberti; and 3) Melletes which includes
H. papilio. The early life histories of most species are
inadequately known and separation of larvae in mix-
ed samples is difficult. Gorbunova (1964) described a
number of larval series which she labeled H.
hemilepidotus, H. gilberti, H. gilberti zapus, H. jor-
dani, and H. papilio,^ but these descriptions are in-
complete as well as incorrect for several species
(Peden 1978; Richardson and Washington 1980).
Hattori (1964) described a series of//, gilberti larvae
(7.1-32.5 mm), and Peden (1978) illustrated postlar-
vae (> 18 mm) of //. hemilepidotus, H. spinosus, H.
zapras, and H. jordani. Richardson and Washington
(1980) described larvae of H. hemilepidotus and H.
spinosus. We here provide the first complete descrip-
tion of//, zapus larvae, and include comments on lar-
val occurrence in the eastern Bering Sea. This work
supplements and clarifies the work of previous
researchers by providing diagnostic characters
useful in distinguishing the species.
MATERIALS AND METHODS
Specimens of//, zapus used in this study were col-
lected during ichthyoplankton surveys conducted in
the Bering Sea by the Northwest and Alaska Fisher-
ies Center between 1977 and 1980. Morphological
measurements were made on 57 unstained larvae
(6.7-22.0 mm SL) following Matarese et al. (1981),
except depth at caudal peduncle which was measured
at the point of least depth. Measurements were
grouped by 1 mm SL intervals, and the means of the
measurements within each interval were plotted as
percentage of the mean of standard lengths or head
lengths within the interval (Kendall and Vinter
1984). A computer-generated best nonparametric
curve, based on all data points, was drawn to illus-
trate relative growth trends. Counts of meristic
structures were made on 18 specimens differentially
stained according to Dingerkus and Uhler (1977)
following procedures outlined in Matarese et al.
(1981). Terminology of head spination generally
follows Richardson and Laroche (1979) and Richard-
son and Washington (1980). Illustrations were made
by the junior author with a camera lucida, and all
specimens were preserved in either 3% Forma-
lin^ buffered with sodium borate or 100% glycer-
in.
Identification of
Hemilepidotus zapus
We have routinely collected three types of Hemi-
lepidotinae larvae during ichthyoplankton surveys in
the eastern Bering Sea (1977-80). According to
Peden (1978), four species of adults occur in this
area: Hemilepidotus hemilepidotus, H. jordani, H.
zapus, and H. papilio. Although preflexion larvae of
H. hemilepidotus and H. jordani cannot presently be
separated, we can separate the two species at noto-
chord flexion according to differences in external
pigment along the posterior body. Hemilepidotus
hemilepidotus larvae develop pigment above the
notochord along the posterior body earlier and in
greater density than larvae of//, jordani (Fig. lA,
B). Initially, the third series of larvae (< 17.0 mm SL)
was misidentified as //. papilio (see Waldron and
Vinter^) based on the presence of urostyle pigment
(Gorbunova 1964). With the acquisition of larger
specimens, > 17.0 mm SL, the complete series was
later identified as H. zapus based on a set of charac-
ters taken in part from Peden (1978) (Table 1). Gor-
bunova's (1964) specimen attributed to H. zapus
lacks pigment on the urostyle; of her two illustra-
tions of//, papilio (footnote 1) only the 10.7 mm SL
^Hemilepidotus papilio (= Melletes papilio from Gorbunova
(1964)).
^References to trade names do not imply endorsement by the Na-
tional Marine Fisheries Service, NOAA.
^Waldron, K. D., and B. M. Vinter. 1978. Ichthyoplankton of
the eastern Bering Sea. Unpubl. manuscr., 77 p. Northwest and
Alaska Fisheries Center, National Marine Fisheries Service,
NOAA, 2725 Montlake Boulevard E., Seattle, WA 98112.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985
447
External pigment
nternal pigment
B
External pigment
nternal pigment
External pigment
nternal pigment
448
Figure 1.- Postanal pigment patterns in //emitepirfotw-s larvae: A) H. jordani, 13.7 mmSL; B)H. hemilepidotus, 12.7 mm
SL; C) H. zapus, 12.6 mm SL.
Table 1. — Comparison of some important differentiating
characters in Hemilepidotus zapus and H. papilio.
This
Characters
study
H. zapus^
H. papilio^
Dorsal spines
X-X1
XI (X1-X11)
XII (X1-X111)
Pectoral fin rays
16-17
16(15-17)
17-18 (16-18)
Total soft fin rays;
dorsal, anal, and
both pectoral fins
71
67-76
69-74
Lateral line pores
54-56
52 (47-58)
59 (49-65)
Number of vertebrae
37-38
37-38
40
Number of horizontal
scale rows in
ventral band
ca. 8
8 or 9
ca. 4
Dorsal fin
notch between third
and fourth spine
yes
yes
no
'Data are from Peden (1978); mean is followed by range in
parentheses.
larvae \sH. zajms, while the 13.7 mm SL larva lacks
urostyle pigment and is probably H. jordani
Early larvae of H. zajms (6.5-17.0 mm SL) were
linked together by the presence of melanophores
above and below the urostyle (Figs. IC, 2); such
melanophores are lacking in all other known
Hemilepidotinae larvae. Larvae undergoing noto-
chord flexion can be distinguished from H. hemilepi-
dotus by the lack of external pigment along the
posterior body and from H. jordani by the presence
of ventral midline pigment which curves up toward
the urostyle (Fig. 1).
After notochord flexion and through the juvenile
period, counts of meristic structures as well as a com-
bination of adult characters (Peden 1978) will allow
separation of the three species. Postflexion larvae of
H. zapus have scales on the caudal peduncle that will
distinguish them from other, similar-sized Hemilepi-
dotinae larvae. These larvae also have a characteris-
tic notch in the first dorsal fin, between the third and
fourth spine, that is present in adults of all Hemi-
lepidotus except H. papilio (Fig. 2F). A summary of
some diagnostic features of all known Hemilepidotus
larvae is presented in Table 2. Larvae and juveniles
of H. papilio remain unknown.
General Trends of Development
Pigmentation (Fig. 2)
In the smallest larvae (6-7 mm SL), pigment ap-
pears on the head dorsally over the midbrain and on
the anterior forebrain. In larger larvae 7-9 mm SL,
additional pigment appears at the base of the hind-
brain, posterior to the eye and in the opercular area.
In postflexion larvae, head pigment increases.
Separate pigment patches appear posterior to the
eye (usually about 5 or 6 spots) and on the operculum
dorsoposterior to the preopercular bone. Larvae 6-7
mm SL have pigment on the nape and on the dorsal
surface of the gut. Gut pigment increases laterally
with development, and in larger postflexion larvae it
becomes more internal than external. By 14-15 mm
SL, nape pigment extends ventrally to the dorsal
surface of the gut.
There are five general areas of pigmentation in the
postanal region: 1) an external row (appearing
more or less double) of melanophores along the dor-
sal midline extending from the nape to the last
myomere; 2) a dorsolateral row of internal pigment
along the notochord, extending from the nape to
about the last 4-7 myomeres; 3) an external row of
melanophores along the ventral body midline from
midbody (about 1 1 myomeres after anus) to the last
myomere; 4) a ventrolateral row of internal pigment
along the notochord, beginning at about 4-6 myo-
meres after the anus and extending to about 6 or 7
myomeres from the end of the tail; and 5) a few ex-
ternal melanophores along the notochord in the
caudal peduncle area, and external melanophores
dorsal and ventral to the notochord at the posterior
tail tip. Prior to notochord flexion, at about 9.0 mm
SL, the anterior ventral midline pigment gradually
becomes more internal. In postflexion larvae, this
ventral midline row is comprised of < 10 melano-
phores beginning about 17 myomeres posterior to
the anus. By 16.7 mm SL, all the postanal pigment is
internal except for the dorsal midline melanophores
and a few spots in the caudal peduncle area. After
about 17 mm SL, melanophores in the caudal pedun-
cle are no longer visible.
Morphology (Table 3; Fig. 3)
Relative growth trends are summarized in Figure
3. Preanal length, head length, depth at pectoral fin,
snout to anal fin length, and snout length increase
with development. Eye diameter as a proportion of
head length undergoes a gradual decrease with
development. Depth at the caudal peduncle and the
length from the snout to dorsal fin origin increase
sharply with development in larvae about 16.0-19.0
mm SL and then decrease in larger specimens.
Meristic Structures (Tables 4, 5)
Branchiostegal rays have begun to ossify in our
smallest specimens (7-8 mm SL), and the adult com-
plement of six rays is completely ossified in larvae
^ 12-13 mm SL.
449
Figure 2. -Larvae of Hemilepidotus zapus: A) 6.7 mm SL; B) 8.7 mm SL; C) 11.0 mm SL;
Fins -All fin rays show their initial ossification in
larvae between 12 and 13 mm SL. Fin formation oc-
curs in the sequence: dorsal spines and fin rays, anal
fin rays, and principal caudal fin rays (12-13 mm SL);
pectoral fin rays (13-14 mm SL); pelvic spine and fin
rays (15-16 mm SL); and secondary caudal fin rays
(16-17 mm SL). The pterygiophores supporting dor-
sal fin rays begin ossifying at 16-17 mm SL, and
those supporting anal fin rays begin ossifying at
17-18 mm SL. The largest specimen (20.0 mm SL)
has completely ossified dorsal and anal pterygio-
phores.
Axial skeleton - Neural and haemal spines have
started ossification in the smallest larvae 7-8 mm SL,
and are fully ossified in larvae 15-16 mm SL. Abdom-
inal vertebral centra are completely ossified in larvae
12-13 mm SL, but the caudal vertebral centra are
not fully ossified until larvae are slightly larger at
about 14-15 mm SL.
Lateral line scales do not begin ossifying until
larvae are 18.0 mm SL, and our largest specimen
(20.0 mm SL) has a fully ossified complement of
scales.
Spination (Table 5) -The development of head
spines is summarized in Table 5. The parietal and
nuchal spines fuse in larvae > 13 mm SL and appear
as a single spine in the larger larvae 18-20 mm SL. A
postocular spine is ossified in larvae 12-13 mm SL
but disappears by 18-20 mm SL. A small spine below
the eye (infraorbital) ossifies by 14-15 mm SL, but is
no longer visible in specimens 20 mm SL.
450
Figure 2.-Continued-D) 13.0 mm SL; E) 16.7 mm SL; F) 22.8 mm SL.
Occurrence of Hemilepidotus zapus in
the Eastern Bering Sea
During 8 yr of sampling ichthyoplankton at a total
of 250 stations in the eastern Bering Sea (in the ap-
proximate area between lat. 60 °N and long. 174°W
with more intensive sampling between the Pribilof
Islands and Unimak Island), only 58 Hemilepidotus
zajMS larvae were collected. The number of positive
stations is indicated in Figure 4.
Small H. zapus larvae (6.7-10.1 mm SL) were col-
lected during winter in surface water north of the
Pribilof Islands (Fig. 4 A). Only a single larva (11.0
mm SL) was taken in February 1978 at the surface
in about the same area over the slope (Fig. 4A). Our
largest collection of larvae (12.2-16.7 mm SL) was
made in late April and early May (Fig. 4B). Most of
the larvae were collected in neuston nets at stations
over the slope, but in May a few larvae were taken
over the continental shelf. Larvae primarily occurred
south of the Pribilof Islands. The largest larvae
(18-22 mm SL) were collected during June and July
at scattered stations throughout the area including
only one northwest of the Pribilof Islands (Fig. 4C).
Although data are insufficient to document the
exact time and geographical extent of spawning, the
presence of small larvae indicates some spawning oc-
curs in early winter north of the Pribilof Islands.
Peden (1978) indicated that adult and postlarval H.
zapus have been collected only along the Aleutian
Islands. Further studies are needed to investigate
whether larvae and juveniles move south to the Aleu-
451
<0
3
O
s.
d)
a:
c
o
T3
C
CO
c
o
Q.
c
3
C3)
C
C
3
(U
o
(0
c
o
c
<u
E
C3)
CO
C
CD
■•— '
CO
o
Q.
•o
a>
o
cu
CO
I
m
<
c
c
o
o
cu
o
c
o
CO
c
o
CO
.E -o
X3
■D
3
•D
jc
"D
^ . 3
3
3
CO O
CO O ""^
*-*
o
CO
"D
CO CX3
CO
■o
CO 00 <"
to
(0
CO
C
CD
§2^
c
CO
> 05 CO
CO
CO
r:
^
!c
CO
o
CO
o
c I'
Oi 0°
T3 O
CO 0)
O -
5.E
^E
o 2
> i5
O CO
^ c
c
CB
E
C3) CD
s: 5
<
o.E
c ■ — ■
O CD
o.E
c ^^
O CO
— CD
CO c
CO —
Q E
—'—CD
CD 05 C
k_ ^_ —
J5 §E
CO
3
o
CO 2 E E
« C ^ C
Q. <U - o
CO > E o
lis
o
. c
OJ JO
OJ CD
E E
o^
E A
' D3
i- -
E E 05
CD O >
O CD
>^ <D CD
CD n ^
CO
3
o
t o >,
00 cE
CD CO O
- CD)
E E
E E 5>
CO O ■>
O CO
>^ CD CD
CQ JD ^
CO
3 "D
O CO
3 <D
c -c=
'^ §
>. O O
CD o ^
E
E
ID
E
o
O W' CD
"e"
<D
- 9^
_ >
(D CO
E -^
o
>> CD)
O !r
CO
° c cz
Q. E .E
CO
CO
o
C
Q.
CO
CC
— " « c
2 O CO CD
CD ^ "O E
O
CD
c
O
o
CO CO CI
CD 3 CO
Q)
CO
CD
.E E ^
D) 9 CD in
CD ^ ^ T—
CD £ CO V
t CD
E 2
T- (D
■^ 13
CD E
CIi
CO
o
CO 1-
C CD
C3) CO CO
^ <'i O n
I"
<= 0) >,
CO c ^
>- ° ^
CD CO O
h (D
E 2
T- <D
>- TD
>-?
CD E
■^ "O
•D
E CD
h. E
C T
CD -"J-
S Q)
o >,
O) CD
c j:
?i '^ <z
3 CO b JD CD
(D
CO
O
TD
5.
Q)
CD
■C
c
CO
-^
^
"O
o
CD
3
CO
_J
re
CD
O
c
o
^ g
CD
E CO
— <D
eI
CD CD D.
O
CD CO
CO
CD C
E S; >-
O -= C
CO .E o
ffl E o
co a: 5;
u
CO
^^
■ ^
3
E
CO
o
:3
CD
;o
E
-C
Q.
CO
i
-S
CD
C
o
O CO
*- CJ)
CD ■^
X
T3
0)
CD
CD
C
CO CD
E
O)
0)
>>
CO
o
cd'
. i5
E - CD ^ i=
(3) ™ lo E o 0)
■q. CO CO = ^ E
c a> o ~ " o>
3 CD -D E i5 'q.
C
CO
c "^
ID
>
c O
O CO
O
O J2 CD
O CO JD 3
o
CO CO c=
0) 3 jD
5 E <!'
E ™ E
o) 9 CD Ln
CD -^^ ^ T—
DD E CO V
CO
CD C
E q3 >•
o •= c
CO .E o
CD
^E
00 O
CD E
.^ CO
CO ^ 3
C Q) c
O) W) CO
CD O o
^\ /-\ ^-'
O)
c
^ >.
o) o
o
CD
CD CO
CD
C
o
z.
o
E 3 ™
-c -c
CO .
3
E
CO 3: S
>
CO
CD
CO
c
CD
CO C 3
— CD JD
— -^ "-1 CO
CO 3: ■£ CD
CO
3
CL
CO
O
to CO C
- 3 CO
CO c
<D
CD
£
t3) O CD tn o
>. •.- ^
£ « V
CD
c
o
CD
c
o
z
0
c
o
c
o
CO
c
CO
CT
OJ
CD
J2
5
£
CO
, .
3
C
o
C
CD
>>
CO
E
E
B
Q- 00 CD
I.
■Q
T3
CD
CO
Q.
CD
CO
CD
n
O
c
c
(0
tJ
c
P <B
■1 =
C "C
CO O
si
■5.0
eI
0} ^
■C CD
°1
CD C
o E
- £
£ o
Q-Z
452
Table 3. — Morphometries (in millimeters) of larvae and juveniles of Hemilepidotus zapus. Specimens
between dasfied lines are undergoing notochiord flexion.
Depth at
Depth at
caudal
Snout to
Standard
Total
Preanal
Head
Snout
Eye
pectoral
pedun-
Snout to
anal
lengtfi
length
length
length
length
diameter
fin
cle
dorsal
fin
6.5
6.9
2.4
1.3
0.1
0.8
1.3
6.7
7.4
2.4
1.3
0.1
0.8
1.3
6.7
7.2
2.4
1.3
0.1
0.8
1.3
7.1
7.5
2.7
1.4
0.1
0.8
1.3
7.1
7.7
2.8
1.3
0.1
0.9
1.3
7.3
7.8
2.7
1.4
0.1
0.9
1.4
7.6
8.2
2.7
1.3
0.1
0.9
1.4
7.7
8.3
2.7
1.3
0.1
0.9
1.5
8.2
8.9
3.1
1.7
0.2
1.0
1.5
8.2
8.9
3.2
1.8
0.2
1.0
1.6
8.5
9.1
3.3
1.9
0.3
1.0
1.6
8.7
" " 9.5 ' '
' ' ' 3.5 " "
2.0
0.3
1.1
" I.V""
8.7
9.4
3.4
2.0
0.3
1.1
1.7
9.1
9.8
3.6
1.9
0.3
1.0
1.7
9.2
10.0
3.6
2.1
0.2
1.1
1.7
9.2
9.8
3.6
1.9
0.2
1.1
1.7
9.3
10.1
3.9
2.1
0.2
1.1
1.7
9.5
10.1
4.0
2.1
0.3
1.2
1.8
9.8
10.5
3.6
1.9
0.2
1.1
1.7
10.1
10.9
4.0
2.3
0.3
1.2
1.8
11.0
12.0
4.4
2.6
0.3
1.3
2.1
12.0
13.5
5.5
3.2
0.6
1.4
2.5
1.0
3.0
5.8
12.2
14.3
5.5
3.3
0.5
1.5
2.5
0.9
5.8
12.2
14.0
5.6
3.4
0.5
1.5
2.6
0.9
3.3
5.9
12.3
14.4
5.6
3.3
0.4
1.5
2.6
1.0
3.2
5.9
12.6
14.5
5.8
3.3
0.5
1.5
2.8
1.1
3.3
6.0
12.9
15.0
5.7
3.5
0.6
1.5
2.7
1.1
3.3
6.1
12.9
14.6
5.6
3.4
0.4
1.5
2.6
1.0
3.4
6.0
13.0
15.0
5.6
3.7
0.6
1.5
2.6
1.1
3.3
6.0
13.0
15.2
5.6
3.5
0.6
1.6
2.7
1.1
3.3
6.0
""i3"2""'
15.4
5.5
3.5
0.6
1.6
■ - - -^'g ""
1.1
3.4
5.9
13.5
16.0
6.0
3.5
0.6
1.6
2.8
1.2
3.5
6.4
13.6
16.0
5.9
3.7
0.6
1.5
2.8
1.2
3.3
6.3
13.8
16.1
5.9
3.7
0.6
1.7
3.0
1.2
3.4
6.3
14.0
16.7
6.3
3.7
0.6
1.8
3.2
1.3
3.7
6.6
14.3
17.1
6.5
3.9
0.6
1.8
3.1
1.3
3.7
6.9
14.4
17.2
6.8
4.0
0.6
1.9
3.2
1.4
4.0
7.1
14.5
17.2
6.9
4.0
0.7
1.9
3.3
1.4
4.1
7.2
14.7
17.5
6.8
3.9
0.6
1.9
3.2
1.3
3.8
7.1
14.9
17.9
7.0
4.0
0.6
1.8
3.3
1.4
4.0
7.2
14.9
18.0
7.0
4.1
0.6
2.0
3.4
1.5
4.2
7.3
15.1
18.6
7.2
4.3
0.7
2.0
3.7
1.6
4.2
7.5
15.2
18.3
7.2
4.5
0.7
2.1
3.7
1.6
4.2
7.5
15.3
19.0
7.5
4.7
0.8
2.0
3.9
1.6
4.4
7.8
15.5
19.0
7.3
4.5
0.8
2.0
3.8
1.6
4.5
7.6
15.6
19.0
7.4
4.6
0.7
2.0
3.8
1.6
4.3
7.7
15.9
19.7
7.8
4.7
0.8
2.1
3.9
1.7
4.6
8.1
16.7
20.7
7.9
5.1
0.8
2.1
4.3
1.8
4.8
8.2
16.8
21.3
8.1
5.4
0.8
2.3
4.5
1.7
5.1
8.5
16.9
20.9
8.2
5.2
0.8
2.2
4.4
1.7
5.0
8.6
18.0
23.0
9.0
6.2
1.0
2.3
5.5
1.9
5.2
9.3
19.1
25.0
9.8
6.3
1.0
2.3
5.6
2.0
5.4
10.0
19.3
24.9
10.1
7.0
1.3
2.6
5.7
1.9
6.1
10.5
20.5
26.0
10.5
6.7
1.3
2.5
6.2
2.0
5.5
10.9
21.0
26.5
10.9
7.0
1.3
2.5
6.3
2.1
5.7
11.1
21.0
26.6
11.1
7.0
1.5
2.5
6.3
2.0
6.0
11.5
21.2
27.0
11.4
7.2
1.6
2.5
6.5
2.0
6.1
11.6
22.0
27.5
11.5
7.3
1.3
2.6
6.7
2.1
6.0
11.9
453
sei
-^48-
<
CI44.
Z
<
^4<H
-36
LLl
O
a.
28;
PREANAL LENGTH
1 S il TS 25"
40
X
HEAD LENGTH
t-3*
0
z
UJ
^^^n
-•3?
^^y^
0
•x
'-''^
K
./
<
/
0?R
y
Z
■ ^
<
V^
1—
/
'^2+
^
u.
X
0
'/
^2&
./
>u
0
K
UJifr
a.
'^i 4 «
\1
t'e
20
3&I
-32
-'28-
o
<
Q24
z
<
I—
20
:i6-
u
a:
UJ12
a.
DEPTH AT PECTORAL
12
16
20
64
t-60^
-■56
o
<
<=>52
z
<
I—
en
48
:44
o
iu40
0.
36:
SNOUT TO ANAL FIN
? i il TS 20
STANDARD LEnCTH (MM)
Figure 3. -Relative trends in selected morphometric features
Table 4. — Development of meristic characters in larvae of Hemilepidotus
Sample
size
Fin rays
Size
interval
(mm SL)
Caudal
Dorsal
Anal
Pectoral
Pelvic P
rincipal
Secondary
Total
7-8
2
8-9
3
9-10
2
MO-12
—
12-13
3
X,11-21
17
8-10
1,0
12
3-5
15-17
13-14
1
Xl,21
17
16
1,3
12
9
21
14-15
3
X-XI-20-21
17
13-16
1,3
12
9
21
15-16
2
X,21
17
16
1.4
12
11-13
23-25
16-17
1
Xl,20
17
17
1,4
12
15
27
18
1
XI,2G
16
16
1,4
12
15
27
20
1
Xl,21
17
16
1,4
12
14
26
'Specimens in this size group did not accept alizarin stain.
^Haemal spines 23-24 are fused.
454
29.6
■
a
X
SNOUT
TO
DORSAL
•—
FIN
/\
z28.8
/
N.
UJ
1
\
_i
n 1
\ "
Q28.0
1
\
q:
j
\
<
1
\
o
j
^27.2
/
>—
/
a
trt
/
u.26.4
1
o
\/
,_
\/
Z25.6
LLl
O
<r.
IU24.8-
Q.
i \
6
12
16
20
10.6
9.8
q9.0
<
a
Z8.2
<
C/)
r.^
^6.6
UJ
o
UJ 5.8-
0.
5.0;
DEPTH AT CAUDAL
PEDUNCLE
12
16
20
EYE DIAMETER
32
28-
I
t—
o
==24
UJ^^
_J
o
<20-
UJ
X
o16-
uj,2J
0^
8
SNOUT LENGTH
4 ~i~ 12 16 20
STANDARD LENGTH (MM)
Figure 3. -Continued- during ontogeny in Hemilepidotus zapus.
12
16 20
zapus. Specimens below the dashed line have connpleted notochord flexion.
Sample
Ptery-
giophores
Axia
skeleton
Branchi-
ostegal
Size
interval
Sp
nes
Cent
ra
Lateral
1 in6
(mnn SL)
size
Dorsal
Anal
Neural
Haema
Precaudal
Caudal
rays
scales
7-8
2
12-19
9
2-3
8-9
3
20
10
4
9-10
2
29
17
5
'10-12
—
12-13
3
35
22
12
23
6
13-14
1
36
23
12
25
6
14-15
3
36
24
12
24-26
6
15-16
2
37
=25
12
26
6
16-17
1
15
37
24
12
25
6
18
1
30
16
37
25
12
26
6
54
20
1
31
17
37
24
12
26
6
56
455
Table 5. — Development of spines in the head region of Hemilepidotus zapus larvae. Specimens below the dash-
ed line have completed notochord flexion.
Size
interval Sample
(mm SL) size Parietal
Nuchal
Preoper-
cular
Oper-
cular
Post-
ocular
Superior
infra-
orbital
Nasal
Post-
temporal
Artic-
Clei-
supra-
ular
thral
cleithral
7-8
2
0-1
8-9
3
1
9-10
2
1
'10-12
12-13
3
21
4
1-2
13-14
1
2-1
4
2
14-15
3
2-1
4
3
1 1
2
15-16
2
2-1
4
3
1 1
'3
16-17
1
2-1
4
3
1 1
1 1
=3
18
1
1
4
3
0
1 1
1 1
^3
20
1
1
4
3
0
0 1
^1 I
^3
'Specimens In this size group did not accept alizarin stain.
^Spines are beginning to fuse at base but points can still be observed.
^Spine(s) reduced in size.
JAIMUARY-MARCH
6.7-11.0 mm SL (n=21)
- 62 OOM
60 00
S8 00
- 56 00
- 54 00
I- 52 00
180 00
170 OOW
160 00
Figure 4. -Occurrence of Hemilepidotus zapu>< larvae in the
eastern Bering Sea: A) January-March (IMF80 and MF7801); B)
April-May (MF77B5(6)); C) June-July (2MF79). Closed circles in-
dicate neuston stations and closed diamonds indicate bongo stations.
Station data on file at the Northwest and Alaska Fisheries Center,
Seattle, WA.
APRIL-MAY
12.2-16.7 nnmSL (n=29)
JUNE-JULY
18.0-22.0 mm SL {n=8)
62 OON
60 00
- 58 00
56 00
54 00
- 52 00
160 00
180 00
62 OON
60 00
58 00
56 00
- 54 00
- 52 00
160 00
456
tians or whether adult H. zapus range further north.
Acknowledgments
We thank Jean R. Dunn and Arthur W. Kendall,
Jr. (Northwest and Alaska Fisheries Center) for
helpful discussions and review of the manuscript.
Alex E. Peden (British Columbia Provincial
Museum) kindly assisted in the identification of
Hemilepidotus zaipus postflexion larvae.
Literature Cited
DiNGERKUS, G., AND L. D. UHLER.
1977. Enzyme clearing of alcian blue stained whole small
vertebrates for demonstration of cartilage. Stain Technol.
52:229-232.
GORBUNOVA, N. N.
1964. Razmnozhenie i razvitie polucheshuinykh bychkov
(Cottidae, Pisces) (Breeding and development of hemilepido-
tine sculpins (Cottidae, Pisces)). [In. Russ.) Tr. Inst.
OkeanoL, Akad. Nauk SSSR 73:235-251. (Transl. by Isr.
Program Sci. Transl., 1966; in T. S. Rass (editor), Fishes of
the Pacific and Indian Oceans, biology and distribution, p.
249-266; available U.S. Dep. Commer., Natl. Tech. Inf. Serv.,
Springfield, Va., as TT 65-50120.)
Hattori, S.
1964. Studies on fish larvae in the Kuroshio and adjacent
waters. [In Jpn., Engl, synop.) Bull. Tokai Reg. Fish. Res.
Lab. 40, 158 p.
Kendall, A. W., Jr., and B. Vinter.
1984. Development of hexagrammids (Pisces: Scorpaeni-
formes) in the Northeastern Pacific Ocean. U.S. Dep.
Commer., NOAA Tech. Rep. NMFS 2, 44 p.
Matarese, a. C, S. L. Richardson, and J. R. Dunn.
1981. Larval development of the Pacific tomcod, Microgadus
proximus, in the Northeast Pacific Ocean with comparative
notes on larvae of walleye pollock, Theragra chalcogramma,
and Pacific cod, Gadus macrocepkalus (Gadidae). Fish. Bull. ,
U.S. 78:923-940.
Peden, A. E.
1978. A systematic revision of the hemilepidotine fishes
(Cottidae). Syesis 11:11-49.
Richardson, S. L., and W. A. Laroche.
1979. Development and occurrence of larvae and juveniles of
the rockfishes Sehastes crameri, Sebastes pinniger, and
Sebastes helvamaculatus (family Scorpaenidae) off Oregon.
Fish. Bull., U.S. 77:1-46.
Richardson, S. L., and B. B. Washington.
1980. Guide to identification of some sculpin (Cottidae) larvae
from marine and brackish waters off Oregon and adjacent
areas in the northeast Pacific. U.S. Dep. Commer., NOAA
Tech. Rep. NMFS Circ-430, 56 p.
Ann C. Matarese
Beverly M. Vinter
NOAA, Natwnal Marine Fisheries Service
Northwest and A laska Fisheries Center
2725 Montlake BouLeniard East
Seattle, WA 98112-2097
AN APPROACH TO ESTIMATING
AN ECOSYSTEM BOX MODEL
Recent trends in ecosystem modeling have produced
complex simulation models which are very data in-
tensive (Andersen and Ursin 1977; Laevastu and
Larkins 1981). However, in many situations the con-
struction of a biomass budget for a box model of an
ecosystem is relatively simple and can provide impor-
tant information about the ecosystem standing stock
and energy flow (Walsh 1981; Pauly 1982; Polovina
1984).
The ECOPATH model is an analytical procedure
to estimate a biomass budget for a box model of an
ecosystem given inputs which specify the com-
ponents of the ecosystem, together with their mor-
tality, diet, and energetics value. A computer pro-
gram for ECOPATH has been written in BASIC-80,
version 5.21, by Microsofti (CP/M version). A listing
of the ECOPATH computer program and a user's
manual are available from the author.
The ECOPATH model produces estimates of mean
annual biomass, annual biomass production, and an-
nual biomass consumption for each of the user
specified species-groups. The species-groups repre-
sent aggregations of species with similar diet and life
history characteristics and which have a common
physical habitat. The ECOPATH model is not a
simulation model with a time component as are some
more complex ecosystem models. It estimates a
biomass budget for the marine ecosystem in a static
situation under the assumption that the ecosystem is
at equilibrium conditions.
Equilibrium conditions are defined to exist when
the mean annual biomass for each species-group does
not change from year to year. This condition results
in a system of biomass budget equations which, for
species-group i, can be expressed as
Production of biomass for species i - all
predation on species i - nonpredatory
biomass mortality for species i - fishery catch
for species i = 0 for all i. (1)
The ECOPATH model expresses each term in the
budget equation as a linear function of the unknown
mean annual biomasses {B,'s) so the resulting
biomass budget equations become a system of simul-
taneous equations linear in the B-s. The mean annual
biomass estimates are obtained by solving the
system of simultaneous linear equations.
'Reference to trade names does not imply endorsement by the Na-
tional Marine Fisheries Service, NOAA.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
457
The formulation of each term of the biomass
budget equation will now be presented in detail.
The Model
Biomass Production
Production (P) for a cohort of animals over 1 yr is
defined as
1 J
F = f N, — (w,) dt
0 dt
and mean annual biomass (B) for the cohort is de-
fined as
B = J NtWfdt
where iV, is the number of animals and w, the mean
individual weight at time t.
Allen (1971) investigated the production to bio-
mass (PIB) ratio for a cohort over a range of mortal-
ity and growth functions. For a number of growth
and mortality functions, including negative exponen-
tial mortality and von Bertalanffy growth, the ratio
of annual production to mean biomass for a cohort is
the annual instantaneous total mortality (Z,). For a
species-group which consists of n cohorts or species,
with instantaneous annual total mortality (Z,) for
cohort or species i, where mortality is determined by
a negative exponential function and growth by a von
Bertalanffy growth function, the total species-group
production (P) is the sum of the cohort production
(P,) and can be expresed as
P= I P,= 1 Z,B,
(2)
i:=i
( = 1
Under the assumption that the Z's are all equal to
say Z, then total species-group production can be ex-
pressed as
P = Z ■ B
where B is the mean annual species-group biomass.
Allen (1971) has also shown that when growth in
weight is linear, the PIB ratio is equal to the recipro-
cal of the mean age for a range of mortality func-
tions. For a number of other growth and mortality
functions the ratio of cohort PIB can be the recipro-
cal of the mean lifespan. Thus, for a range of growth
and mortality functions, total species-group produc-
tion can be expressed as
P = C ■ B
where B is the mean annual species-group biomass,
and C is a parameter.
In an application of ECOPATH to an ecosystem of
French Frigate Shoals where there was very little
fishing mortality, the PIB ratio for fishes and crusta-
ceans was taken as the annual instantaneous natural
mortality (M); whereas, for primary and secondary
producers whose growth is more likely to be linear
than the von Bertalanffy, the PIB ratio was esti-
mated as the reciprocal of the mean age (Polovina
1984).
Predation Mortality
The predation mortality is the fraction of the
biomass of a species-group which is consumed by all
predators excluding fishing mortality. Two types of
information are needed. First the food web or
predator-prey relationships must be defined. A diet
composition matrix DC,, must be specified where an
entry DC,j from this matrix refers to the proportion
(by weight) of prey j in the diet of predator (. The
primary source of this information is the analysis of
stomach contents data. At least in one study it has
been shown that there is a high correlation between
diet indices based on weight, volume, and percentage
of occurrence for stomach content data, and thus
either index may be used to generate the DC matrix
(Macdonald and Green 1983). The second type of in-
formation needed to ascertain predation mortality is
the food requirements of the predator. The
ECOPATH model requires the user to specify FR„
the ratio of annual consumption to mean annual
biomass. The annual food required by the predator is
the product of FP, and P,.
Some values of daily food required as a fraction of
body weight range from 0.005 to 0.02 (Laevastu and
Larkins 1981). Based on these daily estimates a
range of annual food required as a fraction of mean
biomass (FPj is 1.8 to 7.3.
Nonpredation Mortality
All mortality attributable to causes other than
predation and fishing is termed nonpredatory mor-
tality. The ECOPATH model defines ecotrophic effi-
ciency e, as the fraction of total production which is
removed by fishing and predation mortality. This
458
was 0.95 in the French Frigate Shoals model. The
nonpredator mortality rate is (1 - e,) • Z|, and the
amount of production which goes to nonpredation
mortality is
(1 - e,) P, = (1 - e,) C, B,.
For n species-groups the biomass budget Equation
(1) becomes a system of n simultaneous equations as
follows:
C,5i - 1 {FR,)B,DC„ - (1 - e^)C,B, = catchj,
k= 1
C,B, - I^ (FRk) B^ DC,, - (1 - e,) C,B, = catch.
Schoals in the Northwestern Hawaiian Islands pro-
vided the estimates for many of the input parameters
required by the ECOPATH model as well as some
estimates of biomass and production to serve to
evaluate the estimates produced by the model. The
estimates of biomass and production generated by
the application of ECOPATH to French Frigate
Shoals are given in Figure 1 . In general the model's
estimates of biomass and production are in good
agreement with the available field data (Polovina
1984). In the application of the French Frigate
Shoals, the biomasses of the top level carnivores are
treated as fixed inputs thus a particularly appropri-
ate validation of the model is the comparison of the
estimate of net benthic primary production with an
independent estimate from field data. The model
estimated net benthic primary production, adjusted
to the total 1,200 km^ habitat of French Frigate
Shoals, at 2.3 x 10*' kg • km-^ • yr-i while the esti-
mate based on field data was 2.5 x lO'^kg • km"- ■
yr-i (Griggetal. 1984).
C„B„ - I iFR,)B,DC,„ - (1 - e,;)C„B„ = catch„.
*■=!
With input estimates for parameters C„ FR„ DC,j,
and e, for all i and j, and catches (catch,) if there is
fishing, this system of equations is a system of n
simultaneous equations linear in the unknown B-s.
This system of equations can be expressed in matrix
form as AB = C, where A is an n x n matrix of
coefficients, B is an n-dimensional vector of mean an-
nual species group biomass, and C is the vector of
fishery catch where the ith element is the total catch
of the ith species-group.
If the matrix A is of full rank and if there are some
fishery catches for some species so the vector C is not
null, then there typically exists a unique nontrivial
solution vector of biomass B. If there are no fishery
catches then it is necessary to provide an estimate of
at least one of the mean species group biomass 5,
before there exists a unique nontrivial biomass vec-
tor B which solves the budget equation. In the appli-
cation of ECOPATH to an ecosystem at French
Frigate Schoals where there was no fishing mortali-
ty, the biomasses of three apex predators were esti-
mated from field censuses and treated as known in-
puts. In this application the ith element of C vector
was the annual predation by the three apex
predators on the ith species- group.
Five years of field work targeting most of the com-
ponents of the marine ecosystem at French Frigate
The Computer Program
The ECOPATH model has been implemented via
two BASIC language programs. The "dialect" of the
language used is BASIC-80, version 5.21, by Micro-
soft (CP/M version). These programs are designed to
be used interactively on a terminal or a hard-copy
printer. The first program is the input parameter
program which accepts the input parameters and
formats them into a BASIC sequential file. The sec-
ond program is the ECOPATH model itself.
Literature Cited
Allen, K. R.
1971. Relation between production and biomass. J. Fish.
Res. Board Can. 28:1573-1581.
Anojersen, K. p., and E. Ursin.
1977. A multispecies extension to the Beverton and Holt
theory of fishing, with accounts of phosphorus circulation and
primary production. Medd. Dan. Fisk. Havunders., New
Sen, 7:319-435.
Grigg, R. W., J. J. Polovina, and M. J. Atkinson.
1984. Model of a coral reef ecosystem: Part III Resource
Limitation, Community Regulation, Fishery Yield, and
Resource Management. Coral Reefs 3:23-27.
Laevastu T., and H. a. Larkins.
1981. Marine fisheries ecosystem: its quantitative evaluation
and management. Fishing News Books, Farnham, Surrey,
Engl., 162 p.
Macdonald, J. S., and R. H. Green.
1983. Redundancy of variables used to describe importance of
prey species in fish diets. Can. J. Fish. Aquat. Sci. 40:635-
637.
Pauly, D.
1982. Notes on tropical multispecies fisheries, with a short
459
I
57
SEABIRDS
B = 15
P = 81
847
MONK SEALS
SMALL PELAGIC S
B = 1,836
P = 2,020
i
150
SHARKS, JACKS, SCOMBRIDS
B = 536 P = 192
LOBSTERS AND CRABS
B = 1,348
P = 701
B = 13,966
P = 20,949
ZOOPLANKTON
B = 899
P = 3.6 X 10*
t
)
*
2.3X10'
PHYTOPLANKTON
B = 3.3 X 10^
P = 2.3 X 105
BOTTOM FISHES
B = 94
P = 30
GREEN TDRTLES
B = 15
P = 2
4.3 X 10*
HETEROTROPHIC BENTHOS
B = 1.7 X 10^
P = 5.1 X 10^
OS y
g
X
to
2.4X10®
BENTHIC ALGAE
B = 2.0 X 10^
P = 2.5 X 10^
47
Figure l.-Biomass budget schematic for major prey-predator pathways. Annual production denoted as P and mean annual biomass as B
with values in units of (kg/km)'^ based on a habitat area of 1 ,200 km^. The values associated with the arrows represent the pro(iucti()n from the
lower trophic level consumed by the higher trophic level (Polovina in press).
bibliography of the food and feeding habits of tropical fish.
In Report on the regional training course on fishery stock
assessment, 1 September-9 October 1981, Samutprakarn,
Thailand, p. 30-35 and 92-98. Tech. Rep. 1, Part II, SCS/
GEN/82/41, Manila.
Polovina, J. J.
1984. Model of a coral reef ecosystem, Part I: ECOPATH and
its application to French Frigate Shoals. Coral Reefs 3:1-11.
Walsh, J. J.
1981. A carbon budget for overfishing off Peru. Nature 290:
300-304.
Jeffrey J. Polovina
Mark D. Ow
Southwest Fisheries Center Honolulu Laboratory
National Marine Fisheries Service, NOAA
P.O. Box 3830
Honolulu., HI 96812
460
FOOD AND FEEDING OF
THE TOMTATE, HAEMULON AUROUNEATUM
(PISCES, HAEMULIDAE), IN
THE SOUTH ATLANTIC BIGHT'
The tomtate, Haemulon aurolineatum, is an abun-
dant demersal fish in a variety of marine habitats in
the South Atlantic Bight, the Gulf of Mexico, and the
Caribbean Sea (Darcy 1983). They are a reef-associ-
ated species (Parrish and Zimmerman 1977), and in
the South Atlantic Bight they are most commonly
found over hard or "live" bottom reefs in depths
< 55 m (Struhsaker 1969; Manooch and Barans
1982; Sedberry and Van Dolah 1984). While occa-
sionally taken in trawl catches over open, sandy
habitats on the southeastern continental shelf (Wen-
ner et al. 1980), they are much more abundant in
trawls directed at sampling hard bottom, and
generally rank in the top three demersal species by
number or weight in trawl catches (Wenner 1983;
Sedberry and Van Dolah 1984; Sedberry unpubl.
data). Although they are frequently caught on hard
bottom reefs in the South Atlantic Bight, the depen-
dance of these fishes on hard bottom habitat for food
is unknown. Previous investigations in the Carib-
bean have indicated that tomtate are not obligatory
reef dwellers and that they forage extensively in
open sandy areas (see Darcy 1983 for review).
Because of the importance of this species in the hard
bottom ichthyofauna of the South Atlantic Bight and
its importance to fisheries associated with hard bot-
tom reefs, a knowledge of its food habits is important
to our understanding the ecology of this habitat.
Tomtate may be important in transferring energy
from the expansive sand areas of the shelf onto the
much more restricted hard bottom habitat, and their
feeding behavior in the South Atlantic Bight may be
important in maintaining the higher biological pro-
ductivity of hard bottom areas, relative to the open
sandy shelf.
To determine foraging habitat of the tomtate, an
investigation on food habits was conducted. The pur-
pose of this note is to report the results of that study
and to relate the feeding behavior to existing
knowledge of the ecology of hard bottom areas in the
South Atlantic Bight.
Methods
Tomtate were collected during seasonal cruises in
1980 (two cruises- one in winter and one in summer)
and 1981 (four cruises- one each in winter, spring,
summer, and fall) by trawl from eight hard bottom
reef stations off South Carolina and Georgia. Sta-
tions were located in each of three depth zones
representing the inner shelf (16-22 m depth, three
stations), middle shelf (23-38 m, four stations), and
the outer shelf (47-67 m, one station). Detailed
descriptions of station locations and habitat can be
found in Sedberry and Van Dolah (1984) and Wen-
ner et al. (1984). Each station was mapped
using loran C and underwater television, and all sam-
pling was conducted in hard bottom areas mapped by
using this technique (Sedberry and Van Dolah 1984).
Tomtate were measured (standard length, SL) at
sea and their stomachs removed if not conspicuously
empty. Stomachs were individually labeled and pre-
served in 10% seawater-Formalin^.
Stomachs were washed in tap water and transfer-
red to 50% isopropanol in the laboratory, and con-
tents of individual stomachs were sorted by taxa and
counted. Colonial forms (e.g., hydroids, bryozoans)
and algae were counted as one organism. Volume
displacement of food items was measured using a
graduated cylinder, or estimated by using a 0.1 cm^
grid (Windell 1971).
Since the methods of food habits quantification are
variously biased (Hynes 1950; Pinkas et al. 1971;
Windell 1971), the relative contribution of different
food items to the total diet was determined using
three methods: 1) percent frequency occurrence (F),
2) percent numerical abundance (N), and 3) percent
volume displacement (V). These three values were
calculated for individual prey species, for prey
grouped by higher taxonomic categories, and for
higher taxonomic categories pooled for 100 mm
intervals of standard length. To determine the
dependance of tomtate on hard bottom prey
organisms, stomach samples were compared with
benthic samples using IvleVs index of electivity
(Ivlev 1961), calculated as follows:
E =
^1
A +^2
where P, is the percentage of the diet comprised by a
given prey taxon and P2 is the percentage of the food
complex in the environment (i.e., in benthic samples)
comprised by the same prey taxon. Electivity values
range from - 1 to -i- 1 . Negative values imply that
the prey species is avoided by the predator or that it
^Contribution No. 179, South Carolina Marine Resources
Research Institute, P.O. Box 12559, Charleston, SC 29412.
^Reference to trade names does not imply endorsement by the Na-
tional Marine Fisheries Service, NOAA.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
461
is unavailable to the predator. Positive values imply
that the predator prefers the prey species or that it is
feeding on prey species which occur in a different
habitat than those sampled by the benthic sampler. A
value near zero implies no selectivity by the
predator; i.e., the fish is feeding on the prey in pro-
portion to the prey's relative abundance.
Benthic samples and stomach collections were
pooled by depth zone (inner, middle, and outer shelf)
for comparison; however, too few tomtate for ade-
quate comparison were collected at outer shelf sta-
tions. Benthic samples were obtained with diver-
operated suction sampler at the seven inner and mid-
dle shelf, hard bottom sites during the same time
periods in 1980 and 1981 as the fish collections were
made. The suction sampler is very effective at sam-
pling macroinvertebrates on hard substrates (Chess
1979; Wenner et al. 1983). Five replicate benthic
samples were taken during the six cruises at each
reef that was sampled for fishes, and these samples
(30 for each reef) are believed to be adquate repre-
sentatives of the hard bottom invertebrate fauna in
Table 1.— Percent frequency occurrence (F), percent number (N), and percent volume (V) of food items in Haemulon aurolinea-
tum stomachs collected at tiard bottom areas in 1980 and 1981.
Taxon Food item
F
N
V
Taxon Food item
F
N
V
Algae
Polychaeta undetermined
5.3
0.4
3.1
Sargassum sp.
1.0
0.1
0.1
Progoniada regularis
1.0
0.1
<0.1
Cnidaria
Psalmmolyce ctenidophora
2.1
0.2
1.5
Hydrozoa
Sabellidae undetermined
1.0
0.1
0.2
Dynamena cornlcina
1.0
0.1
<0.1
Scoloplos rubra
1.0
0.1
0.2
LIctorella convallaria
1.0
0.1
<0.1
Sptiaerodoridae
Sertularia sp.
1.0
0.1
<0.1
undetermined
1.0
0.1
<0.1
Total Hydrozoa
3.2
0.2
<0.1
Syllidae undetermined
2.1
0.2
<0.1
Anthozoa
Syllis sp.
3.2
0.2
0.1
Actiniaria undetermined
5.3
0.4
0.6
Syllis regulata carolinae
1.0
0.1
<0.1
Platytielminthes
Terebellidae undetermined
2.1
0.2
2.0
Turbellaria undetermined
5.3
1.0
0.7
Travisia parva
1.1
0.2
0.1
Annelida
Total Polychaeta
46.3
8.7
14.6
Polyctiaeta
Mollusca
Ampharete sp.
1.0
0.1
<0.1
Gastropoda
Amphinomidae undetermined
1.0
0.1
<0.1
Caecum pulchellum
1.0
0.1
<0.1
Arabella iricolor
2.1
0.2
0.5
Diodora cayenensis
1.0
0.1
<0.1
Arabellidae undetermined
1.0
0.1
0.1
Gastropoda undetermined
1.0
0.1
0.4
Armandia maculata
6.3
2.4
0.3
Naticidae undetermined
1.0
0.1
<0.1
Capitellidae undetermined
5.3
0.4
0.4
Total Gastropoda
3.2
0.3
0.5
Ceratonereis mirabilis
1.0
0.1
<0.1
Pelecypoda
Chloeia sp.
1.0
0.1
0.2
Ervilia concentrica
5.3
38.2
6.3
Chloela vlridis
1.0
0.1
0.4
Mactra fragilis
1.0
0.1
0.2
Chone americana
2.1
0.2
<0.1
Pelecypoda larvae
1.0
0.1
"^O.l
Diopatra cuprea
1.0
0.1
<0.1
Total Pelecypoda
7.4
38.3
6.5
Drilonereis sp.
2.1
0.2
0.1
Cephalopoda
Eunice vittata
1.0
0.1
<0.1
Octopus sp.
1.0
0.1
0.9
Eunice websteri
1.0
0.1
<0.1
Pycnogonida
Eunicidae undetermined
1.0
0.1
<0.1
Anoplodactytus insigniformis
1.0
0.1
<0.1
Exogone dispar
2.1
0.2
<0.1
Crustacea
Glycera sp.
5.3
0.4
1.2
Copepoda
Glycera americana
3.2
0.2
0.8
Catanopia americana
5.3
13.0
0.3
Glycera tesselata
2.1
0.2
0.3
Longipedia helgolandica
2.1
0.6
<0.1
Goniadides carolinae
1.0
0.1
<0.1
Microsetella norvegica
1.0
0.2
<0.1
Harmothoe sp.
2.1
0.2
<0.1
Saphirella tropica
1.0
0.1
<0.1
Lumbrinerides acuta
1.0
0.1
<0.1
Temora stytifera
3.2
0.4
<0.1
Lumbrineris coccinea
2.1
0.2
0.9
Temora turbinata
6.3
1.2
<0.1
Lumbrineris sp.
1.0
0.1
0.9
Undinula vulgaris
1.0
0.1
<0.1
Malanidae undetermined
3.2
0.5
0.2
Total Copepoda
13.7
15.4
0.4
Nephtyidae undetermined
1.0
0.1
<0.1
Stomatopoda
Nephtys incisa
1.0
0.1
<0.1
Gonodactylus bredini
2.1
0.2
1.4
Notomastus americanus
1.0
0.1
<0.1
Lysiosquilla scabricauda
1.0
0.1
1.7
Notopygos crinita
1.0
0.1
0.1
Stomatopoda larvae
3.2
0.3
0.3
Onuphis sp.
1.0
0.1
<0.1
Stomatopoda undetermined
4.2
0.3
0.4
Onuphis eremita
1.0
0.1
<0.1
Total Stomatopoda
10.5
0.8
3.8
Onuphis nebulosa
1.0
0.1
0.4
Mysidacea
Opfieliidae undetermined
1.0
0.1
<0.1
Bowmaniella portoricensis
3.2
0.2
0.1
Phyllodoce castanea
1.0
0.1
<0.1
Cumacea
Phyllodoce groenlandica
1.0
0.1
0.1
Cumacea B
1.0
0.1
<0.1
Phyllodoce longipes
1.0
0.2
<0.1
Oxyurostylis smithi
3.2
0.2
<0.1
Phyllodoce sp.
1.0
0.1
<0.1
Total Cumacea
4.2
0.3
<0.1
Phyllodocidae undetermined
1.0
0.1
<0.1
462
each depth zone (Wenner et al. 1983, 1984). Details
of benthic sampling and structure of the invertebrate
communities are described elsewhere (Wenner et al.
1983, 1984). The electivity index was calculated for
each species that were numerically dominant in fish
stomachs or in benthic samples collected within the
two depth zones (inner and middle shelf).
Results and Discussion
Haemulon aurolineatum had a generalized diet
and fed on about 120 species of prey (Table 1).
Polychaetes and amphipods were the most important
food and were eaten with almost the same fre-
quency. Polychaetes, however, made up a large
volume of prey because of their large size. Decapods
were also frequently consumed, but made up a small
percentage of the volume or number of prey items.
Pelecypods were the most abundant prey and cepha-
lochordates, while infrequently consumed, made up a
large portion of food volume because of their large
size. Fishes also made up a large portion of food
volume and copepods, though small in volume dis-
placement, were often eaten in large numbers.
Table 1.— Continued.
Taxon Food item
F
N
V
Taxon Food item
F
N
V
Tanaidacea
Decapoda larvae
1.0
0.1
<0.1
Apseudes sp. B
1.0
0.7
<0.1
Leptochela sp.
1.0
0.1
0.4
Isopoda
Leptochela papulata
7.4
0.7
1.7
Carpias bermudensis
1.0
0.1
<0.1
Lucifer faxoni
3.2
0.4
<0.1
Erichsonella flliformis
1.0
0.1
<0.1
Lysmata sp.
1.0
0.2
<0.1
Eurydice littoralis
3.2
0.2
0.1
Natantia undetermined
4.2
0.4
0.6
Paracerceis caudata
1.0
0.1
<0.1
Neopontonldes beaufortensis
1.0
0.1
<0.1
Total Isopoda
6.3
0.4
0.1
Paguridae
1.0
0.1
<0.1
Amphiipoda
Periclimenaeus schmitti
1.0
0.1
<0.1
Acanttionotozomatidae
1.0
0.1
<0.1
Periclimenes sp.
1.0
0.1
0.1
Ampelisca sp.
1.0
0.1
<0.1
Perlcllmenes longicaudatus
2.1
0.2
0.1
Ampelisca cristoldes
1.0
0.1
0.1
Processa sp.
4.2
0.3
0.9
Ampelisca schellenbergi
3.2
0.3
0.1
Processa hemphilli
1.0
0.1
0.2
Ampelisca vadorum
1.0
0.1
0.1
Synalpheus minus
1.0
0.1
0.1
Amphipoda E
3.1
0.2
<0.1
Synalpheus townsendi
1.0
0.1
<0.1
Amphipoda G
1.0
0.2
<0.1
Thor sp.
1.0
0.1
0.2
Amphipoda undetermined
2.1
0.2
0.1
Thor floridanus
1.0
0.1
<0.1
Caprella equlllbra
13.7
1.7
0.2
Trachypenaeus constrictus
2.1
0.2
0.1
Caprella penantis
3.2
0.4
0.1
Xanthidae
1.0
0.1
0.2
Cerapus tubularis
1.0
0.1
<0.1
Total Decapoda
33.7
4.9
6.2
Elasmopus sp. A
2.1
0.4
<0.1
Sipunculida
Elasmopus sp.
1.0
0.1
<0.1
Sipunculida D
1.0
0.1
<0.1
Erichthonlus brasillensis
12.6
2.1
0.2
Bryozoa
Gammaropsls sp.
2.1
0.4
<0.1
Amathia distans
1.0
0.1
<0.1
Lembos unicornis
1.0
0.1
<0.1
Crisia sp.
1.0
0.1
<0.1
Leucothoe splnlcarpa
1.0
0.1
<0.1
Diaperoecia floridana
2.1
0.2
<0.1
Liljeborgia sp. A
2.1
0.2
<0.1
Discoporella umbellata
1.0
0.1
<0.1
Luconacia incerta
2.1
1.5
0.1
Total Bryozoa
5.3
0.4
0.1
Lysianopsis alba
4.2
0.7
0.1
Echinodermata
Melita appendiculata
2.1
1.0
0.1
Echinoidea
Metharpinla floridana
1.0
0.2
<0.1
Clypeasteroidea
Microjassa sp. A
1.0
0.2
<0.1
undetermined
1.0
0.7
<0.1
Monoculodes sp.
1.0
0.1
<0.1
Ophiuroidea
Photis sp.
3.1
0.4
<0.1
Hemiptiolis elongata
1.0
0.1
<0.1
Photis pugnator
1.0
0.2
<0.1
Ophiotfirix angulata
3.2
0.4
0.4
Phtlsica marina
2.1
0.3
<0.1
Ophiuroidea undetermined
17.9
1.5
1.5
Rhepoxynius epistomus
2.1
0.2
<0.1
Total Ophiuroidea
22.1
1.9
1.9
Rudilemboides naglei
6.3
0.7
<0.1
Chaetognatha
Stenopleustes sp. A
1.0
0.1
<0.1
Chaetognatha undetermined
1.0
0.1
<0.1
Stenothoe sp.
3.2
0.2
<0.1
Chordata
Stenothoe georgiana
5.3
0.8
<0.1
Cephalochordata
Synchelldium americanum
1.0
0.1
<0.1
Branchiostoma carlbaeum
4.2
12.4
41.6
Tiron tropakis
1.0
0.1
<0.1
Pisces
Total Amphipoda
47.4
12.8
1.3
Bothidae undetermined
1.0
0.1
0.2
Decapoda
Clupeidae undetermined
1.0
0.1
1.0
Albunea paretii zoea
1.0
0.1
<0.1
Hypleurochilus geminatus
1.0
0.1
0.4
Alpheus normani
1.0
0.1
<0.1
Teleostei larvae
1.0
0.1
<0.1
Brachyura megalopae
1.0
1.2
0.1
Teleostei undetermined
10.5
0.7
18.8
Brachyura undetermined
2.1
0.2
0.3
Total Pisces
14.7
1.0
20.5
Callianassa atlantica
1.0
0.1
0.9
Number of stomachs examined:
Examined stomachs with food:
154
95
463
Ophiuroids were frequently consumed but were
usually represented in stomachs by small arm
fragments.
Small (1-100 mm SL) tomtate had a diet domi-
nated numerically by very small crustaceans (cope-
pods) and volumetrically by fishes and decapods
(Table 2). Amphipods were most abundant prey tax-
on for 101-150 mm tomtate and polychaetes made up
the greatest volume of food. Large (151-200 mm SL)
tomtate primarily consumed pelecypods, which were
the most abundant taxon, and cephalochordates,
which were abundant in the diet and made up the
greatest prey volume.
Many hard bottom invertebrates that were abun-
dant in suction samples at inner and middle shelf
sites were not important in the diet of tomtate (Table
3). Of the eight dominant hard bottom invertebrate
species, only two (the polychaete Chone americana
and the corophoid amphipod Erichthonms brasili-
ensis) at inner shelf sites and one (the caprellid
amphipod Luconacia incerta) at middle shelf sites
made up a greater percentage of the diet than they
did of benthic samples. On the other hand, inverte-
brates that were common in stomachs were general-
ly not abundant in benthic samples and electivity
values were usually positive.
Tomtate are apparently not completely dependent
on hard bottom habitat for prey. Some of the most
abundant prey species are pelagic (e.g., brachyuran
megalopae, copepods). Most benthic prey are in-
faunal species that are restricted to soft sediments.
Amnandia maculata, a dominant prey species on the
inner shelf, is a deposit-feeding polychaete that bur-
rows in soft sediments (Fauchald and Jumars 1979).
Ervilia concentrica, an important prey species on
the middle shelf, was not collected at any of the 1 1
hard bottom stations. This bivalve is common in soft
sediments (Porter 1974). The cephalochordate 5rar^
chiostoma caribaeum, a common prey species on the
middle shelf that was very rare in benthic samples, is
also an infaunal sand bottom species (Hildebrand and
Schroeder 1928). Thus, a large portion of the prey of
Haemulon aurolineatum are not hard bottom epi-
faunal species, suggesting that tomtate are not
Table 2. — Percent frequency occurrence (F), percent number (N), and percent volume (V) of higher tax-
onomic groups of food in the diet of Haemulon aurolineatum, by length interval.
Length Intervals (mm SL)
Prey taxon
1-100
101-150
151-200
F
N
V
F
N
V
F
N
V
4.8
0.4
2.6
6.2
0.3
<0.1
8.3
1.1
3.0
6.3
0.3
0.4
12.5
4.0
6.3
4.2
0.7
0.1
19.0
1.5
11.4
62.5
15.6
35.9
50.0
9.4
13.5
8.3
1.1
4.7
2.1
0.2
<0.1
4.1
0.6
<0.1
12.5
2.1
57.2
0.1
8.0
1.1
4.2
0.6
0.1
47.6
77.1
14.4
4.2
0.6
<0.1
4.2
0.3
<0.1
19.0
1.9
14.7
12.5
1.7
2.2
6.2
6.2
0.3
0.3
4.0
0.1
4.8
0.4
0.2
4.2
0.6
<0.1
6.2
0.3
<0.1
12.5
1.7
0.1
6.2
0.3
0.2
33.3
6.0
7.3
79.2
58.3
7.7
39.6
5.9
0.5
19.0
9.8
20.8
33.3
5.6
11.3
39.6
3.2
5.6
4.8
0.4
0.7
8.3
1.1
0.4
6.2
2.1
0.3
0.1
<0.1
<0.1
14.3
1.1
1.7
25.0
5.0
8.0
22.9
1.4
1.0
4.8
0.4
0.4
4.2
0.6
24
6.2
18.4
51.1
4.3
1.1
28
21
71.5
49-99
26.0
16.7
2.2
44
24
138.2
101-150
17.8
12.5
0.7
79
48
168.3
151-198
14.1
Algae
Cnidaria
Hydrozoa
Anthozoa
Turbellaria
Annelida
[ylollusca
Gastropoda
Pelecypoda
Cephalopoda
Arthropoda
Pycnogonida
Copepoda
Stomatopoda
Mysidacea
Cumacea
Tanaidacea
Isopoda
Amphipoda
Decapoda
Sipunculida
Bryozoa
Echinodermata
Echinoidea
Ophiuroidea
Chaetognatha
Chordata
Cephalochordata
Pisces
Number of stomachs examined:
Examined stomachs with food:
Mean length of fish v*/ith food (mm SL):
Length extremes in interval (mm SL):
464
restricted to hard bottom habitat for food resources.
Although numerous in hard bottom areas (it ranked
third in total number and second in total weight in
trawl catches over all eight trawlable stations and six
sampling periods combined in 1980 and 1981), Hae-
mulon aurolineatum has been characterized as a
reef-related species; i.e., it uses the reef for only part
of each day (Parrish and Zimmerman 1977). Randall
(1967) found sand-dwelling organisms in 16 tomtate
stomachs he examined, but the habitat of the deca-
pods, the predominant prey, could not be inferred
from his results. Parrish and Zimmerman (1977)
noted a diet dominated by sand-flat invertebrates for
an unspecified number of tomtate collected in the
Caribbean. Parrish and Zimmerman (1977) reported
nocturnal foraging, with tomtate sheltering in the
reef during the day. During extensive (about 70
dives) daytime scuba observations by the author off
of South Carolina and Georgia, no tomtate that ex-
hibited foraging behavior was seen, and large schools
were often noted "stacked up" at the edge of rock
ledges protruding out into sand areas. Apparently,
nocturnal feeding behavior described for tomtate in
the Caribbean is also typical for the species in the
South Atlantic Bight. Tomtate forage, apparently at
night, on sand bottom areas of the shelf or in sand
patches often found adjacent to rock outcrops,
returning to the reefs for shelter during the day. This
behavior probably results in considerable energy
transfer, in the form of feces, from open sand bottom
areas of the shelf onto hard bottom reefs.
The fact that two hard bottom invertebrate species
(Erichthonitcs brasiliensis and Luconacia incerta)
were common in tomtate stomachs and that many
additional hard bottom species (e.g., hydroids, many
amphipods, alpheid decapods, and bryozoans) are oc-
casionally eaten indicates that tomtate also forage to
a limited extent on hard bottom.
The high diversity found in hard bottom inverte-
brate communities (Wenner et al. 1983) could be
attributed, in part, to predation by abundant and
diverse fish communities (Petersen 1979). However,
as noted by Wenner et al. (1983), available data in-
dicate that few dominant species of hard bottom
invertebrates are heavily preyed upon by fishes
(Sedberry and Nimmich^). Tomtate, an abundant
^Sedberry, G. R., and T. A. Nimmich. Food habits of some fishes
associated with live bottom habitat off the South Atlantic coast of
the U.S.A. Manuscr. in prep. South Carolina Marine Resources
Research Institute, P.O. Box 12559, Charleston, SC 29412.
Table 3. — Relative abundance (percent of total number of individuals) and electlvlty index values
(E) of dominant species in suction samples (Group A) and Haemulon aurolineatum stomachs
(Group B) by depth zone. Dominant species included those that ranked in the five most abundant
species within each Group (A or B) in either depth zone, for collections pooled for all years and
seasons.
Percent of total nun-
iber of in(
jividuals
Inner shelf
Middle shelf
Benthic
Fish
Benthic
Fish
samples
stomachs
£
samples
stomachs
E
Group A:
Chone amerlcana
0.33
0.36
0.04
0.81
0.09
-0.79
Erichthonius brasiliensis
2.89
9.32
0.53
0.30
0.19
-0.24
Exogone dispar
3.71
0.72
-0.68
0.47
- 1.00
Filograna implexa
20.42
-1.00
63.87
-1.00
Luconacia incerta
3.27
0.36
-0.80
1.03
1.77
0.26
Malacoceros glutaeus
0.41
-1.00
0.81
-1.00
Podocerus sp. A
2.87
-1.00
0.27
-1.00
Syllis spongicola
2.15
-1.00
1.90
-1.00
Total
36.05
10.76
69.46
2.05
Group B:
Armandia maculata
0.22
10.75
0.96
0.03
0.19
0.73
Brachyura megalopae
6.09
1.00
0.00
Branchiostoma caribaeum
0.00
0.01
15.69
0.99
Calanopia americana
0.36
1.00
16.34
1.00
Caprella equilibra
1.55
2.87
0.30
0.34
1.40
0.61
Erichtonius brasiliensis
2.89
9.32
0.53
0.30
0.19
-0.24
Ervilia concentrica
0.36
1.00
48.18
1.00
Luconacia incerta
3.27
0.36
-0.80
1.03
1.77
0.23
Melita appendiculata
0.43
4.66
0.83
0.27
-1.00
Temora turbinata
4.30
1.00
0.28
1.00
Total
8.36
39.07
1.98
84.04
Stomachs with food:
43
50
465
predator on hard bottom areas (Sedberry and Van
Dolah 1984), do not serve as "keystone" predators
(Paine 1969) which influence community structure of
invertebrates on South Atlantic Bight hard bottom
reefs.
Acknowledgments
I thank the many individuals of the South Carolina
Marine Resources Center who were involved in all
phases of the 3-yr BLM (contracts AA551-CT9-27
and AA551-CT1-18) and MMS (contract 14-12-0001-
29185) funded study of hard bottom habitat in the
South Atlantic Bight. I especially thank D. M. Knott,
R. F. Van Dolah, and E. L. Wenner for providing the
data on macrobenthos that was used in the electivity
analysis; C. B. O'Rourke and E. C. Roland (poly-
chaetes), H. Porter (bivalves), and E. L. Wenner
(decapods) for help in prey identification; C. A.
Barans, C. A. Wenner, and the anonymous re-
viewers for comments that improved the manu-
script; and N. M. Beaumont for processing the manu-
script.
Literature Cited
Chess, J. R.
1979. An airlift sampling device for in situ collecting of biota
from rock substrata. Mar. Technol. Soc. J. 12(3):20-23.
Darcy, G. H.
1983. Synopsis of biological data on the grunts Haemulon
aurolineatum and H. plumieri (Pisces: Haemulidae). U.S.
Dep. Commer., NOAA Tech. Rep. NMFS Circ. 448, 37 p.
Fauchald, K., and p. a. Jumars.
1 979. The diet of worms: a study of polychaete feeding guilds.
Oceanogr. Mar. Biol. Annu. Rev. 17:193-284.
HlLDEBRAND, S. P., AND W. C. SCHROEDER.
1928. Fishes of Chesapeake Bay. U.S. Bur. Fish., Bull. 48:
1-366.
Hynes, H. B. N.
1950. The food of fresh-water sticklebacks (Gasterosteus
aculeatus and Pygosteus pungitius), with a review of methods
used in studies of the food of fishes. J. Anim. Ecol. 19:36-58.
IVLEV, V. S.
1961. Experimental ecology of the feeding of fishes. Yale
Univ. Press, New Haven, Conn., 302 p.
Manooch, C. S., Ill, AND C. A. Barans.
1982. Distribution, abundance, and age and growth of the
tomtate, Haemulon aurolineatum, along the southeastern
United States. Fish. Bull., U.S. 80:1-19.
Paine, R. T.
1969. The Pisaster-Tegula interaction: prey patches, predator
food preference, and intertidal community structure. Ecol-
ogy 50:950-961.
Parrish, J. D., and R. J. Zimmerman.
1977. Utilization by fish of space and food resources on an off-
shore Puerto Rican coral reef and its surroundings. In R. L.
Taylor (editor). Proceedings: Third International Coral Reef
Symposium, Vol. I: Biology, p. 297-303. Univ. Miami.
Peterson, C. H.
1979. The importance of predation and competition in orga-
nizing the intertidal epifaunal communities of Barnegat Inlet,
New Jersey. Oecologia 39:1-24.
PiNKAS, L., M. S. Oliphant, and I. L. K. Iverson.
1971. Food habits of albacore, bluefin tuna, and bonito in
California waters. Calif. Dep. Fish Game, Fish Bull. 152:1-
105.
Porter, H. J.
1974. The North Carolina marine and esturine mollusca-an
atlas of occurrence. Inst. Mar. Sci., Univ. North Carolina,
N.C., 351 p.
Randall, J. E.
1967. Food habits of reef fishes of the West Indies. Stud.
Trop. Oceanogr. (Miami) 5:665-847.
Sedberry, G. R., and R. F. Van Dolah.
1984. Demersal fish assemblages associated with hard
bottom habitat in the South Atlantic Bight of the U.S.A.
Environ. Biol. Fishes 11:241-258.
Struhsaker, p.
1969. Demersal fish resources: composition, distribution, and
commercial potential of the continental shelf stocks off south-
eastern United States. U.S. Fish Wildl. Serv., Fish. Ind.
Res. 4:261-300.
Wenner, C. A.
1983. Species associations and day-night variability of trawl-
caught fishes from the inshore sponge-coral habitat, South
Atlantic Bight. Fish. Bull., U.S. 81:537-552.
Wenner, C. A., C. A. Barans, B. W. Stender, and F. W. Berry.
1980. Results of MARMAP otter trawl investigations in the
South Atlantic Bight V. Summer, 1975. S.C. Mar. Resour.
Cent, Tech. Rep. 45, 57 p.
Wenner, E. L., P. Hinde, D. M. Knott, and R. F. Van Dolah.
1984. A temporal and spatial study of invertebrate commu-
nities associated with hard-bottom habitats in the South
Atlantic Bight. U.S. Dep. Commer., NOAA Tech. Rep.
NMFS 18, 104 p.
Wenner, E. L., D. M. Knott, R. F. Van Dolah, and V. G.
BuRRELL, Jr.
1983. Invertebrate communities associated with hard bottom
habitats in the South Atlantic Bight. Estuarine Coastal
Shelf Sci. 17:143-158.
Windell, J. T.
1971. Food analysis and rate of digestion. In W. E. Ricker
(editor), Methods for assessment of fish production in fresh
waters, p. 215-226. IBP (Int. Biol. Programme) Handb. 3,
2ded.
George R. Sedberry
South Carolina Marine Resources Research Institute
P.O. Box 12559
Charlestm, SC 29^12
466
SEMILUNAR REPRODUCTIVE CYCLES IN
FUNDULVS HETEROCLITUS (PISCES:
CYPRINODONTIDAE) IN AN AREA
WITHOUT LUNAR TIDAL CYCLES
Although lunar spawning rhythms are relatively
common in species of shallow-water fish, semilunar
reproductive cycles have been reported in a small but
growing number of species (Korringa 1947;
Johannes 1978). Species with the best documented
semilunar gonad and spawning cycles include the
California grunion, Leuresthes tenuis, (Clark 1925);
Atlantic silversides, Menidia menidia, (Middaugh
1981); the tropical coral reef saddleback wrasse,
Thallassoma duperrey, (Ross 1983); two tropical
damselfishes, Pom,acentrus flairicauda and P. wardi,
(Doherty 1983), and gulf killifish, Funduhus grandis,
(Greeley and MacGregor 1983); and the salt marsh
mummichog, Fundulus heteroclitus, (Taylor et al.
1979; Taylor and DiMichele 1980). On the east coast
of North America, F. heteroditics move up onto
marsh surfaces during high spring tides to spawn
either in empty mussel (Geukensia demissa) shells or
in the outer leaves of salt marsh plants (Spartina
altemiflora) where oxygen levels are relatively high
and sedimentation rates are relatively low (Able and
Castagna 1975; Taylor et al. 1977; Kneib and Stiven
1978; Taylor and DiMichele 1983). Its eggs are ex-
tremely tolerant of desiccation and hatch on the next
series of high spring tides. In addition, semilunar
rhythms of larval hatching are well known for inter-
tidal chironomid insects (Newmann 1978) and for
several species of intertidal and estuarine crabs (see
Christy 1982; Forward et al. 1982).
In most cases, the proximal factors (sensu Giese
and Pearse 1974) responsible for initiating and syn-
chronizing these semilunar cycles are unknown.
However, among the factors postulated as cues are
tidal rhythms in water turbulence and hydrostatic
pressures (Korringa 1947; Newmann 1978; Weld
and Meier 1982; Ross 1983); tidal regimes in the
habitat (Forward et al. 1982); photoperiod in combi-
nation with tidal fluctuations in water temperature
(Miller et al. 1981), in combination with time of high
tide (Middaugh 1981; Middaugh and Takita 1983), or
in combination with interrupted current velocity
(Middaugh and Hemmer 1984); and moonlight
(Saigusa 1980). In addition to its wide distribution in
coastal marshes with distinct lunar cycles of spring
and neap tides, F. heteroclitus is abundant in exten-
sive shoreline habitats and marshes of Chesapeake
Bay, where tidal ranges are small and changes in
water level caused by barometric pressure and wind
frequently and unpredictably override lunar tidal
levels and obliterate semilunar tidal cycles. In the
present study, we measured the reproductive activi-
ty of F. heteroclitus in an area without lunar tidal
cycles in order to determine if semilunar reproduc-
tive rhythms occur. The occurrence of semilunar
reproductive rhythms would suggest that the prox-
imal cues regulating the reproductive cycles are not
factors associated with changes in tidal levels, such
as pressure, or turbulence of currents.
Methods
This study was conducted from May through
August 1982 at a small tidal creek (Muddy Creek)
which flows into the Rhode River (lat. 38°5rN, long.
76°32'W), a subestuary on the western shore of cen-
tral Chesapeake Bay, located about 11.3 km south of
Annapolis, MD. The creek bottom consists of fine
clays and silts, and its banks are fringed by a cattail
{Typha angvstifolia) marsh. Water level was
measured with a Honeywell^ diffused silicon differ-
ential pressure transmitter (accurate to ± 1.238 cm)
at a station operated by the U.S. Geological Survey
on the Rhode River near the mouth of Muddy Creek
about 1,000 m from the site where fish were sam-
pled. Changes in water level at the monitoring sta-
tion accurately reflect water levels at the sampling
site (D. L. Correll^ and R. L. Cory^). Measured daily
high water levels were compared with predicted high
tidal levels published for the Rhode River (National
Oceanic and Atmospheric Administration 1981).
Fundulus heteroclitus is the most abundant fish in
the creek (Mines unpubl. data). Fish were sampled
every 2-3 d during the hours of 0730-1230, using un-
baited minnow traps set just above low water level.
Each sample consisted of 8-12 males and 8-12
females which were tested for readiness to spawn,
and another 8-12 of each sex were taken to deter-
mine gonad indices. Readiness to spawn was deter-
mined in the field by applying gentle pressure from
anterior to posterior along the ventral surface of the
fish. Release of sperm or eggs was interpreted as the
fish being ripe. The gonad index for each fish in the
sample was determined by dissecting out the testes
or ovaries and by drying the gonad and body to con-
stant weight at 60°C and weighing them to the near-
'Reference to trade names does not imply endorsement by the Na-
tional Marine Fisheries Service, NOAA.
^D. L. Correll, Assistant Director, Smithsonian Environmental
Research Center, P.O. Box 28, Edgewater, MD 21037, pers. com-
mun. September 1982.
3R. L. Cory, Oceanographer, U.S. Geological Survey, Smithsonian
Environmental Research Center, P.O. Box 28, Edgewater, MD
21037, pers. commun. September 1982.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
467
est 1 X 10"'' g. The gonad index equals the (gonad
weighty body weight) x 100.
Results
Although tides in the Rhode River subestuary ex-
hibited an approximately semidiurnal rhythm, fluc-
tuations in measured high tide level were not corre-
lated with predicted high tide level (product moment
correlation of log transformed data for daily predict-
ed and measured high tide, r = 0.111; Student's
^test for r i^ 0, P > 0.2; Fig. 1). Moreover, time
series spectral analysis (Thrall and Engelman 1981)
showed that measured tides exhibited only a very
weak peak in spectral density at a frequency of about
12.5 d rather than the strong peak of 7.5 d exhibited
by predicted tidal cycles. Cross correlation between
predicted and measured tides in bivariate spectral
analysis showed low and variable coherence {P >
0.05). Similarly, linear association of the two vari-
ables was weak, with variable phase shifts and vari-
able coefficients necessary to fit one variable to the
other. In addition, the occurrence of tides sufficiently
high to flood the marsh fringing the creek (i.e., tides
> 46 cm) did not occur more frequently at night than
during day (x^ test, P > 0.2), nor more frequently
during any particular lunar phase (x^ test, P > 0.4).
High tides did not occur consistently during any 2-h
period of the 24-h day at the quarters of the new or
full moons (x^ test, P > 0.4). Thus, water levels in the
estuary were neither predictable in amplitude within
the tidal range nor related in any obvious cyclical
pattern to the lunar cycle.
However, both female and male F. heteroclitus
showed distinct semimonthly cycles in readiness to
spawn from May through August (Fig. 1). Females
and males also exhibited a distinct semimonthly cycle
of gonad size, although the cycle of male gonad index
was not as pronounced as that of females, due to the
small changes in size of the testes during spawning
(Fig. 1). The cycles of spawning readiness in males
and females were usually in phase with the lunar
cycle. Comparisons of the observed frequencies of
spawning readiness with frequencies predicted by
cycles with perfect semilunar periods and the same
amplitudes showed no significant differences in 27 of
37 d of observation for females and 33 of 37 d of
observation for males (x^ test, P < 0.05). Observed
frequencies of spawning readiness over the entire
study period were not significantly different from
frequencies predicted by the perfect semilunar cycles
for either females or males (x^ test, P > 0.2).
Although six out of six peaks of spawning readiness
for males occurred during the 7 d surrounding new
or full moons, for females only four of the six peaks
occurred during the first or last quarters of the
moon, indicating that for the small numbers of peaks
occurring during a reproductive season, readiness to
spawn does not coincide with new and full moons
(Fisher's Exact Test for number of spawning peaks
occurring within the specified period, P = 0.227;
Fig. 1). However, if the timing of the peaks in readi-
ness to spawn is considered to lag 3.5 d after the new
and full moons, then all peaks for males and females
occurred within the 7 d surrounding the lagged
period, indicating a significant synchronous semi-
lunar cycle (Fisher's Exact Test on number of peaks
occurring within the specified period, P < 0.01).
Female spawning was correlated with male spawn-
ing (product moment correlation of arcsine trans-
formed spawning frequencies, r = 0.695; Student's
^test for r ¥= 0, P < 0.001). However, neither female
nor male readiness to spawn was correlated with the
measured tides (product moment correlation of arc-
sine transformed frequencies of spawning readiness
with log transformed high tide measurements, r =
0.184 for females and r = 0.272 for males; Student's
^tests for r # 0, P > 0.2). Thus the semilunar cycles
of spawning readiness of both sexes appeared to be
synchronized, but not to be related to the tidal
regime of the estuary.
The reproductive season of F. heteroclitus in the
Rhode River-Muddy Creek estuarine system oc-
curred from late April to September, when water
temperatures were above 17° C (pers. obs.). Mean
gonad indices of female and male samples declined
during the season, both at the peak and at the spent
phases of the semimonthly cycles (Female Gonad In-
dex = -0.124 Day + 14.1 and Male Gonad Index =
- 0.035 Day + 3.83; Student's ^test for slopes ¥=0,P
< 0.05; (Fig. 1)). The decline of mean gonad index
during the season reflected two statistics. First, an
increasing percentage of the population failed to in-
itiate gonad recrudescence during successive cycles.
Figure 1.- Lunar phase, tidal levels, and reproductive cycles of
Fundulus heteroclitus from May to August 1982 in a tidal creek on
central Chesapeake Bay. Full moons (open circles) and new moons
(solid circles) are indicated. Daily high water levels above mean low
water are shown for measurements at the study site and for tidal
levels predicted by National Oceanographic and Atmospheric Ad-
ministration (1981). Horizontal lines indicate water level which
floods the marsh adjacent to the Creek. The percentages of female
and male fish which were ready to spawn are shown for each sample
throughout the spawning season (solid lines), along with
hypothetical spawning cycles with the same amplitudes and perfect
semilunar periods in phase with the new and full moons (dashed
lines). Gonad indices (mean ± SE) for females and males are also
plotted for each sample.
468
MOON O
O
O
O
60-1 predicted ^^^ ^.v^
H- ^ 90H measured
UJ
O LU 60-
•V.
9
d
9
cP°
«te
<h° o
99 III re 0 (na 89 m
°- <f-D ^°o o ° »*»;
o 9
O o
o o°°° o ° °
rrs^
100-1
o
MAY
JUNE
JULY
469
None of the female fish sampled on the May spawn-
ing peaks had undeveloped gonads (individual gonad
indices were all > 10%), whereas many had
undeveloped gonads on the July peaks (38% of the
sample for gonad weights had individual indices
< 5%, and 25% of the sample tested for spawning
were not ripe). Second, gonad size of fish with de-
veloped gonads declined during the season. Mean
gonad indices of females with developed ovaries of
the May peaks were significantly greater than those
of the July peaks (15% versus 9%, respectively)
(Student-Newman-Keuls test of arcsine transformed
data, P < 0.05).
Discussion
In Fundulus heteroclitus and F. conjluentus,
regulation of the annual reproductive cycle is ap-
parently dependent on changing combinations of
photoperiod and temperature (Harrington 1959; Day
and Taylor 1982). The decline in gonad index during
the season in the present study is consistent with a
similar decline observed by Kneib and Stiven (1978)
and Taylor et al. (1979) and suggests that, along with
physical factors, energy availability may be limiting
reproductive output late in the season. Weisberg
(1981) found that supplemental food increased the
gonad indices of F. heteroclitus in Delaware salt
marshes. Histological evidence shows that primary
oocytes in F. heteroclitus can undergo complete
development in one biweekly spawning cycle (Taylor
and DiMichele 1980), so lag time for recrudescence
of spent gonads does not account for reduced repro-
ductive activity late in the season. Funduhis grandis
reproduces throughout the summer in some areas of
the gulf coast (Greeley and MacGregor 1983), but
shows bimodal reproductive activity in spring and
fall with no reproduction in midsummer in shallow
ponds (Waas and Strawn 1983).
In addition to F. heteroclitus (Taylor et al. 1979;
Taylor and DiMichele 1980), semilunar spawning
cycles occur in some populations of F. grandis
(Greeley and MacGregor 1983), F. similis (Greeley
1982), F. majalis (Tedesco et al."), and probably inF.
notatus (inferred from observations of spawning
behavior in Carranza and Winn 1954). Waas and
Strawn (1983) measured a weak lunar, but not a
semilunar cycle in populations of F. grandis in two
nontidal ponds and a tidal creek with lunar tides fre-
quently overridden by wind effects. The semilunar
^Tedesco, M., A. H. Hines, and L. A. Wiechert. 1983. Semi-
lunar gonadal cycles mFunduliis maja/i-s (Pisces: Cyprinodontidae).
Technical Report of Smithsonian Environmental Research Center,
P.O. Box 28, Edgewater, MD 21037.
spawning cycle in F. grandis has been induced in the
laboratory during their reproductive season by inter-
action of photoperiod and tidal changes in water
temperature shifting on a lunar cycle (Miller et al.
1981). Daily disturbances (netting) of F. grandis also
apparently induces circadian gonadal responses
(Weld and Meier 1982). Tidal rhythms in water tur-
bulence and hydrostatic pressure have been postu-
lated for lunar and semilunar reproductive rhythms
in fish (Korringa 1947; Ross 1983) and for semilunar
hatching in intertidal chironomid insects (Newmann
1978). Middaugh (1981) suggested that the biweekly
coincidence of a high tide at the time of sunrise
and/or a lunar cue may serve as a synchronizer for
spawning of Menidia menidia in a South Carolina
estuary. In contrast to M. menidia, which showed a
precise reproductive response to diurnal tidal and
lighting schedules (Middaugh and Takita 1983), M.
peninsulae exhibited a variable and labile response in
which a combination of semidiurnal interruptions of
current and diel light cues was optimal at inducing
spawning synchrony (Middaugh and Hemmer 1984).
However, this synchrony in Menidia spp. had a diel
period, and the laboratory experiments were not run
long enough to test for lunar rhythms. Semilunar
rhythms of larval hatching are well documented for
several species of intertidal and estuarine crabs (see
Christy 1982; Forward et al. 1982). Hatching in the
mud crab, Rhithropanopeus harrisii, followed a
semilunar and diurnal rhythm in populations from an
estuary with semidiurnal and lunar tidal cycles,
whereas hatching was not associated with lunar
rhythms or tidal levels in an estuary with aperiodic
tides (Forward et al. 1982). Moveover, Forward et
al. (1982) induced circatidal rhythms in larval release
in crabs from an estuary with irregular tides by
transplanting them to an estuary with semidiurnal
and lunar tides. However, Saigusa (1980) showed
that the larval hatching cycle of a semiterrestrial
crab Sesarma haematocheir is entrained directly by a
moonlight cycle.
In the present study, in an area without a lunar
periodicity in the tidal cycle, F. heteroclitus had a
semilunar reproductive cycle which lagged the new
and full moons by 3.5 d. Although the study area had
tidal fluctuations with an approximately semidiurnal
period, the diel timing of high tides with respect to
photoperiod also did not appear to cue the semilunar
reproductive cycle. Changes in currents associated
with the diurnal tidal cycle may serve as a synchro-
nizing cue for the time of day of spawning, as it does
for Menidia menidia and M. peninsulae. However,
while identity of the cue remains unknown, the pres-
ent study indicates that tidally mediated factors such
470
as turbulence, hydrostatic pressure, temperature,
and salinity are not responsible for synchronizing the
semilunar rhythm.
Hypotheses concerning the ecological consequen-
ces and adaptive significance of semilunar cycles of
larval release in Uca spp. and other estuarine crabs
have been discussed recently by Christy (1982). His
analysis indicates that convergence among estuarine
crab species in the semilunar timing of larval release
results in rapid seaward transport of larvae, which
minimizes the effects of lethal combinations of high
temperature and low salinities or intense predation
in the upper estuary. However, Rhithropanopeus
harrisii completes its larval development within the
upper reaches of estuaries and shows a variable cycle
of hatching, depending on tidal predictability, which
may be advantageous for retention of larvae within
the estuary (Forward et al. 1982). Lunar spawning
cycles of insular coral reef fish may have evolved to
solve similar problems of larval dispersal away from
predators while assuring return of the recruits to the
adult habitat (Johannes 1978; Ross 1983). Semilunar
spawning cycles of Fundulus heteroditus, Menidia
menidia, Leuresthes tenuis, and other fish which
spawn in the upper intertidal zone (Taylor and
DiMichele 1983; Middaugh 1981; Clark 1925) may
have the adaptive advantage of removing spawning
adults and eggs from subtidal predators. Although
the eggs of F. heteroditus are tolerant of desiccation
(Able and Castagna 1975; Taylor et al. 1977), the
major advantage of the spawning site appears to be
higher oxygen levels and reduced sedimentation
than in the creek (Taylor and DiMichele 1983). How-
ever, spawned eggs of F. heteroditus and M.
menidia are usually found in areas inundated daily
by high tides (Middaugh 1981). In the present study,
62% of the days had tides which flooded the marsh
(Fig. 1), where eggs are probably deposited in the
bases of leaves of Typha angustifolia plants (see
Taylor and DiMichele 1983). Although there may be
additional advantages in areas with predictable tidal
fluctuations with lunar periodicity, the major advan-
tage of semilunar spawning rhythms in F. heterodi-
tus appears to be improved fertilization success af-
forded by synchronized spawning.
Acknowledgments
We are grateful for the assistance of L. Wiechert,
S. Hodgkins, C. Trowbridge, and K. Comtois. R.
Cory and P. Dresler of the U.S. Geological Survey
provided the data for measured tidal levels. R. Ross
and M. Taylor provided helpful discussion. D. Cor-
rell, T. Jordan, and two anonymous reviewers pro-
vided suggestions for improvements in earlier drafts
of the manuscript. This work was supported in part
by the Smithsonian Work/Learn Internship Pro-
gram, Maryland Department of Natural Resources,
and the Smithsonian Environmental Sciences Pro-
gram.
Literature Cited
Able, K. W., and M. Castagna.
1975. Aspects of an undescribed reproductive behavior in
Fundul^(s heteroditus (Pisces: Cyprinodontidae) from Vir-
ginia. Chesapeake Sci. 16:282-284.
Carranza, J., AND H. E. Winn.
1954. Reproductive behavior of the biaclcstripe topminnow,
Fundulus notatus. Copeia 1954:273-278.
Christy, J. H.
1982. Adaptive significance of semilunar cycles in larval
release in fiddler crabs (Genus Uca): Test of an hypothesis.
Biol. Bull. (Woods Hole) 163:251-263.
Clark, F. N.
1925. The life history of Leuresthes tenuis, an atherine fish
with tide controlled spawning habits. Calif. Dep. Fish Game,
Fish Bull. 10, 51 p.
Day, J. R., and M. H. Taylor.
1982. Effects of temperature and photoperiod on the seasonal
reproductive cycle of Fundulus heteroditus L. [Abstr.]
Am. Zool. 22:866.
DOHERTY, p. J.
1983. Diel, lunar and seasonal rhythms in the reproduction of
two tropical damselfishes: Pomacentrus flavicauda and P.
wardi. Mar. Biol. (Berl.) 75:215-224.
Forward, R. B., Jr., K. Lohmann, and T. W. Cronin.
1982. Rhythms in larval release by an estuarine crab Rhithro-
panopeus harrisii. Biol. Bull. (Woods Hole) 163:287-300.
GiESE, A. C, and J. S. Pearse.
1974. Introduction: general principals. In A. C. Giese and
J. S. Pearse (editors). Reproduction of marine invertebrates,
Vol. 1, p. 1-49. Acad. Press, N.Y.
Greeley, M. S., Jr.
1982. Tide-controlled reproduction in the long- nose killifish
Fundulus similis. [Abstr.] Am. Zool. 22:870.
Greeley, M. S., Jr., and R. MacGregor, III.
1983. Annual and semilunar reproductive cycles of the Gulf
killifish, Fundulus grandis, on the Alabama Gulf Coast.
Copeia 1983:711-718.
Harrington, R. W., Jr.
1959. Effects of four combinations of temperature and day-
length on the ovogenetic cycle of a low-latitude fish, Fundulus
confluentus Goode & Bean. Zoologica (N.Y.) 44:149-168.
Johannes, R. E.
1978. Reproductive strategies of coastal niarine fishes in the
tropics. Environ. Biol. Fishes 3:65-84.
Kneib, R. T., and a. E. Stiven.
1978. Growth, reproduction, and feeding of Fundulus hetero-
ditus (L.) on a North Carolina salt marsh. J. Exp. Mar. Biol.
Ecol. 31:121-140.
Korringa, p.
1947. Relations between the moon and periodicity in the
breeding of marine animals. Ecol. Monogr. 17:349-381.
Middaugh, D. P.
1981. Reproduction ecology and spawning periodicity of the
Atlantic silverside, Menidia menidia (Pisces: Atherinidae).
Copeia 1981:766-776.
471
MiDDAUGH, D. P., AND M. J. HeMMER.
1984. Spawning of the tidewater silverside, Menidia penin-
sula (Goode and Bean), in response to tidal and lighting
schedules in the laboratory. Estuaries 7:139-148.
MiDDAUGH, D. P., AND T. TAKITA.
1983. Tidal and diurnal spawning cues in the Atlantic silver-
side, Menidia menidia. Environ. Biol. Fishes 8:97-104.
Miller, C. A., J. M. Wilson, and A. H. Meier.
1981. Induction of semilunar rhythms of reproductive indices
\n Fundulus grandis. [Abstr.] Am. Zool. 21:995.
National Oceanic and Atmospheric Administration.
1981. Tide tables 1982, high and low water predictions, East
Coast of North and South America including Greenland.
U.S. Dep. Commer., 235 p.
Newmann, D.
1978, Entrainment of a semilunar rhythm by simulated tidal
cycles of mechanical disturbance. J. Exp. Mar. Biol. Ecol.
35:173-185.
Ross, R. M.
1983. Annual, semilunar, and diel reproductive rhythms in the
Hawaiian labrid Thallassoma duperrey. Mar. Biol. (Berl.)
72:311-318.
Saigusa, M.
1980. Entrainment of a semilunar rhythm by a simulated
moonlight cycle in the terrestial crab, Sesarma haemntocheir.
Oecologia (Berl.) 46:38-44.
Taylor, M. H., and L. DiMichele.
1980. Ovarian changes during the lunar spawning cycle of
Fundidus heteroclitus. Copeia 1980:118-125.
1983. Spawning site utilization in a Delaware population of
Fundulus heteroclitus (Pisces: Cyprinodontidae). Copeia
1983:719-725.
Taylor, M. H., D. DiMichele, and G. J. Leach.
1977. Egg stranding in the life cycle of the mummichog,
Fundulus heteroclitus. Copeia 1977:397-399.
Taylor, M. H., L. DiMichele, M. M. Levitan, and W. F. Jacob.
1979. Lunar spawning cycle in the mummichog, Fundulus
heteroclitus (Pisces: Cyprinodontidae). Copeia 1979:291-
297.
Thrall, T., and L. Engelman.
1981. Univariate and bivariate spectral analysis. In W. J.
Dixon (editor), BMDP statistical software, p. 604-638. Univ.
Calif. Press, Los Ang.
Waas, B. p., and K. Strawn.
1983. Seasonal and lunar cycles in gonadosomatic indices and
spawning readiness of Fundulus grandis. Contrib. Mar.
Sci., Texas A&M Univ. 26:127-141.
Weisberg, S. B.
1981. Food availability and utilization by the mummichog,
Fundulus heteroclitus (L.). Ph.D. Thesis, Univ. Delaware,
Newark, 104 p.
Weld, M. M., and A. H. Meier.
1982. Circadian gonadal responses to daily disturbances in
gulf killifish. [Abstr.] Am. Zool. 22:866.
Anson H. Hines
Kenric E. Osgood
Joseph J. Miklas
Smithsonian Environmental Research Center
P.O. Box 28
Edgewater, MD 21037
UNDERSEA TOPOGRAPHY AND
THE COMPARATIVE DISTRIBUTIONS OF
TWO PELAGIC CETACEANS
Prey species are not uniformly distributed. Foraging
efficiency, therefore, should be maximized when ef-
fort is concentrated in areas where prey are concen-
trated. Cetacean food is probably most concentrated
in regions of high general productivity. Because the
undersea topography may be a major influence on
productivity, cetacean foraging patterns may be
associated with the topographic patterns of the
ocean floor (Hui 1979). I report here the occurrences
of two species of pelagic odontocete cetaceans, the
Pacific pilot whale, Globicephala Tnacrorhyrwhus,
and the common dolphin, Delphinus delphis, relative
to seafloor topography and to diet. Although it is not
clear if the genus Delphinus in this region is com-
posed of two species or one species with two sub-
species, the vast majority are Delphinus delphis
(Banks and Brownell 1969; Evans 1975). If data
from more than one species are included in this
study, it is assumed that any interspecies difference
in distribution relative to substrate was not signifi-
cant to the analyses.
Methods and Results
This study was conducted in the Southern Califor-
nia Continental Borderland (Fig. 1) which consists of
ridges, deep troughs, and basins (Chase 1968). There
were 61 survey flights totaling 22,353 km. The
flights were conducted at various times, all of them
during midday (1000-1500) from 1968 through 1976.
Totals of 1,057 pilot whales in 38 aggregations (in
January, March, April, July, October, and Decem-
ber) and 47,105 common dolphins in 142 aggrega-
tions (in all months of the year) were observed. The
survey methods have been previously described (Hui
1979).
The data for each species were not divided into
temporal subsets as in Hui (1979), but were treated
as whole sets. The distribution of each species was
examined relative to depth and relative to change in
depth. The method of analysis has been presented in
detail elsewhere (Hui 1979).
Both pilot whales and common dolphins were
distributed uniformly {P > 0.10) throughout the
depth classes but not uniformly among the Contour
Index (CI) classes {P < 0.005). For each species there
were more observations than expected over the
steepest bottom topography and fewer than ex-
pected over the flattest (Table 1).
I also compared the distribution of pilot whales
472
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
among CI classes to the distribution of common
dolphins. Due to the small number of pilot whale
aggregations, the CI range was divided into four
unequal classes to meet the statistical assumptions
for chi-square analysis (Dixon and Massey 1969). The
proportion of pilot whales in each of these classes
34^
33^
32*
120^
119<
118'
117°
Figure 1.- Sightings of pilot whales, Giobicephala macrorhyyichus, and common dolphins, Delphinus delphis. The
study area is bounded on the west by long. 120°00'W and on the east by the coast of California between lat. 34°05'N and
32°24'N. Sightings may not accurately depict the geographic distribution of these species because the survey flights
were not uniformly distributed spatially or temporally. Encounters occurring outside the study area are not shown.
Table 1. — Distribution among contour index classes of observed and expected ag-
gregations (sec text).
Contour index
class
Number of aggregations
(F./)2
Species
Expected (F)
Observed (0
F
Pilot whales
0.01-19.99
13.3
1
11.38
20.00-39.99
6.3
5
0.27
40.00-59.99
5.2
4
0.28
60.00-79.99
7.4
10
0.91
80.00-99.99
5.8
18
X2
25.66
= 38.50
Common dolphins
0.01-19.99
48.0
18
18.75
20.00-39.99
23.2
27
0.62
40.00-59.99
19.3
22
0.27
60.00-79.99
27.2
21
1.41
80.00-99.99
22.2
54
X2
45.55
= 66.60
X2(df
= 4, P = 0.005)
= 14.86
473
was used to compute the expected number of com-
mon dolphins in that class.
The distribution of pilot whales was not the same
as that of common dolphins among the CI classes (P
< 0.005), particularly in the class for the lowest
relief. Of the total chi-square value, 63% is due to
proportionally more observations of dolphins than
pilot whales in this one class (Table 2).
The distributions of the two sets of survey flights
used to collect data for the two species were com-
pared, but the CI range in this case was divided into
10 equal classes. The two sets of survey flights were
equally distributed among the CI classes {P > 0.10).
Table 2. — Comparative distribution among contour index
classes of pilot whales and common dolphins.
Contour index
Dolphin
aggrega
tions
(F-/)2
class
Expected (F)
Observed {f)
F
0.01-39.99
22.4
45
22.80
40.00-59.99
14.9
22
3.38
60.00-79.99
37.4
21
7.19
80.00-99.99
67.3
54
X^
2.63
= 36.00
X2
(df
= 3,
P =
0.005)
= 12.84
'Computed from pilot whale sightings; see text.
Discussion
In the California Bight, pilot whales and common
dolphins are distributed similarly above undersea
topography of high relief, but common dolphins oc-
cur more frequently than pilot whales over areas of
low relief. This difference may be linked to differ-
ences in feeding habits.
Pilot whales and common dolphins have significant
morphological and physiological differences that are
associated with their foods and feeding methods.
Pilot whales are larger (7 m vs. 2 m in length) and
have fewer but larger teeth (40 vs. 200) than com-
mon dolphins (Orr 1972). Pilot whales are capable of
diving to 610 m (Bowers and Henderson 1972) while
common dolphins dive to 257 m (Evans 1971).
The diet of the common dolphin in the Southern
California Bight includes 19 species of fish, 2 species
of squid, and miscellaneous crustaceans (Fitch and
Brownell 1968; Evans 1975).
In contrast to common dolphins, pilot whales ap-
pear to be stenophagous, eating primarily squid.
Atlantic pilot whales, GLobicephala melaena, eat
primarily squid {Illex illecebrosus). The only fish
reported eaten (cod, Gadus morhua) composes <10%
of the diet (Sergeant 1962). There has been no study
on the Pacific pilot whale comparable with that of
Sergeant's (1962) on the Atlantic form; however, the
stomachs of four wild Pacific pilot whales have been
examined. They contained squid but no fish (W. A.
Walker,! (] \y Woodhouse,^ D. J. Seagars^). In cap-
tivity an Atlantic pilot whale rejected mullet (Mugili-
dae) and blue runner (Carangidae) fish and accepted
only squid (probably Loligo pealei) until it was trick-
ed into eating some herring (Clupeidae); and then the
indications were that "He did not seem to digest the
fish as well" (Kritzler 1949).
Squid distribution cannot be related to any particu-
lar bottom topography along the California coast
because squids are not easily collected with sampling
methods used in distribution studies (Mais 1974).
However, it may be inferred that the narrow range
of seafloor topographies visited by pilot whales
reflects the narrow range of their diet and the areas
where squid can be most easily caught by pilot
whales.
Also concentrated over areas of canyons and
escarpments are anchovies (Mais 1974), a major com-
ponent of the dolphin diet (Fitch and Brownell 1968;
Evans 1975). Common dolphins frequent these areas
most. However, common dolphins are euryphagous.
Some prey probably occur over seafloor of low relief,
although this could not be confirmed from fish
reports because bottom topography is not a para-
meter which is recorded in fish distribution studies.
If some prey do occur over areas of low relief, their
distribution would partially explain why dolphins oc-
cur over seafloor of low relief more frequently than
do pilot whales.
My analyses show that the daytime distribution
patterns of these two pelagic cetacean species are
not random but are related to bottom topography.
Although the distributions are similar, they are not
the same. Differences in distributions may be due to
the different foraging patterns but no firm conclu-
sion can be drawn until more information is
available.
Acknowledgments
I thank G. A. Bartholomew, M. F. Platter-Rieger,
F. G. Wood, and two anonymous reviewers for their
helpful comments; also D. J. Seagars, W. A Walker,
and C. W. Woodhouse for information on the
'W. A. Walker, Research Associate, Section of Mammalogy,
Natural History Museum of Los Angeles County, Los Angeles, CA
90007, pers. commun. July 1980.
-C. W. Woodhouse, Curator of Vertebrate Department, Santa
Barbara Museum of Natural History, 2559 Puesta del Sol Road,
Santa Barbara, CA 93105, pers. commun. July 1980.
'D. J. Seagars, Wildlife Biologist, National Marine Fisheries Ser-
vice, Southwest Region, 300 S. Ferry St., Terminal Island, CA
90731, pers. commun. January 1981.
474
stomach contents of Pacific pilot whales. My special
thanks to W. E. Evans of Hubbs Sea World
Research Institute for his support and encourage-
ment throughout this study, which was supported by
ONR contract T0044 subproject RR0310201 (W. E.
Evans, principal investigator), and NMFS agree-
ment 01-6-200 11439.
Literature Cited
Banks, R. C, and R. L. Brownell.
1969. Taxonomy of the common dolphins of the eastern Paci-
fic ocean. J. Mammal. 50:262-271.
Bowers, C. A., and R. S. Henderson.
1972. Project Deep Ops: Deep object recoverj' with pilot and
killer whales. NUC TP 306, 86 p. Naval Undersea Center,
San Diego, CA 92152.
Chase, T. E.
1968. Sea floor topography of central eastern PacijRc Ocean.
Bur. Commer. Fish. Circular 291, 33 p.
Dixon, W. J., and F. J. Massey, Jr.
1969. Introduction to statistical analysis. 3d ed. McGraw-
Hill, N.Y., 638 p.
Evans, W. E.
1971. Orientation behavior of delphinids: radio telemetric
studies. Ann. N.Y. Acad. Sci. 188:142-160.
1975. Distribution, differentiation of populations, and other
aspects of the natural history of Delpkinus delphis Linnaeus
in the northeastern Pacific. Ph.D. Thesis, Univ. California,
Los Angeles, 164 p.
Fitch, J. E., and R. L. Brownell, Jr.
1968. Fish otoliths in cetacean stomachs and their importance
in interpreting feeding habits. J. Fish. Res. Board Can. 25:
2561-2574.
Hui, C. A.
1979. Undersea topography and distribution of dolphins of the
genus Delphimis in the southern California bight. J. Mam-
mal. 60:521-527.
Kritzler, H.
1949. The pilot whale at Marineland. Natural History 58:
302-308, 331-332.
Mais, K. F.
1974. Pelagic fish surveys in the California current. Calif.
Dep. Fish Game, Fish Bull. 162, 79 p.
Orr, R. T.
1972. Marine mammals of California. Univ. Calif. Press,
Berkeley, 64 p.
Sergeant, D. E.
1962. The biology of the pilot or pothead whale Globicephala
melaena (Traill) in Newfoundland waters. Fish. Res. Board
Can., Bull. 132, 84 p.
Clifford A. Hui
Chemistry and Biochemistry Branch, Code 521
Naval Ocean Systems Center
San Diego, CA 92152-5000
LARVAL AND JUVENILE GROWTH OF
SABLEFISH, ANOPLOPOMA FIMBRIA, AS
DETERMINED FROM OTOLITH INCREMENTS
The black cod or sablefish, A naplopoma fimbria, has
been the subject of an intensifying fishery off the
west coast of North America over the last decade.
Biological information on this species, however, in-
cluding data on spawning, early life history, age and
growth, and population structure, is relatively
meager. Sablefish are widely distributed in the
northern Pacific, with adults most abundant at
depths of 366-915 m (Hart 1973). Mason et al. (1983)
suggested that eggs are spawned and developed in
waters deeper than 300 m and colder than 6°C off
Canada. Juveniles occur in shallow water, however,
and larvae are almost exclusively neustonic (Kendall
and Clark^). Thus larval development and growth oc-
cur in much warmer water than that inhabited by
later stages, particularly in the southern portion of
the species range.
Sablefish growth has been described by Heyamoto
(1962) and Pruter (1954), among others, who used
scale annuli to define the growth pattern. More re-
cent work, however, has shown that the age esti-
mates, particularly for older, mature fish, are in er-
ror; growth is apparently much slower and longevity
much greater than previously thought (Beamish and
Chilton 1982). The warmer neustonic habitat of the
larvae may result in different growth patterns in
early life; ontogenetic changes in growth and habitat
are relatively common among deeper living fishes
(Boehlert 1982; Luczkovich and 011a 1983). The only
observations on growth of young sablefish are those
of Heyamoto (1962), who suggested that juveniles of
12-16 cm fork length (FL) were about 6 mo old. In
the present study we report on the growth of field-
collected larval and juvenile sablefish where age was
estimated by enumerating growth increments on the
otoliths.
Materials and Methods
Larval and juvenile sablefish were collected in
1981-83. Larvae were taken in 0.5 m neuston nets
(Sameoto and Jaroszynski 1969) with 0.505 mm
mesh, off the coasts of Oregon and Washington dur-
ing May 1982 by the RV Posey don. Samples were im-
mediately preserved in 80% ethanol. After sorting.
^Kendall, A. W., Jr., and J. Clark. 1982. Ichthyoplankton off
Washington, Oregon, and northern California, April-May 1980.
Processed Rep. 82-11, 44 p. Northwest and Alaska Fisheries
Center, National Marine Fisheries Service, NOAA, 2725 Montlake
Blvd. East, Seattle, WA 98102.
FISHERY BULLETIN: VOL. 83, NO. 3, 1985.
475
larvae were stored in individual vials labeled with
sample number and date. Additional larvae were col-
lected with neuston nets in May 1983 by the RV
Ekvator. Larger juveniles (> 70 mm standard length
(SL)) were taken in a small mesh purse seine
deployed from 24 to 40 km off of the Oregon-Wash-
ington coasts during the summer months of 1981
(Fig. 1). Specimens were frozen on board and held
until measurements and otoliths were taken. Fork
lengths to the nearest millimeter were recorded for
these larger juveniles and standard lengths to the
nearest 0.1 mm were measured for all larvae and
small juveniles. No corrections were made for poten-
tial shrinkage from preservation of young larvae, but
alcohol preservation causes no noticeable shrinkage
in length of anchovy larvae (Theilacker 1980). For
subsequent analysis, fork lengths were converted to
standard length by the relationship SL (mm) = 0.91
FL (mm) -1.15 (n = 54, r^ = 0.999), which was
based upon specimens 21.7 to 297 mm FL.
Otoliths of larval sablefish were removed and
cleaned under a dissecting microscope fitted with
polarizing filters. Increments on otoliths from larvae
< 26 mm SL were clearly visible from the focus to
the margin (Fig. 2); these otoliths were left intact, af-
fixed to microscope slides with histological mounting
medium and cover slips, and increments were read in
the sagittal plane (see Taubert and Coble 1977 for
terminology). For larger larvae and most juveniles, a
sagittal section of the otolith provided the clearest in-
crements. The left otolith of every pair was mounted
in histological medium on a microscope slide and the
Figure 1.- Distribution of AnopUrpoma fimbria samples, along
the Pacific coast, used for age and growth analysis. Circles
represent the neuston samples taken during May 1982,
triangles represent the purse seine samples taken during sum-
mer 1981, and squares represent the 1983 neuston samples.
476
mm
Figure 2. - Sagitta otolith from a larval Anoplopomafiynbria (22.0
mm SL; duplicate increment counts were 37 and 40 d). Scale bar
= 0.1 mm.
internal surface was ground until the focus was visi-
ble. The microscope slide was heated and the section
was turned over to expose the external surface.
Grinding and polishing continued, while care was
taken to insure that material was not lost from the
margin. The result was a clear, thin section of the
otolith in the sagittal plane. For some of the larger
juveniles (> 100 mm SL), transverse sections were
cut from the otoliths using a diamond saw, mounted
on microscope slides, and ground to make the incre-
ments clear. All otoliths were read under a com-
pound microscope at 400 x or 1,000 x magnifica-
tion. Two independent counts were made for each
otolith. These counts were made at least 2 wk apart;
the age assigned to each specimen was the mean of
the two counts.
Increments, comprised of adjacent light and dark
ring pairs, were distinct and clear in the smallest
otoliths (Fig. 2), but interpretation became more dif-
ficult as the increments became progressively
smaller and as changes in growth patterns occurred
in the otolith structure of the older specimens. There
was no evidence of subdaily patterns in the incre-
ments, and each increment was assumed to repre-
sent 1 d. Support for the daily deposition of incre-
ments was provided by data on three live juvenile
sablefish held in the laboratory (Table 1). The
specimens were captured by neuston net off
Newport, OR, and transported to the laboratory
where they were fed to satiation daily on Artemia. A
check, apparently associated with capture and
transfer to the laboratory, was evident on the otolith
of each fish. The numbers of increments past this
check corresponded closely to days captive; the
minor differences are attributed to counting error
and/or difficulty in interpretation of the check (Table
.1). We thus consider the increments to be deposited
with a daily periodicity. Hereafter increment counts
will be equated with days after first increment for-
mation; as we discuss later, first increment forma-
tion may occur at first feeding.
Data from the 1982-83 larval collections and the
1981 juvenile collections were fitted separately with
simple linear regressions. Nonlinear curves (expo-
nential, logistic, and Laird-Gompertz) were fitted to
combined data with the NLIN procedure on the
SAS- statistical package (SAS Institute, Inc. 1982).
Table 1. — Growth and increment formation in captive
specimens of Anoplopoma fimbria. L^, L2: standard length
(mm) at capture and death, respectively.
Capture date
'-I
h
Days
captive
Increment
past check
Total
increments
2 May 1983
17 May 1983
24 May 1983
19.9
14.1
53.8
60.4
53.4
109.7
31
40
32
31
38
33
63
95
87
Results and Discussion
This study considers a total of 105 individuals, in-
cluding 71 larvae and juveniles (9.8 to 41.2 mm SL)
from the 1982 neuston collections, 21 juveniles
(102.8 to 259.6 mm SL) from the 1981 purse seine
collections, and 13 larvae (10.4 to 25.3 mm SL) taken
in the 1983 neuston collections. Mean increment
counts ranged from 9 increments for the youngest
larva to 180 increments for the oldest juvenile. The
abundance of larval sablefish in the neuston (Kendall
and Clark footnote 1) at such young ages suggests
that larvae move rapidly after hatching from the
deep spawning region rather than early growth oc-
curring at depths as suggested by Mason et al.
(1983). The difference between the two increment
counts for each otolith increased with increasing
count, but the coefficient of variation remained the
^Reference to trade names does not imply endorsement by the Na-
tional Marine Fisheries Service, NOAA.
477
same for the two ranges. For the larvae collected in
1982, with an overall mean of 30.8 increments, the
mean difference was 1.67 increments (n = 71, stan-
dard deviation (SD) = 1.45). For the 1981 juvenile
collections, with overall mean of 109.5 increments,
the mean difference between the two estimates was
6.57 increments {n = 21, SD = 5.03).
Growth rates of field-collected larval and juvenile
sablefish differ considerably. The data for the 1982
larval collections is described by the line
SL = 0.375 (age, d) + 5.27
n = 71, r2 = 0.838,
suggesting a mean growth rate for small larvae of
0.375 mnVd and an intercept of 5.27 mm, which coin-
cides with the size of newly hatched larvae (Mason et
al. 1983). Similarly the 1981 juvenile data is de-
scribed by the line
SL = 1.469 (age, d) - 0.926
n = 21, r2 = 0.822,
tain of these growth differences may have been a
function of gear selection. If net avoidance is a func-
tion of fish size, as for most other planktonic
organisms (Barkley 1972), then the oldest specimens
taken in the neuston gear may have been only the
slow-growing members of that cohort. Alternatively,
interruptions of increment formation, resulting in
underestimates of age, may occur. This has been
observed for some species by Geffen (1982). In the
laboratory specimens, however, one individual (L2 =
60.4 mm SL, Table 1) ceased eating for 5-6 d,
became emaciated, and died. The last five incre-
ments near the margin were smaller than the re-
mainder, but the 1 : 1 correspondence of days to incre-
ments suggests that increment formation continued.
Estimated age-at-length data from all years were
combined to describe the growth of sablefish to an
age of about 200 d. Comparing exponential, logistic,
and Laird-Gompertz growth models, the best fit (as
judged by residual sums of squares) was provided by
the Laird-Gompertz growth model (Fig. 3) in the
form:
suggesting a mean growth rate of 1.47 mm/d. Cer-
L( = L^{AJa){l - exp(- at))
280
Figure 3. -Estimated age at length for all Aru/plorpcmm
fimbria in the study. Specimens taken in neuston nets (n =
84, including the 13 from 1983) are represented by circles,
1981 juvenile specimens from purse seine collections (n =
21) are represented by triangles. The equation and line
represent the least squares fit of the Laird-Gompertz
growth model.
20 40 60 80 100 120 140 160 180 200
MEAN AGE (DAYS)
478
where L, = standard length (mm) at age t (d), L,, =
initial length (^-intercept), and A^^ and a are fitted
parameters (Table 2).
This sigmoid curve suggests relatively slow
growth to an age of about 50 d and a length of about
25 mm SL, followed by rapidly accelerating growth
through the juvenile stage, an inflection point at
113.2 mm, and an asymptotic length near 307.8 mm.
Since sablefish achieve lengths to 100 cm (Hart
1973), these results should not be extrapolated
beyond the ages in the present study. Also, the
predicted fit of zero age individuals (Lq) is 1.22 mm
SL (Table 2; Fig. 3). This value does not accurately
reflect the length of sablefish at hatching. Egg size in
sablefish ranges from 1.8 to 2.2 mm and newly
hatched larvae are 5 to 6 mm (Mason et al. 1983). If
daily increments are first laid down at first feeding
as in some other species (Laroche et al. 1982), then
this intercept is clearly an underestimate. Mean egg
size suggests a length at first feeding of about 8 mm
(Shirota 1970). The smallest larva taken in the pres-
ent study was 9.8 mm SL (Fig. 3). This part of the
curve may be related to the inclusion of the older,
slower growing neustonic specimens. Another factor
may be effects of shrinkage; small specimens were
preserved in ethanol, older juveniles frozen. The
magnitude of shrinkage for A. fimbria is unknown,
but capture and preservation of other fish larvae
causes shrinkage which decreases with increasing
age or size (Theilacker 1980). Thus increases in ac-
tual length for small individuals may have been
relatively greater, changing the fitted equation and
possibly increasing the length at time zero (Fig. 3).
Heyamoto (1962) estimated growth for young
sablefish, suggesting that specimens 12.3 to 16.4 cm
FL (11.1 to 14.8 cm SL) were 6 mo old. His data,
however, were based upon estimating the age at
collection by difference between capture and an
assumed spawning season. In our study, 6-mo-old
specimens were > 24 cm SL. The specimens cap-
tured by Heyamoto (1962) were taken by trawl in
320 to 412 m, much deeper than the epipelagic
juveniles in our study. Beamish et al. (1983) used
daily increments as part of a study to validate an-
nulus formation in sablefish. In nine specimens 23 to
27 cm FL (208 to 245 mm SL), they observed from
270 to 350 (mean 313) increments but suggested
that the fish were 1 yr old due to the inability to
count all increments. Based upon our growth curve
(Fig. 3), their ages would be overestimates.
Recent observations of laboratory growth are in
substantial agreement with growth described by our
curve. Shenker and Olla^ found average growth
rates as high as 2.3 mm/d for juvenile sablefish fed ad
Table 2.— Fitted parameters of the Laird-
Gompertz growth model for larval and juvenile
Anoplopoma fimbria in the present study. The
curve is fitted to all larvae and juveniles (W =
105) based upon counts of otolith increments.
Parameter
Estimate
Asymptotic
standard error
1.2203
0.1084
0.0196
0.4675
0.0146
0.0015
libitum. These fish were near the lengths where our
curve predicts fastest growth (2 mnVd, Fig. 3). High
growth rates were also observed for fish smaller
than 25 mm, where our data suggest relatively slow
growth. Grover and Olla'* noted starvation of field-
collected sablefish larvae based upon morphological
criteria; thus food probably limits sablefish growth in
the field. This species apparently has a great scope
for growth given high laboratory rations or patches
of high prey density in the field.
The distribution of dates of first increment forma-
tion were estimated by back calculating from the
ages of all specimens in our study. Since larvae and
juveniles were from different years and sampling
gears, it is possible that differences would be ob-
served in this distribution. Since the plankton gear
selects for smaller larvae due to avoidance by later
stages, the results could be biased if the entire
spawning season were not sampled. The median
dates for the 1982 larvae (8 April) and the 1981
juveniles (18 March), however, were similar. Thus all
105 samples were combined and the distribution of
the dates of first increment formation plotted (Fig.
4). The distribution has a mode in early April. If the
first increment is formed in association with first
feeding, as in most other species studied (Brothers et
al. 1976; Taubert and Coble 1977; Laroche et al.
1982), then the spawning dates would precede the
distribution in Figure 4. Ware (1975) provided an
egg size-incubation time relationship for fishes;
sablefish, with a 2 mm egg, would have an incubation
time of 13 d. If a similar time is spent in yolk absorp-
tion before first feeding, peak spawning would occur
in early March. This generally agrees with most
other reports of the spawning season for A. fimbria.
^Shenker, J., and B. L. 011a. Laboratory growth and feeding of
]uwem\e ssb\eT\s\ Ano^lcrpoma fimhris. Unpubl. manuscr.
■•Grover, J., and B. L. OUa. Field evidence for starvation of larval
sablefish, Anoplopoma fimbria. Manuscr. in prep. Northwest
and Alaska Fisheries Center, Newport Field Office, National
Marine Fisheries Service, NOAA, c/o Marine Science Center,
Marine Science Drive, Newport, OR 97365 (direct correspondence
to B. L. 011a).
479
I/)
z
Ui
2
o
LlI
a.
CD
2
r>
z
15
FEBRUARY
20 25 I
i
10 15 20 25
MARCH
30 I
10 15 20 25
APRIL
30
10 15
MAY
Figure 4. -Distribution of dates of first increment formation for A noplopam-a fimbrin, determined by back-calculations using
age and collection date.
Phillips (1958) defined the peak spawning season off
California to be January-February. Bell and Gharrett
(1945) suggested that the spawning season was
around December off Washington based upon fisher-
men's observations and the presence of spent
females in January. Farther north, Thompson (1941)
observed ripe females and fertilized eggs in March at
Cape St. James (lat. 51°45'N). More recent work has
shown that the spawning season off British Columbia
occurs in January to February with the peak of
spawning in February (Mason et al. 1983).
Our observed growth rates for A. fimbria during
the first 6 months of life are high for a temperate-
subarctic species, yet are clearly below the potential
growth rate as shown in the laboratory (Shenker and
011a footnote 3). Similar but lower laboratory growth
rates (1.2 mm/d) were observed for 100 to 150 mm
juvenile red hake, Urophycis chuss, by Luczkovich
and 011a (1983). Both of these species contrast mark-
edly with larval juvenile growth in other taxa. Boeh-
lert and Yoklavich (1983), for example, summarized
laboratory and field growth measurements for 13
species in the genus Sebastes and noted growth rates
ranging from 0.092 to 0.590 mm/d. Young sablefish
thus utilize the neustonic and pelagic environment to
rapidly reach sizes at which migration to the benthic
adult habitat occurs.
Acknowledgments
This work was supported by the Northwest and
Alaska Fisheries Center, National Marine Fisheries
Service, Seattle, WA, through contracts 81-ABC-
00192-PR6 and 83-ABC-00045. We thank A. W.
Kendall, Jr., W. G. Pearcy, and J. Shenker for pro-
viding specimens for this study, Chris Wilson for
technical assistance with otolith preparation, and R.
Methot for reviewing the manuscript.
Literature Cited
Barkley, R. a.
1972. Selectivity of towed-net samplers. Fish. Bull., U.S. 70:
799-820.
Beamish, R. J., and D. E. Chilton.
1982. Preliminary evaluation of a method to determine the age
of sablefish {A noplopoma fimbria). Can. J. Fish. Aquat. Sci.
39:277-287.
Beamish, R. J., G. A. McFarlane, and D. E. Chilton.
1983. Use of oxy tetracycline and other methods to validate a
method of age determination for sablefish. In B. R. Meteff
(editor). Proceedings of the International Sablefish Sympo-
sium, p. 95-116. Alaska Sea Grant College Program, Univ.
Alaska, Fairbanks, Sea Grant Rep. 83-8.
Bell, F. H., and J. T. Gharrett.
1945. The Pacific coast blackcod, Anoplopoma fimbria.
Copeia 1945:94-103.
Boehlert, G. W.
1982. Ontogenetic changes in growth and their relationship
with temperature and habitat change. In G. M. Cailliet and
C. A. Simenstad (editors), GUTSHOP '81. Fish food habits
studies, p. 115-123. Proceedings of the Third Pacific Work-
shop, December 6-9, 1981, Pacific Grove, Calif.; Wash. Sea
Grant Prog., Univ. Wash., Seattle, WSW-WO 82-2.
Boehlert, G. W., and M. M. Yoklavich.
1983. Effects of temperature, ration, and fish size on growth
of juvenile black rockfish, Sebastes melaruyps. Environ. Biol.
Fishes 8:17-28.
Brothers, E. B., C. P. Mathews, and R. Lasker
1976. Daily growth increments in otoliths from larval and
adult fishes. Fish. Bull., U.S. 74:1-8.
Geffen, a. J.
1982. Otolith ring deposition in relation to growth in herring
(Clupea harengus) and turbot {Scopthalmus maximtts) larvae.
480
Mar. Biol. (Berl.) 71:317-326.
Hart, J. L.
1973. Pacific fishes of Canada. Fish. Res. Board Can. Bull.
180, 740 p.
Heyamoto, H.
1962. Age of younj; sablefish, AvopUrpmna fimbria (Pallas)
1811. J. Fish. Res. Board Can. 19:1175-1177.
Laroche, J. L., S. L. Richardson, and A. A. Rosenberg.
1982. Age and growth of a pleuronectid, Paraphrya vetulus,
during the pelagic larval period in Oregon coastal waters.
Fish. Bull., U.S. 80:93-104.
LuczKovicH, J. J., AND B. L. Olla.
1983. Feeding behavior, prey consumption, and growth of
juvenile red hake. Trans. Am. Fish. Soc. 112:629-637.
Mason, J. C. R. J. Beamish, and G. A. McFarlane.
1983. Sexual maturity-, fecundity, spawning, and early life
historj' of sablefish {Anoplapoma fvmbrixj) off the Pacific
coast of Canada. Can. J. Fish. Aquat. Sci. 40:2126-2134.
Phillips, J. B.
1958. The fishery for sablefish, A noplopoma fimbria. Calif.
Fish Game 44:79-84.
Pruter, a. T.
1954. Age and growth of the Oregon sablefish, Anoplopoma
fitnhrta. Pac. Mar. Fish. Comm. Bull. 3:121-128.
Sameoto, D. D., and L. 0. Jaroszynski.
1969. Otter surface sampler: a new neuston net. J. Fish. Res.
Board Can. 26:2240-2244.
Shirota, a.
1970. Studies on the mouth size of fish larvae. Bull. Jpn. Soc.
Sci. Fish. 36:353-368.
SAS Institi'te, Inc.
1982. SAS users guide. SAS Institute, Inc., Raleigh, NC,
494 p.
Tai'bert. B. D., and D. W. Coble.
1977. Daily rings in otoliths of three species oi Lepfrmis and
Tilnpia monsambira. J. Fish. Res. Board Can. 34:332-340.
Theilacker, G. H.
1980. Changes in body measurement of larval northern an-
chovy, Engrnuii.'< mordaj-, and other fishes due to handling
and preservation. Fish. Bull., U.S. 78:685-692.
Thompson, W. F., Jr.
1941. A note on the spawning of the blackcod (Anoplopoma
fmihria). Copeia 1941:270.
Ware, D. M.
1975. Relation between egg size, growth, and natural mortal-
ity of larval fish. J. Fish. Res. Board Can. 32:2503-2512.
George W. Boehlert
College of Oceanography and Marine Science Center
Oregon State University
Nevyport. OR 97365
Present address:
Southwest Fisheries Center Honolulu Laboratory
National Marine Fisheries Service, NOAA
P.O. Box 3830
Honolulu, HI 96812
Mary M. Yoklavich
College of Oceanography and Marine Science Center
Oregon State University
Newport, OR 97365
481
INFORMATION FOR CONTRIBUTORS TO THE FISHERY BULLETIN
y
Manuscripts submitted to the Fishei'y Bulletin will reach print faster if they conform to the following instructions.
These are not absolute requirements, of course, but desiderata.
CONTENT OF MANUSCRIPT
The title page should give only the title of the paper,
the author's name, his affiliation, and mailing address, in-
cluding ZIP code
The abstract should not exceed one double-spaced page.
In the text. Fishery Bulletin style, for the most part,
follows that of the U.S. Government Printing Office Style
Manual. Fish names follow the style of the American
Fisheries Society Special Publication No. 12, A List of Com-
mon and Scientific Names of Fishes from the United States
and Canada, Fourth Edition, 1980.
Tfext footnotes should be typed separately from the text.
Figures and tables, with their legends and headings,
should be self-explanatory, not requiring reference to the
text. Their placement should be indicated in the right-hand
margin of the manuscript.
Preferably figures should be reduced by photography to
5% inches (for single-column figures, allowing for 50%
reduction in printing), or to 12 inches (for double-column
figures). The maximum height, for either width, is 14
inches. Photographs should be printed on high quality or
glossy paper.
Do not send original drawings to the Scientific Editor;
if they, rather than the photographic reductions, are needed
by the printer, the Scientific Publications Office will request
them.
Each table should start on a separate page Consistency
in headings and format is desirable. Vertical rules should
be avoided, as they make the tables more expensive to print.
Footnotes in tables should be numbered sequentially in
arable numerals. To avoid confusion with powers, they
should be placed to the left of numerals.
Acknowledgments, if included, are placed at the end of
the text.
Literature is cited in the text as: Lynn and Reid (1968)
or (Lynn and Reid 1968). All papers referred to in the text
should be listed alphabetically by the senior author's sur-
name under the heading "Literature Cited." Only the
author's surname and initials are required in the literature
cited. The accuracy of the literature cited is the respon-
sibility of the author. Abbreviations of names of periodicals
and serials should conform to Serial Sources for the BIOSIS
Data Base. (Chemical Abfttracts also uses this system, which
was developed by the American Standards Association.)
Common abbreviations and symbols, such as mm, m,
g, ml, mg, °C (for Celsius), %, "/qq, and so forth, should be
used. Abbreviate units of measure only when used with
numerals. Periods are only rarely used with abbreviations.
We prefer that measurements be given in metric units;
other equivalent units may be given in parentheses.
FORM OF THE MANUSCRIPT
The original of the manuscript should be typed, double-
spaced, on white bond paper. Please triple space above
headings. We would rather receive good duplicated copies
of manuscripts than carbon copies. The sequence of the
material should be:
TITLE PAGE
ABSTRACT
TEXT
LITERATURE CITED
TEXT FOOTNOTES
APPENDIX
TABLES (Each table should be numbered with an
arabic numeral and heading provided).
LIST OF FIGURES (Entire figure legends)
FIGURES (Each figure should be numbered with an
arabic numeral; legends are desired)
ADDITIONAL INFORMATION
Send the ribbon copy and two duplicated or carbon copies
of the manuscript to:
Dr. William J. Richards, Scientific Editor
Fishery Bulletin
Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service, NOAA
75 Virginia Beach Drive
Miami, FL 33149-1099
Fifty separates will be supplied to an author free of
charge and 50 supplied to his organization. No covers will
be supplied.
Contents— Cont "■
GASKIN, DAVID E., and ALAN P. WATSON. harbor porpoise, Phocoena pho-
coena, in Fisli Harbour, New Brunswick, \ ' a: occupancy, distribution, and
movements 427
Notes
GROSSMAN, GARY D., MICHAEL J. HARRIS, and JOSEPH E. HIGHTOWER.
The relationship between tiiefish, Lopholatilus chamaeleonticeps, abundance and
sediment composition off Georgia 443
MATARESE, ANN C., and BEVERLY M. VINTER. The development and occur-
rence of larvae of the longfin Irish lord, Hemilepidotus zapus (Cottidae) 447
POLOVINA, JEFFREY J., and MARK D. OW. An approach to estimating an eco-
system box model 457
SEDBERRY, GEORGE R. Food and feeding of the tomtate, Haemulon aurolineatum
(Pisces, Haemulidae), in the South Atlantic Bight 461
HINES, ANSON H., KENRIC E. OSGOOD, and JOSEPH J. MIKLAS. Semilunar
reproductive cycles in Fundulus heteroclitus (Pisces: Cyprinodontidae) in an area
without lunar tidal cycles 467
HUI, CLIFFORD A. Undersea topography and the comparative distributions of two
pelagic cetaceans 472
BOEHLERT, GEORGE W., and MARY M. YOKLAVICH. Larval and juvenile growth
of sablefish, Anoplopoma fimbria, as determined from otolith increments 475
• GPO 593-096
K^^^'^'Co,
Fishem Bulletin
"^^IrES O^ ^
''EB 7 1986
^!^H2E3E!!ZMl5s:
Vol. 83, No. 4
October 1985
PARRISH, R. H., D. L. MALLICOATE, and K. F. MAIS. Regional variations in the
growth and age composition of northern anchovy, Engraulis mordax 483
JOHNSON, PHYLLIS T. Parasites of benthic amphipods: microsporidans oiAmpelisca
agassizi (Judd) and some other gammarideans 497
OVERHOLTZ, WILLIAM J., and ALBERT V. TYLER. Long-term responses of the
demersal fish assemblages of Georges Bank 507
WAHLEN, BRUCE E., and TIM D. SMITH. Observer effect on incidental dolphin mor-
tality in the eastern tropical Pacific tuna fishery 521
SINGER, MICHAEL M. Food habits of juvenile rockfishes (Sebastes) in a central Califor-
nia kelp forest 531
READ, ANDREW J., and DAVID E. GASKIN. Radio tracking the movements and
activities of harbor porpoises, Phocoena phocoena (L.), in the Bay of Fundy,
Canada 543
HOHN, ALETA A., and P S. HAMMOND. Early postnatal growth of the spotted
dolphin, Stenella attenuata, in the offshore eastern tropical Pacific 553
BROWN, R. S., and N. CAPUTI. Factors affecting the growth of undersize western
rock lobster, Panulirus cygnus George, returned by fishermen to the sea 567
JAMIESON, G. S., and A. CAMPBELL. Sea scallop fishing impact on American lobsters
in the Gulf of St. Lawrence 575
WARLEN, STANLEY M., and ALEXANDER J. CHESTER. Age; growth, and distribu-
tion of larval spot, Leiostomus xanthurus, off North Carolina 587
ALBERS, W D., and P J. ANDERSON. Diet of Pacific cod, Gadiis macrocephalus,
and predation on the northern pink shrimp, Pandalus borealis, in Pavlof Bay,
Alaska 601
BOEHLERT, GEORGE W, DENA M. GADOMSKI, and BRUCE C. MUNDY. Vertical
distribution of ichthyoplankton off the Oregon coast in spring and summer
months 611
AU, DAVID W. K., and WAYNE L. PERRYMAN. Dolphin habitats in the eastern tropical
Pacific 623
FREEMAN, MARY C, NATE NEALLY, and GARY D. GROSSMAN. Aspects of the
life history of the fluffy sculpin, Oligocottus snyderi 645
BARLOW, JAY. Variability, trends, and biases in reproductive rates of spotted dolphins,
Stenella attenuata 657
{Continued on back cover)
Seattle, Washington
U.S. DEPARTMENT OF COMMERCE
Malcolm Baldrlge, Secretary
NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION
John V. Byrne, Administrator
NATIONAL MARINE FISHERIES SERVICE
William G. Gordon, Assistant Administrator
Fishery Bulletin
The Fishery Bulletin carries original research reports and technical notes on investigations in fishery science, engineering, and economics.
The Bulletin of the United States Fish Commission was begun in 1881; it became the Bulletin of the Bureau of Fisheries in 1904 and
the Fishery Bulletin of the Fish and Wildlife Service in 1941. Separates were issued as documents through volume 46; the last document
was Na 1103. Beginning with volume 47 in 1931 and continuing through volume 62 in 1963, each separate appeared as a numbered bulletin.
A new system began in 1963 with volume 63 in which papers are bound together in a single issue of the bulletin instead of being issued
individually. Beginning with volume 70, number 1, January 1972, the Fishery Bulletin became a periodical, issued quarterly. In this form,
it is available by subscription from the Superintendent of Documents, U.S. Government Printing Office, Washington, DC 20402. It is also
available free in limited numbers to libraries, research institutions, State and Federal agencies, and m exchange for other scientific
publications.
SCIENTIFIC EDITOR, Fishery Bulletin
Dr. William J. Richards
Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service, NOAA
Miami, FL 33149-1099
Editorial Committee
Dr. Bruce B. Collette
National Marine Fisheries Service
Dr. Donald C. Malins
National Marine Fisheries Service
Dr. Edward D. Houde
Chesapeake Biological Laboratory
Dr. Merton C. Ingham
National Marine Fisheries Service
Dr. Reuben Lasker
National Marine Fisheries Service
Dr. Jerome J. Pella
National Marine Fisheries Service
Dr. Jay C. Quast
National Marine Fisheries Service
Dr. Carl J. Sindermann
National Marine Fisheries Service
Mary S. Fukuyama, Managing Editor
The Fishery Bulletin (ISSN 0090-0656) is published quarterly by the Scientific Publications Office, National Marine Fisheries Service;
NOAA, 7600 Sand Point Way NE, BIN C15700, Seattle, WA 98115. Second class postage is paid in Seattle, Wash., and additional offices.
POSTMASTER send address changes for subscriptions to Superintendent of Documents, U.S. Government Printing Office, Washington,
DC 20402.
Although the contents have not been copyrighted and may be reprinted entirely, reference to source is appreciated.
The Secretary of Commerce has determined that the publication of this periodical is necessary in the transaction of the public business
required by law of this Department. Use of funds for printing of this periodical has been approved by the Director of the Office of Manage-
ment and Budget through 1 April 1986.
i
Fishery Bulletin
CONTENTS
Vol. 83, No. 4 October 1985
PARRISH, R. H, D. L. MALLICOATE, and K. F. MAIS. Regional variations in the
growth and age composition of northern anchovy, Engraulis mordax 483
JOHNSON, PHYLLIS T. Parasites of benthic amphipods: microsporidans of Ampelisca
agassizi (Judd) and some other gammarideans 497
OVERHOLTZ, WILLIAM J., and ALBERT V. TYLER. Long-term responses of the
demersal fish assemblages of Georges Bank 507
WAHLEN, BRUCE E., and TIM D. SMITH. Observer effect on incidental dolphin mor-
tality in the eastern tropical Pacific tuna fishery 521
SINGER, MICHAEL M. Food habits of juvenile rockfishes (Sebastes) in a central Califor-
nia kelp forest 531
READ, ANDREW J., and DAVID E. GASKIN. Radio tracking the movements and
activities of harbor porpoises, Phocoena phocoena (L.), in the Bay of Fundy,
Canada 543
HOHN, ALETA A., and P S. HAMMOND. Early postnatal growth of the spotted
dolphin, Stenella attenuata, in the offshore eastern tropical Pacific 553
BROWN, R. S., and N. CAPUTI. Factors affecting the growth of undersize western
rock lobster, Panulirus cygmis George, returned by fishermen to the sea 567
JAMIE SON, G. S., and A. CAMPBELL. Sea scallop fishing impact on American lobsters
in the Gulf of St. Lawrence 575
WARLEN, STANLEY M., and ALEXANDER J. CHESTER. Age, growth, and distribu-
tion of larval spot, Leiostomus xanthurus, off North Carolina 587
ALBERS, W. D., and P J. ANDERSON. Diet of Pacific cod, Gadus macrocephalus,
and predation on the northern pink shrimp, Pandalus borealis, in Pavlof Bay,
Alaska 601
BOEHLERT, GEORGE W, DENA M. GADOMSKI, and BRUCE C. MUNDY. Vertical
distribution of ichthyoplankton off the Oregon coast in spring and summer
months 611
AU, DAVID W. K., and WAYNE L. PERRYMAN. Dolphin habitats in the eastern tropical
Pacific 623
FREEMAN, MARY C, NATE NEALLY, and GARY D. GROSSMAN. Aspects of the
life history of the fluffy sculpin, Oligocottus snyderi 645
BARLOW, JAY. Variability, trends, and biases in reproductive rates of spotted dolphins,
Stenella attenuata 657
(Continued on next page) ;
iV,b!ine Biotogfea! LahoratOfv f
FEB 7 1986 j
Seattle, Washington i I
1985
LJ^(2£^ Hole, Mass. {
For sale by the Superintendent of Documents, U.S. Government Printing Office, Washington
DC 20402— Subscription price per year: $21.00 domestic and $26.25 foreign. Cost per single
issue: $6.50 domestic and $8.15 foreign.
Contents— Continued
Notes
PETERSON, CHARLES H, R BRUCE DUNCAN, HENRY C. SUMMERSON, and
BRIAN F. BE AL. Annual band deposition within shells of the hard clam, Mercenaria
mercenaria: consistency across habitat near Cape Lookout, North Carolina 671
SULLIVAN, LORETTA E, DENNIS A. EMILIANI, and K. NEAL BAXTER. Stand-
ing stock of juvenile brown shrimp, Penaeus aztecus, in Texas coastal ponds 677
THOMAS, DAVID H. A possible link between coho (silver) salmon enhancement and
a decline in central California Dungeness crab abundance 682
FFLDKAMP, STEVEN D. The effects of net entanglement on the drag and power out-
put of a California sea lion, Zaloiphus califomiamts 692
PARSONS, GLENN R. Notes on the life history of the catshark, Scyliorhinus
meadi 695
LIBBY, DAVID A. A comparison of scale and otolith aging methods for the alewife,
Alosa pseudoharengus 696
MAULE, ALEC G., and HOWARD F. HORTON. Probable causes of the rapid growth
and high fecundity of walleye, Stizostedion vitreum vitreum, in the mid-Columbia
River 701
TAYLOR, D. M., R. G. HOOPER, and G. R ENNIS. Biological aspects of the spring
breeding migration of snow crabs, Chionoecetes opilio, in Bonne Bay, Newfoundland
(Canada) 707
CREED, ROBERT P., JR. Feeding, diet, and repeat spawning of blueblack herring, Alosa
aestivalis, from the Chowan River, North Carolina 711
Index 717
Notices
NOAA Technical Reports NMFS published during first 6 months of 1985.
The National Marine Fisheries Service (NMFS) does not approve, recommend or en-
dorse any proprietary product or proprietary material mentioned in this publication.
No reference shall be made to NMFS, or to this publication furnished by NMFS, in
any advertising or sales promotion which would indicate or imply that NMFS approves,
recommends or endorses any proprietary product or proprietary material mentioned
herein, or which has as its purpose an intent to cause directly or indirectly the adver-
tised product to be used or purchased because of this NMFS publication.
REGIONAL VARIATIONS IN THE GROWTH AND AGE COMPOSITION
OF NORTHERN ANCHOVY, ENGRAULIS MORDAX
R. H. Parrish,! D. L. Mallicoate,! and K. F. Mais^
ABSTRACT
Data from the Sea Survey Program conducted by the California Department of Fish and Game were
analyzed to describe regional variations in growth and age composition of northern anchovy, Engraulis
mordax. Juvenile growth appeared to be greater at higher latitudes and in the offshore portion of the
Southern California Bight. Adult growth was less variable; however, there were statistically significant
differences between regions. In addition, the growth rate for the southern stock was markedly lower than
that of the central stock. This difference in growth rates was used to characterize the area of overlap
between the two stocks. Age composition varied with depth of water and geographical location within
the Southern California Bight and with latitude Young-of-the-year and yearling fish were found in larger
proportions in shallow water and in the southern and inshore areas of the Southern California Bight.
Age compositions of northern anchovies sampled in the California and Mexican purse seine fisheries were
compared with those of the Sea Survey Program. This comparison suggests that the present California
area restrictions, which exclude the fishery from the nearshore area, greatly reduces the number of young
fish in the catch.
The purpose of this study is to describe regional
variations in growth and age composition of the
northern anchovy, Engraulis mordax. Data for the
study were taken by the Sea Survey Program of the
Cahfornia Department of Fish and Gama Mais
(1974) described this program and analyzed the data
for the most common species taken in the survey.
This report is an extension of Mais' work and focuses
on geographical variations in age composition and
growth rates and on depth variations in age
composition.
Meristic and morphometric (McHugh 1951) and
electrophoretic (Vrooman et al. 1981) studies on the
stock structure of the northern anchovy suggest that
there are three stocks (northern, central, and
southern) and that the boundaries between the
stocks occur in central California and central Baja
California. There is also recent evidence (Parrish^)
of a fourth stock which spawns in the fall in central
California and in the northern and offshore areas
of the Southern California Bight.
Mais (1974) showed that the southern stock of
northern anchovies was smaller at age than the cen-
tral stock. In addition, northern anchovies are known
'Southwest Fisheries 'Center Pacific Fisheries Environmental
Group, National Marine Fisheries Service, NOAA, P.O. Box 831,
Monterey, CA 93942.
^California Department of Fish and Game, 1301 West 12th Street,
Long Beach. CA 90813.
^Parrish, R. H. 1983 Evidence for a fall spawning anchovy
stock. Paper presented at 1983 CalCOFI Conference
Manuscript accepted January 1985.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
to be larger off central California than off southern
California (Collins 1969; Mais 1974; Mallicoate and
Parrish 1981), and they are larger in the offshore
areas of the Southern California Bight than in the
inshore areas (Mais 1974). These differences could
be due to varying growth rates between regions,
varying seasonality of spawning, varying age com-
positions, size-specific migration, or a combination
of these factors.
Tkgging experiments have shown that northern an-
chovies move from southern California to central
California, from central California to southern
California, and from southern California to
Ensenada, Mexico; there is a northerly movement
in summer and a southerly movement in winter
(Haugen et al. 1969). Mais (1974) found northern an-
chovies to be distributed more offshore in some years
and more inshore in other years, and he found them
concentrated closer to shore and in the northern part
of the Southern California Bight during the fall
months. Mais (1974) suggested that northern an-
chovies begin an offshore and southeastward move-
ment in late winter, which coincides with the onset
of major spawning activity. These movements of
anchovy may affect the measurement of growth
rates and age compositions within the different
regions.
METHODS
The data used in the study were taken from north-
483
FISHERY BULLETIN: VOL. 83. NO. 4
ern anchovies caught by midwater trawl. The gear
and sampling procedures are described by Mais
(1974). The data set covers the period 1966-1983 and
consists of 101 cruises. Twenty-three cruises extend-
ed north of Point Conception, 77 cruises occurred
in southern California and northern Baja California,
and 8 cruises extended into southern Baja Califor-
nia. Several cruises extended into more than one
region. There were a total of 4,166 trawl hauls, of
which 3,017 contained anchovies. Standard lengths
were normally taken from about 25 anchovies in each
trawl haul in which they occurred; otoliths, for
aging, were usually taken from a subsample of up
to 10 fish. A total of 60,082 northern anchovies were
measured, of which 20,772 were aged by California
Department of Fish and Game personnel with
methods developed by Collins and Spratt (1969).
For purposes of determining age composition and
growth rates of northern anchovies, it was assumed
that February was the birth month of all fish sam-
pled. Anchovies off California and Baja California
have a peak in spawning in February- March; however,
some spawning does occur all year (Ahlstrom 1966).
The age determinations used in this report are, of
course, not accurate to the month. They are based
on the number of annuli, the seasonality of annuli
formation, an assumed February birth month, and
the month the fish were caught. Annuli formation
occurs in May in California (Collins and Spratt 1969).
A 1-yr-old anchovy would therefore be an anchovy
caught in February with no annuli on its otoliths.
A lV2-yr-old anchovy would be a fish with one an-
nuli which was caught in August. An anchovy born
in February would be 15 mo old when its first an-
nuli was formed. An anchovy spawned in September
would be 8 mo old if it formed its first annuli in its
first May and 20 mo old if it formed its first annuli
in its second May.
Differences in growth between geographical
regions were compared by linear regression analyses
which included anchovies of 1 V2 yr of age and older.
Evaluation of the relationship between age composi-
tion and water depth in the area of capture was made
by grouping the samples into depth strata. The strata
were established partially on the number of
observations.
lb determine growth rates, the data were process-
ed with a computer program (Mallicoate and Par-
rish 1981) which calculates and plots the mean
length, standard deviation of length, and length
range by age and month. The program also tabulated
the number of observations by age and month; these
data were used for determining age composition.
Our preliminary analysis of the sea survey data
showed an alongshore cline in the mean length of
northern anchovies (Fig. 1). It also revealed a bias
in the selection of fish to be aged. Aged fish were
generally larger at all latitudes than were the un-
aged fish. This bias is apparently due to a consis-
tent tendency for samplers to pick larger anchovies
for the subsample which was aged. Anchovies < 100
mm SL were particularly susceptible to not being
selected for aging (Tkble 1). On checking with the
field biologists who took the data, we found a second
source of bias which occurred only in trawl hauls of
exclusively small fish. When trawl hauls were con-
sidered by the sampler to be "obviously" all young-
of-the-year fish, there was a tendency not to take
otoliths for age determination. These sampling
biases affect the analyses of age composition
presented in this report but do not affect the grow^th
analyses.
Table 1.— Two types of length bias in sampling northern anchovies in the Sea
Survey Program.
No. fish
Standard
measured in
No.
length
No. fish
hauls sampled
otolith
(mm)
measured
for otoliths
samples
iBias 1
2Bias 2
<70
2,174
1,275
460
0.59
0.36
70-80
2,366
1,939
684
0.82
0.35
80-90
4,667
4,241
1,667
0.91
0.39
90-100
7,077
6,367
2,498
0.90
0.39
100-110
8,988
7,875
2,997
0.88
0.38
110-120
12,058
10,834
4,164
0.90
0.38
120-130
1 1 ,744
10,462
4,215
0.89
0.40
130-140
7,390
6,456
2,748
0.87
0.43
140 +
3,619
3,036
1,339
0.84
0.44
Total
60,082
52,484
20,772
'Bias 1 is the decision to sample for otoliths (i.e., the proportion of fish in trawl hauls which
were sampled for otoliths).
^Bias 2 is the selection of larger fish by the sampler (i e., the proportion of fish in trawl hauls,
which were sampled for otoliths, for which otolith samples were taken).
484
PARRISH ET AL.: REGIONAL VARIATIONS IN NORTHERN ANCHOVY
140-
FlGURE 1.— Mean length of aged and unaged
northern anchovies and the number of an-
chovies by half degree of latitude
30
LATITUDE
The data were inadequate to calculate growth
curves or age composition on the one-half degree of
latitude interval used in Figure 1; therefore, geo-
graphical regions were selected based partially on
the number of observations. For example, the
southern and central Baja California and central
California areas, which had fewer samples, were
more widely spaced than the southern California and
northern Baja California areas. Nearly all of the an-
chovy samples taken south of lat. 32°N or north of
lat. 34°N were taken within one-half degree of the
coast. The lat. 32°-34°N area included a large amount
of samples taken further than one-half degree from
the coast. This area, the Southern California Bight,
contains numerous islands and basins; we, therefore,
divided it into regions which approximate the natural
basins described in Emery (1954) (Fig. 2).
RESULTS
Growth
Earlier studies on northern anchovies from British
Columbia (Pike 1951), northern California
(Waldvogel 1977), central California (Clark and
Phillips 1952), and southern California (Spratt 1975)
showed considerable variation in their growth (Fig.
3A). Anchovies in British Columbia, lat. 49°N, and
northern California, lat. 41°N, are of the northern
stock (Vrooman et al. 1981) and have a summer
spawning season. Anchovies in southern California,
lat. 33 °N, are of the central stock, whereas those in
central California, lat. 36°N, are considered to be
a mixture of northern and central stocks (Vrooman
et al. 1981); anchovies in both southern and central
California have a late winter (February-April) spawn-
ing season (Parrish footnote 3). Anchovies in British
Columbia were the fastest growing of all the four
areas in their first year of life, whereas anchovies
in northern California were the slowest. Anchovies
in central and southern California showed similar
growth rates after their first year of life; however,
the growth rate of anchovies in central California
was greater than the growth rate of those in
southern California in their first year.
Our study shows that the growth of anchovies has
a distinct geographical pattern. Anchovies sampled
in the Central California region (CC) and the off-
shore area of the Southern California Bight [i.&, San
Nicolas (SN) and Tknner and Cortez Banks (TCB)
regions] have the fastest juvenile growth (Fig. 3). An-
chovies in these areas attain an average length of
120 mm before they are IV2 yr old. In the inshore
areas of the Southern California Bight and in Baja
California there is a continuous decline in the growth
rate associated with decreasing latitude (Figs. 3, 4).
Anchovies reach a mean length of 120 mm at about
age 2 in the Santa Barbara Channel region (SBC)
485
FISHERY BULLETIN: VOL. 83, NO. 4
NO"
125" 120" II5» 110"
Figure 2.— Geographical regions for which the growth and age composition of northern anchovies were determined.
and in the remaining offshore region, Catalina Basin
(CB). In the San Pedro Channel (SPC), Coronado
Escarpment (CE), and Ensenada (E) regions an-
chovies reach 120 mm at about age 3. In the Cape
San Quentin (CSQ) and Sebastian Viscaino Bay
(SVB) regions anchovies reach 120 mm at about age
4 or later.
The Cape San Quentin (CSQ), Sebastian Viscaino
Bay (SVB), and Southern Baja California (SB)
regions include anchovies from both the central and
southern stocks, and there are marked differences
in their grov^h (Fig. 4). Anchovies from the southern
stock appear to reach an asymptotic mean size of
about 92 mm, whereas those from the central stock
continue to grow throughout their lives. Note the oc-
currences of 2- to 4-yr-old fish with monthly mean
lengths of about 92 mm (Fig. 4 CSQ, SVB, SB).
Assuming that stocks can be identified by size at age,
the Cape San Quentin region appears to be
dominated by the central stock; however, the
486
PARRISH ET AL.: REGIONAL VARIATIONS IN NORTHERN ANCHOVY
3 4 5
nCE (YERRS)
3 4
RGE (YERRS
Figure 3— Age-length relationships of northern anchovies taken in A. Earlier studies 1) British Columbia (Pike 1951), 2) Central Califor-
nia (Clark and Phillips 1952), 3) Northern California (Waldvogel 1977), and 4) Southern California (Spratt 1975), CC. Central Califor-
nia; SN, San Nicolas; TCB, Tknner and Cortez Banks; CB, Catalina Basin; SBC, Santa Barbara Channel.
487
FISHERY BULLETIN: VOL. 83, NO. 4
3 4 5
AGE (YEARS)
3 4 5
RGE (YEARS)
Figure 4.— Age-length relationships of northern anchovies taken in SPC, San Pedro Channel; CE, Coronado Escarpment; E,
Ensenada; CSQ , Cape San Quentin; SVB, Sebastian Viscaino Bay; and SB, Southern Baja California.
488
PARRISH ET AL.: REGIONAL VARIATIONS IN NORTHERN ANCHOVY
southern stock does extend into this region. The
most northerly trawl sample which could be iden-
tified, by size at age, as southern stock was a June
1971 sample taken at lat. 30.3°N. Southern and cen-
tral stock anchovies broadly overlap in the Sebas-
tian Viscaino Bay region; however, the region is
occupied principally by the southern stock in the
summer and by the central stock in the fall and
winter. The Southern Baja California region is
dominated by the southern stock; however, central
stock anchovies, as identified by size at age, were
taken as far south as lat. 26.5°N in November 1967.
The fact that the central stock is the farthest south
in winter and the southern stock the farthest north
in summer suggests that the separation of the stocks
is aided by different environmental preferences,
possibly temperature
The Central California region is an area of overlap
between the northern and central anchovy stocks.
In addition, as previously mentioned (Parrish foot-
note 3), a fall spawning stock may occur in central
California and the offshore areas of the Southern
California Bight. Vrooman et al. (1981) did not have
any samples south of Monterey in central Califor-
nia or from the offshore and northern areas of the
Southern California Bight. Samples from these areas
may consist of a mixture of different stocks with dif-
ferent spawning seasons. Our assumption of a
February birth month in these areas must therefore
be evaluated.
Regression Analysis
Growth in length of anchovies in the size range
sampled by the Sea Survey Program (i.&, 40-180 mm
SL) can be divided into two phases. The early,
juvenile phase extends until the fish are about 1 yr
old. Methot (1981) found that in the Southern
California Bight juvenile growth averages about 9
mm/mo, and it is at a maximum when the fish are
between 40 and 50 mm SL. The second, adult phase
extends from a little over 1 yr old until death. Growth
during this phase is more than an order of magni-
tude less than the early phase (i.e, 0.48-0.69 mm/mo).
Examination of the age-length relationships (Figs.
3, 4) in the central stock shows that growth in the
adult phase is essentially linear. Therefore, we used
linear regressions to compare growth of anchovies
from different regions. These analyses included
only fish of IV2 yr of age and older. This model has
several advantages for comparing the growth dur-
ing the two phases described above. By limiting the
model to the linear segment of the age-length rela-
tionships, the slopes of the regressions can be used
to compare the regional variations in growth rate
during the adult phase Another advantage is that
the expected length at 172 yr of age can be used to
compare regional variation in growth during the
juvenile phase
Juvenile Growth
In the area occupied by the central stock, growth
during the juvenile phase shows considerable varia-
tion among regions. There were significant dif-
ferences in growth to age IV2. Fastest growth oc-
curred in the north, and the slowest was in the south
(Tkble 2, Fig. 5). Mean standard length at IV2 yr of
age was 123.6 mm in the Central California region,
113.4 mm in the San Pedro Channel region, and
103.6 mm in the Cape San Quentin region. The three
southernmost Baja California regions contain mix-
tures of the central and southern stocks; therefore,
data from these regions were divided into central
and southern stock sets, based on length and month,
for the analyses. In contrast to those of the central
stock, anchovies of the southern stock attain only
91.8 mm by age IV2. Within the Southern Califor-
nia Bight there is also an inshore-offshore gradient,
with faster juvenile growth in the offshore regions
and slower grov^th in the inshore regions (i.e, lengths
at age IV2 in the Coronado Escarpment, Catalina
Basin, and Tanner and Cortez Banks regions were
110.5, 116.4, and 119.2 mm respectively).
An analysis of covariance showed that the dif-
ferences in size at age IV2 are not significantly dif-
ferent {a = 0.01) in two pairs of regions. The San
Nicolas region (120.4 mm at age IV2) and the Ikn-
ner and Cortez Banks region (119.2 mm) are the first
pair, and the Catalina Basin region (116.4 mm) and
the Santa Barbara Channel region (116.2 mm) are
the second pair. In all other pairs of regions, size at
age IV2 is significantly different at the a = 0.0001
level.
Adult Growth
The regressions demonstrate that growth during
the adult phase is relatively constant between the
different regions occupied by the central stock, with
slopes varying from a low of about 6 mm/yr to a high
of about 8 mm/yr (Ikble 2). In contrast, anchovies
of the southern stock have essentially no adult
growth after age IV2 (i.e, slope = 0.07 mm/yr).
Although the differences in adult growth between
regions is not large, there are statistically significant
differences (Tkble 3). The San Nicolas region and the
Tknner and Cortez Banks region have adult growth
489
FISHERY BULLETIN: VOL. 83, NO. 4
Table 2.— Regression parameters and statistics for the relationship between age and
length of northern anchovies older than IV2 yr: Central California (CC), San Nicolas
(SN), Tanner-Cortez Banks (TCB), San Nicolas combined with Tanner-Cortez Banks
(SN+TCB), Catalina Basin (CB), Santa Barbara Channel (SBC), Catalina Basin com-
bined with Santa Barbara Channel (CB+SBC), San Pedro Channel (SPC), Coronado
Escarpment (CE), Ensenada (E), Cape San Quentin (CSQ), Sebastian Viscaino Bay
and Southern Baja California, central stock only (SVB+SB), and Southern Baja Califor-
nia, southern stock only (S).
Mean
Mean
Length at
Adult
SD of
SDof
age
length
age IV2
growth
length at
adult
Area
(Yr)
(SL mm)
(SL mm)
(mm/yr)
r
age Vh
growth
N
Central Stock
CC
3.4
138.4
123,6
7.75
0.702
1,563
0.431
335
SN
3.3
131.1
120.4
5.97
0.613
0,713
0.205
1,410
TCB
3.2
130.8
119.2
6.69
0.623
0,975
0.286
860
SN+TCB
3.3
131.0
120.0
6.23
0.616
0,577
0.167
2,270
CB
3.1
126.7
116.4
6.29
0.582
0,633
0.192
2,092
SBC
2.9
125.6
116.2
6.83
0.636
0,689
0.224
1,374
CB-hSBC
3.0
126.3
116.4
6.50
0.606
0,465
0.145
3,466
SPC
2.8
121,3
113.4
6.07
0.575
0,435
0.146
3,497
CE
2.7
118.7
110.5
6.89
0.569
0.666
0.235
1,798
E
2.8
116.5
106.2
8.08
0.636
0.944
0.321
934
CSQ
2.5
111.1
103.6
7.54
0.649
0.776
0.291
923
SVB+SB
2.4
106.4
101.1
5.76
0,443
1.571
0.618
358
Southern Stock
8'
2.9
91.9
91.8
0.07
0.009
1.274
0.421
335
'Combined from three areas: CSQ, SVB, and SB.
150-
140-
J 130 H
5 120 H
o
^ 110 H
100-
90-
3
AGE
6
Figure 5.— Linear regressions showing the expected length at age (Tkble
1) of northern anchovies taken in CC, Central California; SN, San
Nicolas; TCB, Tknner and Cortez Banks; CB, Catalina Basin; SBC,
Santa Barbara Channel; SPC, San Pedro Channel; CE, Coronado
Escarpment; E, Ensenada; CSQ, Cape San Quentin; SVB + SB, Se-
bastian Viscaino Bay and Southern Baja California, central stock only;
and S, Southern Baja California, southern stock only.
490
PARRISH ET AL.: REGIONAL VARIATIONS IN NORTHERN ANCHOVY
patterns which are not statistically different (a =
0.01), and since the two regions are adjacent we have
considered them together. Also there is no signi-
ficant difference (a = 0.01) in adult growth in the
Catalina Basin and the Santa Barbara Channel
regions, but since these regions are geographically
separated we have retained them as separate
regions. The relatively large standard deviations of
the regression slopes (Ikble 2) for fish from the Cen-
tral California and the Sebastian Viscaino Bay and
the Southern Baja California regions may indicate
that these regions are the most likely to have mix-
tures of more than one stock.
There was no significant difference {a = 0.01) be-
tween growth of adults in the best growth regions
(Ensenada, Cape San Quentin, and Central Califor-
nia). The difference between the Coronado Escarp-
ment and the Santa Barbara Channel regions is not
significant at the a = 0.1 level nor are the differences
between the Catalina Basin, combined San Nicolas-
Tknner and Cortez Banks, San Pedro Channel, and
combined Sebastian Viscaino Bay and Southern Baja
California regions.
Tknner and Cortez Banks, and Catalina Basin) dif-
fer from the other regions in that they are dominated
by fish 3 yr and older (Fig. 6A, Tkble 4). Central
California and Tknner and Cortez Banks also have
substantial percentages of young-of-the-year fish,
whereas the other two regions do not.
Anchovies in the three inshore regions of the
Southern California Bight (Santa Barbara Channel,
San Pedro Channel, and the Coronado Escarpment)
have very similar age compositions (Fig. 6B, Tkble
4). One- and two-yr-old fish are the most numerous
in these three regions. Young-of-the-year and 3 yr-
olds are slightly less abundant than 1- and 2-yr-olds,
and there are fewer older fish in the samples.
Baja California is characterized by a dominance
of young fish (Fig. 6C, Ikble 4). The age composi-
tions in the Ensenada, Cape San Quentin, and Sebas-
tian Viscaino Bay regions are very similar; young-
of-the-year and 1-yr-old fish are the most abundant,
and there is rapid decrease in the abundance of fish
with increasing age. Anchovies in southern Baja
California are principally from the southern stock.
The age composition in this region shows a pre-
Table 3. — Significance levels for differences in growth of adult northern anchovies from different geographical
regions: Ensenada (E), Central California (CC), Cape San Quentin (CSQ), Coronado Escarpment (CE), Santa Barbara Chan-
nel (SBC), Tanner and Cortez Banks (TCB), Catalina Basin (CB), San Nicolas combined with Tanner and Cortez Banks (SN+TCB),
San Pedro Channel (SPC), San Nicolas (SN), Sebastian Viscaino Bay and Southern Baja California, central stock only (SVB+SB),
and Southern Baja California, southern stock only (S). Geographic areas are arranged in order from largest to smallest slopes.
Area
E
CC
CSQ
CE
SBC
TCB
CB
SN+TCB
SPC
SN
SVB+SB S
E
CC
0.5573
CSQ
0.2217
0.6517
—
CE
0.0019
0.0514
0.0754
—
SBC
0.0015
0.0477
0.0629
0.9422
—
TCB
0.0013
0.0331
0.0384
0.6516
0.6951
—
CB
0.0000
0.0000
0.0000
0.0605
0.0628
0.2400
—
SN+TCB
0.0000
0.0003
0.0002
0.0283
0.0280
0.0000
0.8141
—
SPC
0.0000
0.0000
0.0000
0.0015
0.0033
0.0465
0.3560
0.4659
—
SN
0.0000
0.0000
0.0000
0.0042
0.0042
0.0367
0.2547
0.3234
0.6902
—
SBV + SB
0.0000
0.0085
0.0051
0.0826
0.0952
0.1616
0.3943
0.4372
0.6048
0.7379
—
8
0.0000
0.0000
0.0000
0.0000
0.0000
0.0000
0.0000
0.0000
0.0000
0.0000
0.0000 —
Age Composition by Area
Geographical variation in age composition is one
factor which could influence the observed variation
in mean size of anchovies in the various regions;
therefore, age composition was calculated for each
of the regions used earlier (Fig. 2). Few anchovies
< 60 mm SL occur in the data, and it appears that
young-of-the-year fish are apparently not susceptible
to capture by the midwater trawl gear used in the
sea survey until they are about 6 mo old.
Central California and the three offshore regions
within the Southern California Bight (San Nicolas,
ponderance of 1-yr-olds, and like the other Baja
California regions there are few fish of age 4 or older.
Age Composition by Depth Strata
Anchovies primarily live within the upper mixed
layer; they occur in the surface layer over the con-
tinental shelf and over deepwater regions. Mais
(1974) showed that the average size of anchovies
sampled in offshore areas was greater than that of
anchovies sampled near the coast. The percentage
of trawl hauls containing anchovies was quite con-
stant in areas with different water depths, varying
491
FISHERY BULLETIN: VOL. 83, NO. 4
50-
40-
30-
B
1^
0
1 — I — I —
2 3 4+
0
I r
I 2
AGE
n — I —
3 4 +
1^
0
n 1 r
2 3 4+
Figure 6.— Age composition of northern anchovies taken in the following geogra-
phical regions: A. Central California and offshore areas of the Southern California
Bight; Central California (CC), San Nicolas (SN), Tknner and Cortez Banks (TCB),
and Catalina Basin (CB); B. Inshore areas of the Southern California Bight; Santa
Barbara Channel (SBC), San Pedro Channel (SPC), and Coronado Escarpment (CE);
C. Baja California; Ensenada (E), Cape San Quentin (CSQ), Sebastian Viscaino Bay
(SVB), and Southern Baja California (SB).
Table 4. — Percentage age composition of northern an-
chovies by geographical region: Central California (00),
San Nicolas (SN), Tanner-Cortez Banks (TOB), Oatalina
Basin (OB), Santa Barbara Channel (SBC), San Pedro
Channel (SPO), Coronado Escarpment (OE), Ensenada
(E), Cape San Quentin (CSQ) Sebastian Viscaino Bay
(SVB), Southern Baja California (SB).
Age
No.
fish
Area
0
1
II
III
IV
V
Vl-i-
CC
19.3
17.2
14.7
23.9
17.7
5.7
1.6
436
SN
5.6
15.5
27.7
26.0
15.9
7.4
2.0
1,721
TOB
12.6
12.6
24.3
28.3
13.6
6.5
2.1
1,136
OB
3.7
18.7
29.2
29.2
12.8
5.2
1.1
2,538
SBC
21.8
29.6
22.2
15.2
8.2
2.4
0.6
1,989
SPO
21.6
28.6
25.4
15.6
6.3
1.9
0.5
5,439
OE
23.5
28.1
26.9
14.6
5.4
1.3
0.2
2,965
E
25.8
23.6
23.4
17.1
7.6
2.3
0.2
1,464
CSQ
33.8
33.7
15.5
11.2
4.4
1.2
0.1
1,779
SVB
38.1
30.8
12.8
13.5
4.5
0.3
—
896
SB
18.8
45.7
19.6
11.5
3.7
0.7
—
409
between 64 and 77% (Ikble 5). This is probably in-
fluenced by the fact that trawling (in the upper 30
m) was carried out normally in areas where fish
schools had already been detected by depth recorder
or sonar.
In southern California (lat. 32°-34°N) young-of-the-
year anchovies comprise more than one-half of the
anchovies sampled in the 5-25 fathom-depth stratum
(Tkble 6A). One- and two-yr-olds comprise more than
one-half of the anchovies in the 26-50, 51-150,
151-300, and 301-500 fathom strata. The most abun-
dant age group in the 26-50 stratum is age 1; there
are essentially equal numbers of age 1 and age 2 an-
chovies in the 51-150 and 151-300 strata; 2-yr-olds
are the most abundant age group in the 301-500
stratum; and 3-yr-olds are the most abundant age
group in the 701-1- stratum. Age groups 3-6-f- each
show an increasing percentage with increasing
depth. Collectively they comprise about 11% of the
5-25 stratum, 31% of the 51-150 stratum, and 51%
of the 701 -f- stratum. The same general pattern oc-
curs in northern Baja California (lat. 29.5°-32°N);
however, the percentage of young fish declines more
Table 5.— Percentage of mid-
water trawl hauls taking north-
ern anchovies by depth strata.
Trawl hauls were normally with-
in 30 meters of the surface.
% sets
Total
with
Depth (fm)
sets
anchovies
5-25
704
75
26-50
828
69
51-150
554
69
151-300
546
76
301-500
752
77
501-700
437
73
701 -^
345
64
Total
4,166
72
492
PARRISH ET AL.: REGIONAL VARIATIONS IN NORTHERN ANCHOVY
Table 6. — Age composition (%) of northern anchovies taken in shallow and deep-
water areas (depth in fathonns).
A
Depth:
Lat. 320-340N
1
Age
5-25
26-50
51-150
151-300 301-500
501-700
701 +
0
56.5
26.3
16.9
7.8
5.5
3.0
6.5
1
20.6
29.5
26.5
27.4
25.8
17.9
15.5
II
12.5
24.1
26.0
27.9
30.6
32.0
26.8
III
7.0
12.3
20.1
22.8
22.7
28.2
27.1
IV
2.5
5.8
6.8
9.1
10.5
13.3
15.3
V
0.8
1.5
3.2
3.6
3.8
4.9
7.2
VI +
0.2
0.5
0.6
1.4
1.1
0.6
1.7
n
1,579
1,492
1,102
2,199
3,704
2,091
1,086
B
Depth:
Lat. 29.50-320N
Age
5-25
26-50
51-150
151 +
0
1
56.1
23.1
36.8
40.4
21.0
28.5
8.9
28.8
II
12.3
10.8
24.2
26.9
III
6.2
7.8
14.2
23.3
IV
1.9
3.6
9.4
8.7
V
0.3
0.6
2.5
3.0
VI +
—
—
0.2
0.3
n
935
619
480
1,189
C Aug.-Dec,
Depth:
Lat. 29.50-32''N
Lat.
320-340N
Age
5-25
26-50
51-150
151 +
5-25
26-50
51-150
151-300
0
62.8
52.6
38.7
24.9
66.2
37.8
26.4
16.0
1
18.2
32.3
29.2
43.0
15.6
29.0
24.7
21,0
II
11.7
10.6
19.9
24.4
12.1
22.5
25.8
32.4
III
5.7
4.0
8.2
6.4
5.0
8.6
16.1
21.2
IV
1.6
0.5
4.1
1.2
0.9
2.0
5.1
8.3
V
—
—
0.7
—
0.2
0.1
1.8
0.9
VI +
—
—
—
—
—
—
—
0.2
n
806
378
267
405
1,286
1,013
546
990
slowly with increasing depth there than in southern
California (Tkble 6B). In both southern California
and northern Baja California, there is a direct rela-
tionship between average age and depth of water in
which fish were caught. In the period August-
December when smaller (< 60 mm) anchovies can
be caught by midwater trawls, there is a greater
dominance of young-of-the-year fish in the shallower
water (Tkble 6C). In the northern Baja California
area, 63% of the 5-25 stratum and 53% of the 25-50
stratum were young-of-the-year fish. In southern
California the corresponding percentages were 66
and 38.
Sea Survey - Fishery Comparisons
The purse seine fleets which harvest anchovies
operate primarily out of San Pedro, California, and
Ensenada, Mexico. The age composition of anchovies
in the San Pedro fishery (Mallicoate and Parrish
1981) contains a smaller proportion of age 0 and age
1 fish than does the sea survey data for the San
Pedro Channel region. We only had 2 years of age
composition data for the Ensenada fishery available
to us (Sunada and Silva 1980), but this limited in-
formation shows the same dominance of younger an-
chovies as in the sea survey data for this region. The
San Pedro fishery had several regulations which
reduced the numbers of young fish in the catch.
These included a 5-in minimum size limit and a series
of area closures which prevent the fleet from fishing
in nearshore areas. The Ensenada fishery did not
have regulations which influenced the age composi-
tion of the catch.
Tb evaluate the effects of the area closures and size
limit on the San Pedro fishery, we broke the sea
survey data into depth classifications, < 50 fathoms
and > 50 fathoms. The > 50 fathom classification
was intended to approximate the area of the fishery
(i.e, the coastal strip is excluded). In this area the
493
FISHERY BULLETIN: VOL. 83, NO. 4
age composition of anchovies taken by the Sea
Survey Program is very close to that taken by the
fishery; conversely, the age composition of the
fishery is unlike that taken in areas < 50 fathoms
(Fig. 7). The California fishery no longer has a 5-in
size limit; however, the closure of the nearshore area
appears to be the dominant factor in reducing the
catch of young anchovies.
<50fm
\kr ^^\ FISHERY
30-
§20-
1 \ '\ >50(m
UJ
a.
.1 \ ^ .
10-
fl \\.
1 \\\
! >v ••
0 1
2 3 4
AGE
5 6+
Figure 7.— Comparison of the age com-
position of northern anchovies taken in
the San Pedro purse seine fishery with
those taken in areas with <50 fathoms
and >50 fathoms of water in the mid-
water trawl Sea Survey Program.
DISCUSSION
Our data show that the growth rate and the age
composition of northern anchovies vary geographi-
cally. The greatest differences in growth appear to
occur during the juvenile stage; growth in adults
shows much less regional variation. Juvenile growth
is greatest in central California and in the offshore
areas of the Southern California Bight. In the in-
shore regions there is a trend toward reduced
juvenile growth from central California to southern
Baja California. Average size at age IV2 falls from
123.6 mm to 91.8 mm over this area. Growth in adult
anchovies appears to be the greatest in northern
California, and it is also relatively high in British
Columbia (Pike 1951), central California, and north-
ern Baja California. Adult growth appears to be
relatively low in the Southern California Bight; this,
however, may be an artifact as this area probably in-
cludes resident fish plus slower growing fish which
have moved into this region from the south. Age com-
position showed a large variation among regions, and
the pattern of this variation appears to be closely
related to the gyral circulation within the Southern
California Bight. There is also a strong relationship
in age composition to the depth of water at trawl
sites. Adult anchovies dominated the catches in the
offshore, deepwater regions of the Southern Califor-
nia Bight and in central California. Age also had a
strong latitudinal gradient with adult fish domi-
nating in the north and young-of-the-year and year-
ling fish dominating in the shallow water areas off
central and northern Baja California. Adult an-
chovies appear to be concentrated in areas of the
Bight where prevailing currents will result in
southerly and inshore larval transport (Parrish et al.
1981). At recruitment, anchovies appear to be heavily
concentrated in shallow water, and young fish ap-
pear to be concentrated in the nearshore area where
they will tend to be advected northward by the
southern California gyra
As vidll be discussed later, the interpretation of the
regional differences in juvenile growth is dependent
upon the stock structure in the various regions.
Earlier studies (McHugh 1951; Vrooman et al. 1981)
showed that the boundary between the southern and
central stocks was in the northern Sebastian Vis-
caino Bay area. This is supported by the present
study, and, as previously mentioned, the boundary
is further north in the summer and fall and further
south in winter and spring. We feel that there is am-
ple evidence that the southern stock had the smallest
juvenile growth rate and that growth during the
adult phase is minor. Vrooman et al. (1981) suggested
that the boundary between the northern and cen-
tral stocks occurs in the central California area; both
northern and central stocks occurred in samples
taken at San Francisco (lat. 37°50'N) and Monterey
(lat. 36°50'N). Their data might be interpreted to
suggest that a fourth stock occurred in the San Fran-
cisco and Monterey samples, and in addition it has
been suggested (Parrish footnote 3) that this fourth
stock spawns during the fall in central California and
the offshore areas of the Southern California Bight.
Unfortunately the Vrooman et al. (1981) study did
not have any samples from the region between
Monterey (lat. 36°50'N) and Newport (lat. 33°30'N),
nor were there any samples from the offshore areas
of the Southern California Bight. It is therefore not
presently possible to determine the amount of stock
mixture over much of the accepted range of the cen-
tral stock.
Variation in juvenile growth of northern anchovies
in the different regions may be due to genetic fac-
tors, differences in the seasonality of spawning, or
environmental factors. The northern stock has a
relatively short spawning season with a strong peak
in July (Richardson 1980). The central stock has a
494
PARRISH ET AL.: REGIONAL VARIATIONS IN NORTHERN ANCHOVY
more extended spawning season with a broad peak
from February to April, and there is some spawn-
ing all year in the central stock region. It is not yet
known if the anchovies that spawn in central and
southern California during the summer and fall are
from the central stock, northern stock, or a possi-
ble fall spawning stock. If the anchovies in this
region are predominatly from the central stock, the
relatively high juvenile growth in central California
and the offshore portion of the Bight might be due
to a favorable feeding environment. Offshore por-
tions of the Southern California Bight have been
shown to have considerably more plankton and
nutrients than the inshore portions (Reid et al. 1958;
Owen 1980). If the anchovies in the area occupied
by the central stock have a large component that are
not central stock, the increased juvenile growrth could
be due to the genetic differences, due to environmen-
tal differences, or caused by the assumption of a
February birth month. At our "assumed" age of IV2
yr, an anchovy spawned in the fall would be about
6 mo older than the "normal" central stock anchovy.
If the growth that occurred during these additional
5 mo was at the normal adult rate (i.e, 0.48-0.69
mm/mo), there would be only a 2-4 mm difference
in the size of the two fish. However, the difference
in mean length between lV2-yr-old anchovies in the
central California and Cape San Quentin regions is
20 mm. If, however, growth during the 5 mo is even
one-half of the average juvenile rate (i.e, 9 mm/mo)
the difference in size at "IV2" yr could be achieved.
CONCLUSION
The interpretation of regional variations in the
growth and age composition of northern anchovies
in the area between central California and central
Baja California and the implications of this study for
fisheries management are dependent upon the stock
structure of the anchovies in the area.
If a significant proportion of these fish are not
from the central stock, this study suggests the
following:
1. The observed regional variation in age composi-
tion may be the result of mixtures of stocks with
different mortality rates.
2. The juvenile growth rate of anchovies in the cen-
tral stock is lower than that of anchovies from
the northern stock(s). The reason for this lower
growth rate could be either genetic, environ-
mental, or dependent upon the seasonality of
spawning.
3. The southern California and Mexican fisheries
are based on different stock mixtures, and thus
the interactions between these fisheries would
not be as great as they would be if both were
based entirely on the same stock.
If essentially all of these anchovies are from the
central stock, this study suggests the following:
1. The offshore regions of the Southern California
Bight contain a disproportionate share of the
adult anchovies; however, recruitment does not
occur here to any significant extent.
2. Recruitment occurs largely in shallow water
along the coast, and the northern Baja Califor-
nia region has the largest percentage share of
young-of-the-year anchovies.
3. Larvae and juveniles recruited from the offshore
regions of the Southern California Bight tend
to move or be advected south and inshore
4. The relatively high juvenile growth rates in cen-
tral California and the offshore regions of the
Southern California Bight are due to favorable
environmental conditions.
5. As they grow older anchovies tend to move, or
be advected, north and offshore
6. Mixing of adults is not complete; otherwise
length at age and age composition would be the
same everywhere
7. Due to the inferred tendency for recruitment to
occur in the south, an extensive fishery on the
central stock would reduce the proportion of
older anchovies and result in fewer older an-
chovies in the northern and offshore areas.
8. The combination of the large Mexican fishery,
which has been associated with a reduction in
the proportion of older anchovies (Mais 1982),
and the continued closure of the nearshore areas
where younger fish are concentrated will severe-
ly impact the California fishery.
ACKNOWLEDGMENTS
We are grateful to Roy Mendelssohn, Alec Mac-
Call, Janet Mason, and Rick Methot for their com-
ments and editorial assistance In addition we wish
to thank Susie Myers for her help in completing the
manuscript.
LITERATURE CITED
Ahlstrom, E. H.
1966. Distribution and abundance of sardine and anchovy lar-
vae in the California Current Region off California and Baja
California, 1951-64: A summary. U.S. Fish Wildl. Serv., Spec
Sci. Rep.-Fish. 534, 71 p.
495
FISHERY BULLETIN: VOL. 83, NO. 4
Clark, F. N., and J. B. Phillips.
1952. The northern anchovy (Engraulis mordax) in the
California fishery. Calif. Fish Game 38:189-207.
Collins, R. A.
1969. Size and age composition of northern anchovies
{Engraulis mordax) in the California anchovy reduction
fishery for the 1965-66, 1966-67, and 1967-68 seasons. Calif.
Dep. Fish Game Fish Bull. 147:56-74.
Collins, R. A., and J. D. Spratt.
1969. Age determination of northern anchovies, Engraulis
mordax, from otoliths. Calif. Dep. Fish Game Fish Bull.
147:39-55.
Emery, K. 0.
1954. Source of water in basins off southern California. J.
Mar. Res. 13:1-21.
Haugen, C. W., J. D. Messersmith, and R. H. Wickwire.
1969. Progress report on anchovy tagging off California and
Baja California, March 1966 through May 1969. Calif. Dep.
Fish Game Fish Bull. 147:75-89.
Mais, K. F
1974. Pelagic fish surveys in the California Current. Calif.
Dep. Fish Game Fish Bull. 162:1-79.
1981. Age-composition changes in the anchovy, Eng^-aulis
mordax, central population. Calif. Coop. Oceanic Fish. In-
vest. Rep. 22:82-87.
Mallicoate, D. L., and R. H. Parrish.
1981. Seasonal growth patterns of California stocks of north-
ern anchovy, Engraulis mordax. Pacific mackerel. Scomber
japonicus, and jack mackerel, Trachurus symmetri-
cus. Calif. Coop. Oceanic Fish. Invest. Rep. 22:69-81.
McHuGH, J. L.
1951. Meristic variations and populations of northern anchovy
{Engraulis mordax mordax). Bull. Scripps Inst. Oceanogr.
6:123-160.
Methot, R., Jr.
1981. Growth rates and age distributions of larval and juvenile
northern anchovy, Engraulis mordax, with inferences on lar-
val survival. Ph.D. Thesis, Univ. California, San Diego, 388 p.
Owen, R. W.
1980. Eddies of the California Current System: physical and
ecological characteristics. In D. M. Power (editor). The
California Islands: Proceedings of a multidisciplinary sym-
posium, p. 237-263. Santa Barbara Mus. Nat. Hist. (Calif.).
Parrish, R. H., C. S. Nelson, and A. Bakun.
1981. Transport mechanisms and reproductive success of
fishes in the California Current. Biol. Oceanogr. 1:175-203.
Pike, G. C.
1951. Age, growth and maturity studies on the Pacific anchovy
{Engraulis mordax) from the coast of British Columbia.
M.A. Thesis, Univ. British Columbia, Vancouver, 44 p.
Reid, J. L., G. I. Roden, and J. G. Wyllie.
1958. Studies of the California Current System. Calif. Coop.
Oceanic Fish. Invest. Rep., 1 July 1956 to 1 January 1958,
p. 28-56.
Richardson, S. L.
1980. Spawning biomass and early life of northern anchovy,
Engraulis mordax, in the northern subpopulation off Oregon
and Washington. Fish. Bull., U.S. 78:855-876.
Spratt, J. D.
1975. Growth rate of the northern anchovy, Engraulis mor-
dax, in southern California waters, calculated from
otoliths. Calif. Fish Game 61:116-125.
Sunada, J. S., and S. Silva.
1980. The fishery for northern anchovy, Engraulis mordax,
off California and Baja California in 1976 and 1977. Calif.
Coop. Oceanic Fish. Invest. Rep. 21:132-138.
Vrooman, a. M., p. a. Paloma, and J. R. Zweifel.
1981. Electrophoretic, morphometric, and meristic studies of
subpopulations of northern anchovy, Engraulis mordax.
Calif. Fish Game 67:39-51.
Waldvogel, J. B.
1977. Age, maturity and distribution of northern anchovy
Engraulis mordax in Humboldt Bay, California. M.S.
Thesis, Humboldt State Univ., Areata, CA, 36 p.
496
PARASITES OF BENTHIC AMPHIPODS: MICROSPORIDANS OF
AMPELISCA AGASSIZI (JUDD) AND SOME OTHER GAMMARIDEANS
Phyllis T. Johnson^
ABSTRACT
Microsporidan infections were found in individuals of 11 species of benthic amphipods collected during
a 2V2-year survey of populations on the continental shelf of the northeastern United States. Ampelisca
agassizi (Judd) was the most numerous and broadly distributed species of amphipod. A microsporidan
confined to the abdominal muscles was common in most populations of A. agassizi. It is provisionally
assigned to the genus Thelohania. There were prevalences up to 37% depending upon the population
surveyed, but the microsporidans did not seem to contribute to mortality in A. agassizi populations, with
the possible exception of adult males. Microsporidans in other amphipod species parasitized various organs
and tissues according to the amphipod species and type of microsporidan. The relationships of the
microsporidans with the genera Thelohania, Stempellia, and Nosema are discussed.
In the late 1970's, a monitoring program was
developed within the National Oceanic and At-
mospheric Administration (NOAA) to assess the
presence of pollutants and their effects on the fauna
and flora of the continental shelf of the United
States. As a part of this plan, the Northeast Monitor-
ing Program (NEMP) has been conducted on a
seasonal basis from the Gulf of Maine to Cape Hat-
teras by the Northeast Fisheries Center, National
Marine Fisheries Service In connection with NEMP,
studies have been made of types and prevalences of
parasites, diseases, and other abnormalities of
various populations of benthic gammaridean am-
phipods. Samples were mainly from stations on the
Georges Bank and Mid-Atlantic Bight.
The results of the survey will be presented in a
series of papers. This, the first report, discusses
microsporidan parasites, particularly those of
Ampelisca agassizi (Judd).
Published information on parasites and patho-
logical conditions of gammaridean amphipods is
limited and concerns mainly the parasites of selected
estuarine and freshwater species, particularly the
microsporidan parasites (Bulnheim 1975). Data col-
lected during the present survey concern a broad ar-
ray of species of marine amphipods. Communities
of benthic amphipods are unlike most animal com-
munities because they are composed of numerous in-
dividuals of several to many related species that live
in very close proximity to one another. Indeed, it is
common for a population to contain two or more
^Northeast Fisheries Center, Oxford Laboratory, National Marine
Fisheries Service, NOAA, Oxford. MD 21654.
species of a single genus. It is also common for a
thousand or more individuals of a single species,
together with varying numbers of other species, to
be crowded onto one-tenth of a square meter of the
bottom (Dickinson et al. 1980). This unique popula-
tion structure makes studies of parasites and
diseases of the amphipods of great general biological
interest.
The methods used for collecting and preparing the
benthic amphipods are satisfactory for study of
many facets of the host-parasite relationships that
exist in these animal communities: effects of
parasites on their hosts, host specificity of parasites,
seasonal prevalence, and modes of passage of
parasites through host populations. On the other
hand, paraffin-embedded sections seldom allow
specific identification of parasites. Depending on the
parasite group, this may require examination of live
animals or of whole specimens fixed and stained by
special methods.
It is hoped that the data presented here and else-
where will serve as a framework for more definitive
studies on the taxonomy, life history, and other
aspects of the various parasite species.
MATERIALS AND METHODS
Amphipods were sampled 11 times over a 2V2-yr
period from July 1980 to December 1982 on NEMP
cruises (Tkble 1). The 35 stations where benthic am-
phipods were collected are shown in Figure 1. Not
all stations were visited on each cruise, being sam-
pled from 1 to 10 times each during the survey. The
11 stations indicated by solid circles on Figure 1 had
Manuscript accepted November 1984.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985
497
FISHERY BULLETIN: VOL. 83, NO. 4
Table 1.— Sampling cruises for benthic amphipods, July 1980-
December 1982.
Cruise
Date
NEMP cruise no.
designation
July 1980
AL80-07
A
September 1980
AL80-09
B
December 1980
DE80-09
C
April-May 1981
KE81-04
D
July 1981
AL81-07
E
August-September 1981
AL81-10
F
November 1981
DE81-07
G
January-February
1982
AL82-01
H
March-April 1982
AL82-03
1
August-September
1982
AL82-10
J
November-December 1982
AL82-12
K
consistent, and usually numerous, amphipod popula-
tions and were sampled five or more times. They
yielded the majority of data presented in this pa-
per.
Collections of bottom sediments and accompany-
ing biota were made with a 0.1 m^ Smith-Mclntyre^
grab. Generally a single grab was taken at each sta-
tion sampled. If the first grab contained few amphi-
pods but was from a station where they usually were
abundant, a second and sometimes a third grab was
taken. Sediment contained in the grab was washed
through a 1.0 mm sieve, and amphipods were either
collected with forceps or gently scraped from the
sieve and placed in a jar of 10% seawater Formalin.
On cruises A, B, and E (see Tkble 1), supplemental
specimens were collected at some stations by use of
an epibenthic sled or scallop dredge
Storage of samples was in Formalin except that
amphipods were transferred temporarily into 30 ppt
artificial seawater for identification and enumera-
tion, inspection for various gross lesions, and for
determination of life-history stages and microspori-
dan infections of the muscle in the case ofAmpelisca
agassizi (Judd). A stereomicroscope was used for
these procedures. Up to 30 and occasionally more
individuals of each species in the sample, depending
on numbers present, were processed for histologi-
cal examination by standard means. Finished tissue
sections were stained with hematoxylin and eosin.
Depending on size and number to be embedded, 1
to 12 amphipods of a single species from a single
station were embedded on their sides in each paraf-
fin block. Several serial sagittal sections were taken,
first laterally and then near the midline of the amphi-
pods. Because of unavoidable variations in size and
depth of the amphipods in the block, not all were sec-
tioned at the same levels. Parts of the hemocoel,
^Reference to trade names does not imply endorsement by tiie
National Marine Fisheries Service, NOAA.
skeletal muscle, and appendages of all amphipods
were present in sections. Usually, parts of the gills,
hepatopancreas and other parts of the gut, heart,
brain, and gonads were also present. Other tissues
and organs, particularly the antennal gland, hemo-
poietic tissues, eyes, and ventral nerve cord, often
were not included.
Measurements of microsporidan spores were
based on fixed material, either whole or embedded,
sectioned, and stained.
RESULTS
The amphipod population sampled at any one time
at a particular station was a mixture of up to 14 dif-
ferent species. Commonly five to eight species were
collected in a single grab except at station 23, which
was strongly dominated by Ampelisca agassizi. Of
eight samples from station 23, three contained only
A. agassizi, and A. agassizi made up 94 to 99% of
the remaining samples. Ibtals of the eight samples
from station 23 were 2,788 individuals of A.
agassizi and 23 individuals of other species (99% A.
agassizi).
Ampelisca agassizi was the most numerous and
broadly distributed of the species investigated, and
occurred at 17 stations including the 11 major ones.
Certain information on the life history of this species
is pertinent. It is an annual, tube-building species
that produces a single brood of young (Bousfield
1973). Overwintering is in the juvenile stage Gonads
of both sexes develop during the subadult stage
Breeding begins in the spring, and newly ovigerous
females are found from spring through autumn.
Postovigerous females tend to remain in the popula-
tion for an unknown period after the young are re-
leased from the brood pouch. Adult males are pelagic
or epibenthic, probably short-lived, and usually were
missing from samples collected with the Smith-
Mclntyre grab. Only the adult male has strongly
developed transverse pleosomal muscles (muscles of
the first three abdominal segments) (Fig. 2).
Presumably, these muscles aid in swimming. The
transverse muscles lie lateral to the longitudinal
muscles and are developed during the subadult stage
They can be seen in various stages of development
through the translucent cuticle of subadult
males.
Females of the gammaridean, tube-dwelling
amphipods so far studied leave their tubes to molt
to the adult stage Mating and egg extrusion take
place in the water column (Mills 1967). Population
dispersal is presumed to occur either by ovigerous
females settling away from their original location
498
JOHNSON: MICROSPORIDANS OF AMPEUSCA AGASSIZI
MARYLAND
i^ZZ^^-^.'" CAPE
'^ • HATTERAS:
^ ., ,76'
50 100 150 200
KILOMETERS
Figure 1.— Benthic stations of Northeast Monitoring Program at which populations of gammaridean amphipods were sampled dimng
the survey, 1980-82.
and probably in a less populated area (Mills 1967)
or by emigrating juveniles (Bousfield 1973). Thus,
juveniles and perhaps ovigerous and postovigerous
females of A. agassizi and other species could at
times be immigrants into locations with already
established populations of older juveniles and
subadult males and females.
Microsporidans of Ampelisca agassizi
Most of the populations of A. agassizi sampled
were regularly infected by a species of microsporidan
that attacks the longitudinal pleosomal muscles
(Figs. 3, 4). Infected muscles were chalky white in
fully developed infection, and easily visible through
499
FISHERY BULLETIN: VOL. 83, NO. 4
4K/
^■*v
x:
sv
Figure 2.—Ampelisca agassizi: Transverse pleosomal muscles
of an adult male Bar = 0.2 mm.
the translucent cuticle. Usually, only one to three
muscles were infected. Inspection of 150 micro-
sporidan-infected amphipods showed that in eight
cases transverse pleosomal muscles were also in-
volved, and in three cases, only the transverse
muscles were infected. One postovigerous female,
with microsporidan infection in muscle, also had
what appeared to be the same organism in one of
the ganglia of the ventral nerve cord.
On the basis of a tissue section she examined, A.
Cali^ determined that this microsporidan is a
pansporoblastic organism with the clusters appear-
ing to be in groups of eight. However, she said fur-
ther that possibly some clusters contained more than
eight spores. This is a point difficult to determine
in sectioned material. Spores are oval and of fairly
uniform size Ones dissected out singly from infected
muscle (not paraffin embedded) measured approx-
imately 3 fim X 1.5 ^m. In Call's opinion, the A.
agassizi parasite is best provisionally placed in the
genus Thelohania, without specific designation.
Figure 3.—Ampelisca agassizi: Longitudinal pleosomal muscles
infected by microsporidans (open arrows). Normal muscle is also
present (closed arrow), g, midgut. Bar = 0.2 mm.
Numerical information on this microsporidan is
based on samples taken on cruises D-K, because
determination of microsporidan infection was by
study of sectioned material only from cruises A-C,
and infections can be missed by this method. Con-
sidering all stations on cruises D-K, juveniles had
a lower prevalence of grossly visible infection than
did male and female subadults and ovigerous females
(Tkble 2), but this was not invariably the case in in-
dividual samples. In 5 of the 38 samples with micro-
Table 2. — Prevalence of microsporidan infec-
tions in Ampelisca agassizi by life-history
stages. All stations, cruises D-K.
Life-history stage
No. infections/
total collected
(o/o prevalence)
'A. Call, Rutgers University, Newark, NJ 07102, pers. commun.
1983.
Juveniles
Subadults
Ovigerous females
Postovigerous females
Adult males
Totals
517/4,868 (11)
1 ,335/5,293 (25)
111/501 (22)
82/413 (20)
1/55 (2)
2,046/11,130(18)
500
JOHNSON: MICROSPORIDANS OF AMPELISCA AGASSIZI
ft .m%
Am ^
'1 ' ^
*H' ^*
•^^
ji»'
I.' m^ ^ V
I
1%
w^
^ IP Cil
Figure i.—Ampelisca agassizi: Groups of spores and prespores
of the muscle-infecting microsporidan. Bar = 10 fjm.
sporidan-infected A. agassizi, prevalence was equal
to or slightly higher in juveniles than in subadults
or ovigerous females. Prevalence was very low in the
small sample of adult males, but varied considerably
in individual samples of both males and postovi-
gerous females (Ikble 3). The three stations with the
most consistently numerous populations of A.
agassizi also had the highest prevalences of micro-
sporidan infection. These were stations 23, 33, and
48, with overall prevalences of 30%, 37%, and 22%,
respectively. Overall prevalence at other stations
ranged from 0 to 14%.
The majority of infected hosts showed no reaction
to the presence of the microsporidans. However,
there was occasional melanization in heavily infected
muscle, with invasion of hemocytes into the mass of
spores, some encapsulation of spores and infected
muscle, and lysis of many spores. In these cases, it
appeared that the muscle had lost its integrity; that
is, the sarcolemma probably was no longer entire
Often, other infected muscle near the necrotic mass
of spores and muscle showed no evidence of attack
by host defense mechanisms.
The second microsporidan of A. agassizi parasi-
tized epithelial cells of the posterior half of the
midgut. Juveniles, male and female subadults, and
ovigerous and postovigerous females were infected.
The parasite resembled Nosema, the spores being
single and free in the cytoplasm of the host cell (Fig.
5). Spores were slightly oval and about 2 ^m in the
greater dimension. Infected cells were hypertrophied
(Fig. 6). In one heavy infection, many spores were
free in the gut and apparently most infected cells
had ruptured. There was no host reaction to infec-
tion. This parasite occurred twice in individuals with
microsporidan infection in abdominal muscle.
Based on sectioned material, overall prevalence of
the gut microsporidan was < 0.1% (25/2403).
Prevalence in samples with one or more infected A.
agassizi was 3.7% (25/678), range 1-6%. Amphipods
with microsporidans in the gut epithelium were from
stations 23, 33, 47, 48, 49, 50, and 51.
Microsporidans in Species Other Than
A. agassizi
Males and females of Unciola species (probably all
U. irrorata Say and U. inermis Shoemaker) were
hosts to a microsporidan that infected longitudinal
muscles of the pleosoma In three instances, a similar
or the same microsporidan was found in a ganglion
of the ventral nerve cord, and not in muscla Spores
appeared similar to those of the A. agassizi parasite;
they measured about 3 x 1.5 ^m; and there were
eight or more spores per envelope Unlike the A.
agassizi parasite, vegetative stages were often pres-
ent along with developed and developing spores. Un-
ciola species have an opaque cuticle, and infected
muscle cannot be seen grossly. Based on sectioned
Table 3. — Prevalence of microsporidan infections in Ampelisca
agassizi by life-history stages. Stations 47 and 48, cruises E and F.
Life-history
stage
No. infections/
total collected
(% prevalence)
No. infections/
total collected
(% prevalence)
Cruise E
Cruise F
Station 47
(depth
48 m)
(depth 62 m)
Juveniles
29/851
(3)
130/1,124 (12)
Subadults
45/258
(17)
12/53 (23)
Ovigerous females
14/84
(17)
11/53 (20)
Postovigerous
0/24
(0)
6/29 (21)
females
Adult males
0/34
(0)
1/3 (33)
Totals
88/1,251 (7)
160/1,262(13)
Cruise E
Cruise F
Station 48
(depth
72 m)
(depth 68 m)
Juveniles
2/33
(6)
5/29 (17)
Subadults
66/246
(27)
28/1 1 1 (25)
Ovigerous females
0
(-)
11/51 (22)
Postovigerous
0
(-)
3/27 (11)
females
Adult males
0/1
(0)
0/4 (0)
Totals
68/280
(24)
47/222 (21)
501
FISHERY BULLETIN: VOL. 83, NO. 4
Mr
Figure 5.—Ampelisca agassizi: Nosema-\ike microsporidan in
the midgut epithelium. Bar = 10 ixm.
A'-
• ■
# »
*0
«
*:? .'
— ,^' _\ _^^
Figure 6.—Ampelisca agassizi: Hypertrophy of midgut epi-
theUal cells infected by a Nosema-Vike microsporidan. Infected
epithelium to left, normal epithelium to right. Bar = 60 ^im.
material, prevalence v^as 8.3% (23/277), considering
only samples containing infected Unciola spp.
Prevalence was 1.7% when considering all Unciola
spp. that were sectioned and examined (Ikble 4).
There was no host reaction to infection in the
ganglia, but animals with muscle infection often
showed some melanization and encapsulative
response (Fig. 7). Scattered small melanized nodules
were common in the hemocoel of infected Unciola
spp., but it was not evident whether they had form-
ed in response to microsporidans.
Other amphipod species with microsporidan infec-
tions are listed in Table 4. Prevalence was usually
very low. Most of the parasites appeared like the
muscle-infecting microsporidans of A. agassizi and
Unciola spp. A Nosema-\ike parasite similar to the
gut microsporidan of A. agassizi, but smaller (0.7
ixm), occurred in the hepatopancreatic epithelium of
a specimen of Leptocheirtis pinguis (Stimpson).
Another L. pinguis harbored a larger A^osema-like
species in oocytes and heart muscle Infected oocytes
were necrotic and encapsulated by hemocytes. The
generalized muscle parasite of Melita dentata
(Kr0yer) s. lat. was also A^osema-like.
W n
f
#
O
t
i t
1% #
^
^t^^
m"
"^W
^"^
5"^
*
#
liiS#*
Figure 7.— Unciola sp.: Host reaction to microsporidans in ab-
dominal muscle Some groups of degenerating spores and
prespores are surrounded by melanized material. A few nuclei
of encapsulating host cells are visible around the mass of
microsporidans. Bar =10 jim.
502
JOHNSON: MICROSPORIDANS OF AMPELISCA AGASSIZI
Table 4. — Microsporidans in amphipods other than Ampelisca agassizi.
No. infections/
Amphipod
total examined
1
^•ositive
Type of
species
(% prevalence)
(
stations
Tissues infected
microsporidan
Unciola spp.
23/1,365(1.7)
33,
35, 38,
Abdominal muscle.
"Thelohania"
(irrorata Say and
47, 48, 51,
ganglia of ventral
inermis Shoemaker)
110, 112
nerve cord
Ampelisca
4/448
(0.9)
57,
66
Muscle, tegmental
"Thelohania"
vadorum Mills
glands, oocytes
Ampelisca
1/48
(2.1)
62
Connective tissue.
"Thelohania"
verrilli Mills
muscle
Ericthonius
1/436
(0.2)
38
Abdominal muscle
"Thelohania"
rubrlcornis Smith
Eriopisa elongata
1/29
(3.4)
47
Ganglia of ventral
"Thelohania"
(Bruzelius)
nerve cord
Leptocheirus
1/913
(0.1)
47
Abdominal muscle
"Thelohania"
plnguis (Stimpson)
1/913
(0.1)
15
Oocytes, heart
Nosema-Wke
1/913
(0.1)
20
muscle
Epithelium of
hepatopancreas
Nosema-Wke
Melita dentata
2/44
(4.5)
51
Generalized in
Nosema-Wke
(Kr^yer) s. lat.
muscle
Monoculodes
1/110
(0.9)
40
Abdominal muscle
"Thelohania"
edwardsi Holmes
Photis dentata
4/301
(1.3)
33
Abdominal muscle.
"Thelohania"
Shoemaker
ganglia of ventral
nerve cord
The microsporidan of Ampelisca vadorum Mills
resembled that of Unciola spp., but fully developed
spores were not seen (Fig. 8). Muscle, tegmental
8
4Mi
•»•
x*" ^-*
glands, and oocytes were infected. Often, groups of
microsporidans had "used up" the host tissue, and
appeared like groups of extracellular, closely knit,
vegetative and sporulating stages, but some of these
groups were unmistakably in the shape of tegmen-
tal glands and oocytes and were in the correct
anatomical positions. In one case, muscle fibers were
still present adjacent to the mass of microsporidans
and in another, microsporidans infected a recogni-
zable tegmental gland. Host reactions to the micro-
sporidans had not occurred in the few infected A.
vadorum available for study.
More than 35 specimens each of the following
species were sectioned and examined, but micro-
sporidans were not found: Anonyx sarsi Steel &
Brunei (36 specimens), Byblis serrata Smith (316
specimens), Casco bigelowi (Blake) (60 specimens),
Corophium crassicorne (Bruzelius) (50 specimens),
Harpinia propinqua Sars (116 specimens), Orcho-
menella minuta Kr0yer (64 specimens), Phox-
ocephalus holbolli Kr0yer (73 specimens), Pseuduni-
cola obliquua (Shoemaker) (46 specimens), and
Rhepoxynius epistomus (Shoemaker) (249
specimens).
%
i
Figure 8— Ampelisca vadorum: Vegetative and prespore
stages of a muscle-infecting microsporidan. Bar =10 jjm
DISCUSSION
Bulnheim (1975) and Sprague (1977) have hsted
and discussed the various microsporidans reported
from amphipods. Most of the hosts are freshwater
and estuarine forms, and depending on the species
503
FISHERY BULLETIN: VOL. 83, NO. 4
of microsporidan, muscles, ovaries, connective
tissues, and gut epithelia are infected. One of the
microsporidans, a parasite of Gammarus pulex L.,
infects the longitudinal abdominal muscles of its host
in the same manner as does the A. agassizi parasite,
but is knovv^n to have a variable number of spores
per envelope It was named Glugea muelleri (Pfeif-
fer, 1895, in van Ryckeghem 1930), later named
Thelohania giraudi (Leger and Hesse, 1917), and has
been called Stempellia muelleri (Pfeiffer) by
Bulnheim (1975) and Microsporidium giraudi
(Leger and Hesse) by Sprague (1977). The relation-
ship of "Glugea muelleri Pfeiffer" and the micro-
sporidan from A. agassizi remains to be determined.
Although "Glugea muelleri Pfeiffer" and the A.
agassizi parasite are remarkably similar in being
restricted to the longitudinal abdominal muscles of
their hosts, the latter is probably significantly
smaller. Fixed spores of the A. agassizi parasite are
about 1.5 X 3 ^m, and fresh spores of "Glugea
muelleri" are 2.2 x 4.5 jum.
The method of transmission of the A. agassizi
parasite is not known. Microsporidans are usually
transmitted orally, but transovarial transmission also
occurs in amphipods. Transovarially transmitted
microsporidans of Gammarus duebeni Lilljeborg in-
fect the ovary, and, depending on the species, cause
complete or partial feminization of males (Bulnheim
1975, 1977). The parasite of A. agassizi did not in-
fect the ovary, and because it was regularly found
in normal males, it apparently does not cause
feminization of males. Bulnheim (1971) successful-
ly transmitted "G. muelleri Pfeiffer" to several
species of Gam/marus, including euryhaline ones, by
feeding of infected muscle
Prevalence of the muscle parasite of A. agassizi
apparently increases with age of the host, and it
could be hypothesized that this microsporidan is
transmitted orally, that the older the host the more
chances it has had to become infected, and that the
parasite does not contribute to increased mortality
in the population. Adult males are active swimmers
and might prove an exception because impaired mus-
cle function could lead to increased predation. If this
occurred, one would expect infected males to be
preferentially removed from the population, leading
to a lower prevalence of infection in this stage In-
deed, prevalence in adult males was only 2%.
However, relatively few males were collected during
the survey, and the low prevalence could prove to be
sampling artifact. Note that in the sample from
cruise E, station 47 (Tkble 3), both postovigerous
females and adult males were uninfected, but 2 mo
later, at the same station, prevalence in post-
ovigerous females was 21% and the only infected
adult male found during the survey was also collected
at that time The discrepancy in prevalence might
be due to sampling of slightly different populations.
As discussed below, there is no assurance that the
same population vras sampled spatially, and temporal
differences conceivably might also have complicated
the results.
Relationships of the microsporidans seen in the
various species of amphipods could not be decided
on the basis of material fixed and prepared as it was.
It would be interesting to determine whether the
parasites of Unciola spp. and Ampelisca vadorum
are the same or different species, and what their
relationship is to the A. agassizi parasite There were
some differences in the habits and the developmen-
tal stages present in the three amphipods. Vegetative
stages were common in the case of the A. vadorum
parasite and fairly common in Unciola spp., but
usually rare or absent in A. agassizi. Several dif-
ferent tissues were infected in A. vadorum, but ex-
cepting a few infections in nervous tissue, only ab-
dominal muscle was infected in Unciola spp. and A.
agassizi. Previous investigators have found that
microsporidan infection is well tolerated by am-
phipod hosts, and that defense reactions against
these parasites generally are limited and may come
into play mainly when host tissue becomes necrotic
(reviewed by Bulnheim 1975). The muscle-inhabiting
microsporidan of A. agassizi is obviously a primary
parasite of that species and is seldom attacked by
the host. However, the similar parasite of Unciola
spp. often either provokes attack merely by its pres-
ence or damages the muscle so that a response oc-
curs to the necrotic tissue In either event, it is possi-
ble that this parasite is not fully adapted to Unciola
spp., because arthropods are known to be less
tolerant of non-adapted parasites (Salt 1970;
Unestam and Weiss 1970)
With exception of the muscle-infecting species
from A. agassizi, microsporidans are not common
parasites of benthic amphipods in the areas sampled,
even considering that some infections must have
been missed because not all would be seen in the
limited number of sections examined from each
amphipod.
Sampling methods used in the survey do not lend
themselves to precise studies on progression of
parasitic infections through particular populations.
Sampling cannot be done often enough to show if
and when additions to populations (with perhaps dif-
ferent prevalences of parasites) are provided by im-
migrating juveniles or other stages of these short-
lived animals. Further, populations may not be
504
JOHNSON: MICROSPORIDANS OF AMPELISCA AGASSIZI
homogeneous over the area sampled at a single sta-
tion. Sediment sampling with a grab is imprecise,
as the different depths of samples taken at stations
47 and 48 on cruises E and F testify (Table 3). It is
probable that return to an exact location was never
accomplished. Even if populations were homo-
geneous, predation by fish, and other short-term
disturbances, may cause local impoverishment of
populations or differences in population composition
that would not be detected in the necessarily blind
sampling done with a Smith-Mclntyre grab.
A general pattern does emerga In the area
surveyed, microsporidans are dominant parasites of
the most numerous and ubiquitous species, A.
agassizi, but are rare in all other species. This may
be a reflection of the fact that only A. agassizi con-
sistently occurred in dense populations at certain
stations at all sampling times, a circumstance that
would promote spread of a host-specific and horizon-
tally transmitted parasite.
ACKNOWLEDGMENTS
Thanks are due to Frank Steimle and Robert Reid
of the Northeast Fisheries Center Sandy Hook
Laboratory, and Linda Dorigatti, Gretchen Roe, and
Sharon MacLean of the Oxford Laboratory, who col-
lected the amphipods. Ann Frame, Sandy Hook
Laboratory, provided expert advice and training in
identification of amphipods. Linda Dorigatti iden-
tified material from cruises A-C, and along with
Gretchen Roe, Dorothy Howard, and Cecelia Smith
of the Histology Section, Oxford Laboratory,
prepared the specimens for histological examination.
Ann Call, Rutgers University, Newark, NJ, review-
ed the manuscript and provided identification of the
muscle-inhabiting microsporidan of A. agassizi.
LITERATURE CITED
BOUSFIELD, E. L.
1973. Shallow-water Gammaridean Amphipoda of New
England. Cornell Univ. Press, Ithaca, N.Y., 312 p.
BULNHEIM, H.-P.
1971. ijber den Wirtskreis der Mikrosporidie Stempellia
miiUeri. Arch. Protistenkd. 113:137-145.
1975. Microsporidian infections of amphipods with special
reference to host-parasite relationships: a review. Mar. Fish.
Rev. 37(5-6):39-45.
1977. Geschlechtsumstimmung bei Gammarus duebeni
(Crustacea, Amphipoda) unter dem Einfluss hormonaler und
parasitarer Faktoren. Biol. Zentralbl. 96:61-78.
Dickinson, J. J., R. L. Wigley, R. D. Brodeur, and S. Brown-
Leger.
1980. Distribution of gammaridean Amphipoda (Crustacea)
in the Middle Atlantic Bight region. U.S. Dep. Commer.,
NOAA Ifech. Rep. NMFS SSRF-741, 46 p.
Leger, L., and E. Hesse.
1917. Sur les Microsporidies de la Crevette d'eau douce C.
R. Seances Soc Biol. Fil. 80:12-15.
Mills, E. L.
1967. The biology of an ampeliscid amphipod crustacean
sibling species pair. J. Fish. Res. Board Can. 24:305-355.
Salt, G.
1970. The cellular defence reactions of insects. Cambridge
Univ. Press, Cambridge, 118 p.
Sprague, V.
1977. Systematics of the Microsporidia. In L. A. Bulla, Jr.,
and T. C. Cheng (editors). Comparative pathobiology. Vol.
2. Plenum Press, N.Y., 510 p.
Unestam, T., and D. W. Weiss.
1970. The host-parasite relationship between freshwater cray-
fish and the crayfish disease fungus Aphanomyces astaci:
responses to infection by a susceptible and a resistant
species. J. Gen. Microbiol. 60:77-90.
VAN Ryckeghem, J.
1930. Les Cnidosporidies et autres parasites du Gammarvs
pulex. La Cellule 39:401-416.
505
LONG-TERM RESPONSES OF THE DEMERSAL FISH ASSEMBLAGES
OF GEORGES BANK
William J. Overholtzi and Albert V. Tylers
ABSTRACT
The resilience of demersal fish assemblages on Georges Bank was investigated with data from seasonal
bottom trawl surveys conducted by the Northeast Fisheries Center, National Marine Fisheries Service,
Woods Hole, Massachusetts, from 1963 to 1978. Cluster analysis proved to be a useful statistical method
for delineating assemblage boundaries and associated species. Assemblages persisted over the long-term
and changed spatial configuration only slightly on a seasonal basis. Declines in biomass, numerical densi-
ty, and changes in relative abundance occurred ranging from mild to severe Assemblage changes were
probably triggered by intense fisheries as well as inherent trophic dynamics of component species. Results
have useful multispecies management connotations. The assemblage concept appears to be an appropriate
operational or conceptual framework for further management and modeling applications.
Most community ecological studies have necessari-
ly concentrated on the short-term aspects or season-
ality of assemblages. Typically 1 to 3 yr of field
measurements are analyzed with information theory,
niche breadth procedures, or multivariate statistical
methods. Demersal fish assemblages in particular
have been investigated in a number of locations [see
studies by Tyler (1971), Oviat and Nixon (1973),
Stephenson and Dredge (1976), Hoff and Ibara
(1977), Gabriel and Tyler (1980), and Inglesias
(1981)]. The recurrent theme in most of these studies
centers around seasonally varying diversity because
of environmentally induced migration, temperature
usually acting as the dominant driving variable
Unfortunately, many interesting questions cannot
be addressed in these studies because of their short-
term horizon. It is important to consider the long-
term ramifications of fishery system responses. The
temporal scale referred to here as "long-term" does
not refer to geologic time, but rather ecological time,
the span of years during which the actions of fishery
ecologists evoke system responses. Fishery
ecologists are limited in their ability to function
within this time frame. For instance, a plant ecologist
could predict with some certainty the type of forest
that would eventually occupy a cleared site, if left
undisturbed, but comparable knowledge for fishery
'Department of Fisheries and Wildlife, Oregon State Universi-
ty, Corvallis, OR 97331; present address: Northeast Fisheries
Center Woods Hole Laboratory, National Marine Fisheries Service,
NOAA, Woods Hole, MA 02543.
^Department of Fisheries and Wildlife, Oregon State Universi-
ty, Corvallis, OR 97331; present address: Department of Fisheries
and Oceans, Pacific Biological Station, Nanaimo, BC V9R 5K6,
Canada.
systems is lacking, especially in the marine
environment.
Are fish assemblages stable? How do they respond
to exploitation? Holling (1973) investigated sys-
tem responses to man's activities, showing that in
closed systems, such as freshwater lakes, the pro-
pensity to remain stable is high, but not infallible
Smith (1972) critiqued the Great Lakes experience,
concluding that the activities of man, notably fishing
and pollution, when coupled with biological inter-
actions, caused significant community alterations in
this system. Few marine studies, with the exception
of Soutar and Isaacs (1969), Sutherland (1980),
DeVries and Pearcy (1982), and some general over-
view papers (Brown et al. 1976; Richards et al. 1978),
have stressed the long-term temporal and spatial
aspects of marine system response
Longer term temporal and spatial questions were
examined with data from research conducted at the
Northeast Fisheries Center (NEFC) (Grosslein
1969). Concentrating on Georges Bank, we used
cluster analysis to produce yearly fall and spring
dendrograms for the period 1963-78 and 1968-78,
respectively. Assemblages were defined, component
species were identified, distributional maps plotted,
and the information was examined to elucidate long-
term temporal and spatial patterns. Further
analyses led to trajectories of species catch-per-unit-
effort (CPUE), assemblage total biomass, estimates
of intra-assemblage diversity, and other measures of
community response It is suggested that fishing,
coupled with interspecific interactions, appeared to
have played a major role in determining trends in
the Georges Bank assemblages.
Manuscript accepted November 1984.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
507- 5
FISHERY BULLETIN: VOL. 83, NO. 4
METHODS
Georges Bank, a large, submerged, marine plateau,
is located off the northeastern coast of the United
States (Fig. 1). It has been the site of an intense
fishery for several centuries, and a large interna-
tional fleet exploited the area from the 1960's to the
mid-1970's. The NEFC has conducted annual bot-
tom trawl surveys on the Northwest Atlantic con-
tinental shelf since the autumn of 1963. Annual
spring surveys commenced in 1968 and, in addition,
several summer and winter cruises have been under-
taken on an intermittent basis. Surveys were con-
ducted from Nova Scotia to Hudson Canyon from
1963 to 1966 and coverage was extended to Cape
Hatteras beginning in 1967. Grosslein (1969) and
Azarovitz (1982) described the details and justifica-
tion for the surveys, but a brief summary is
appropriate
The objective of the surveys is to obtain statistical-
ly meaningful abundance estimates of the offshore
marine fish populations in the aforementioned areas.
Secondary objectives included the collection of data
for distribution studies, age and growth determina-
tions, predator-prey interactions, and a host of
special purpose investigations. The potential area
was divided into zones (strata) based on depth and
biological considerations. Stratified random samples
were selected with allocation to each strata propor-
tional to its area. A 30-min sample with a standar-
dized research bottom trawl and a 1.25 cm cod end
liner was accomplished. All fish, as well as major in-
vertebrates, were sorted to species, weighed, and
measured, and some fish were sampled for other
MAINE
44'
42°
40"
74'
72*
70'
68'
66°
64"
Figure 1.— Georges Bank and Gulf of Maine region with shoreline place names and other associated geographical landmarks.
508
OVERHOLTZ and TYLER: DEMERSAL FISH ASSEMBLAGES
analyses. Sampling frequency averages about one
station for every 250 mi^ or roughly 300 locations
in a normal survey from Cape Hatteras to Nova
Scotia.
Data from a selected portion of this time series
was used in cluster analyses that defined demersal
fish assemblages. Specifically, a group of 36 species
representing the dominant fishes on Georges Bank,
were chosen as the focus for the investigation (Ihble
1). This choice was based on a preliminary examina-
tion of the data to determine which species were
most important in terms of biomass and numerical
density. Catches (kg) for each of the species from
every station in a particular cruise were organized
into a data matrix and processed with an agglomera-
tive cluster analysis program (Keniston 1978). lb
remove skewness in the species matrices, we trans-
formed the data prior to clustering by using an In
(x + 1) conversion. Station dissimilarities were
calculated by using the Bray-Curtis dissimilarity in-
dex, an ecological distance measure that is sensitive
to dominant species (Clifford and Stephenson 1975;
Boesch and Swartz 1977).
Table 1.— Species cited by common name in the text.
Common name
Scientific name
Spiny dogfish
Winter skate
Little skate
Smooth skate
Thorny skate
Atlantic herring
Alewife
Offshore hake
Silver hake
Atlantic cod
Haddock
Pollock
White hake
Red hake
Cusk
American plaice
Summer flounder
Fourspot flounder
Yellowtall flounder
Winter flounder
Witch flounder
Windowpane
Gulf stream flounder
Atlantic mackerel
Butterfish
Bluefish
Blackbelly rosefish
Longhorn sculpin
Sea raven
Gunner
American sand lance
Atlantic wolffish
Ocean pout
American goosefish
Short-finned squid
Long-finned squid
Squalus acanthias
Raja ocellata
Raja erinacea
Raja senta
Raja radiata
Clupea harengus
Alosa pseudoharengus
Merluccius albidus
Merluccius bilinearis
Gadus morhua
Melanogrammus aeglefinus
Pollachius virens
Urophycis tenuis
Urophycis chuss
Brosme brosme
Hippoglossoldes platessoides
Paralichthys dentatus
Paralichthys oblongus
Limanda ferruginea
Pseudopleuronectes americanus
Glyptocephalus cynoglossus
Scophthalmus aquosus
CItharichthys arctifrons
Scomber scombrus
Peprilus triacanthus
Pomatomus saltatrix
Helicolenus dactylopterus
Myoxocephalus octodecemspinosus
Hemitripterus americanus
Tautogolabris adspersus
Ammodytes americanus
Anarhichas luptus
Macrozoarces americanus
Lopliius americanus
lllex illecebrosus
Loligo pealei
The resulting dissimilarity matrix was used in a
group average fusion strategy to combine stations
with similar species distributions (Clifford and
Stephenson 1975). These station combinations were
displayed in dendrograms, which were examined and
assemblage groups were chosen by two criteria:
large-scale separations, as shown in Figure 2, and
dissimilarity levels. Stations from these assemblage
groups were plotted on cruise maps from the original
sampling plan and areas were delineated. This pro-
cess was repeated for all spring and fall cruises to
provide a consecutive series of maps, which were
then examined for continuity (Fig. 3). Finally, data
from several consecutive years were pooled to
delineate assemblages designated, based on nearby
geographic features or depth zones.
Species lists were prepared for the assemblages
outlined in the pooled cluster results, and data were
analyzed to further define the structure of each
group. Length frequencies from species in the dif-
ferent assemblages were used to separate life history
stages and catch-per-tow data were used to in-
vestigate trends in distribution and abundance Ex-
amination of food habit data in the literature and
NEFC documents gave further insight into assem-
blage structure Trajectories of assemblage CPUE
for selected species were plotted and examined for
long-term trends. Ibta! assemblage CPUE was also
investigated and compared with previous trends
reported by other authors for the region.
Gradient analyses were performed with the objec-
tive of explaining species distributions based on a
set of location, physical, and chemical variables.
Canonical correlations, using information on latitude,
longitude, depth, bottom temperature, bottom oxy-
gen, and bottom salinity, were employed to define
possible gradients that might be useful indicators of
species distribution (Pimentel 1979). Data for the
autumn cruise were obtained from measurements
of bottom temperature and depth made aboard the
RV Albatross IV {U.S.A.) 20 October to 5 November
1976, and corresponding information on bottom
salinity and oxygen from the RV Anton Dohrn
(Federal Republic of Germany) 14 November to 1
December 1976. Information for the spring cruise
was procured from measurements of bottom
temperature and depth from the RV Albatross IV,
17 April to 3 May 1978, and salinity and oxygen data
that was obtained from the RV Argus (Union of
Soviet Socialist Republics) from 13 to 28 April 1978;
these two data sets were chosen because they cor-
responded closely in time to the available station
information.
509
FISHERY BULLETIN: VOL. 83, NO. 4
^
^
1.0r
.8 -
.6 -
.4 -
.2 -
0
^ -- in oj
o o o o
o m o
m
1-
o
oooppoo oooQoP ooo ooo
CO to -^ C\J
o o o o
<T> (£> a O) .
oOooooooooooooooooooooooOooooo
~' ro^(Ch-ro<M<Mioio<DCvjioto^aO'^*ir)ODif>
OfOinototficDO^ioto
tmio-^cvjiOcvj — toT-^tofO
- -ooo -
ro cvj po iT)
STATION
Figure 2.— Typical dendrogram, autumn 1966, showing duster station groups and dissimilarities. Dashed line indicates
a dissimilarity of 0.65.
RESULTS
Five important assemblage groups were present
on Georges Bank from fall 1963 to 1978. For refer-
ence, w^e name these groups: Slope and Canyon,
Intermediate, Shallow, Gulf of Maine Deep, and
Northeast Peak. A consistent spatial pattern
emerged as consecutive fall cruises were examined
and plotted. The same five groups appear to have
been present in similar locations since 1963. These
five assemblages were present at the mid- and end-
points of the fall time series also (Fig. 3). The groups
appear to change their spatial configuration slight-
ly on an annual basis, but the general area of each
group was maintained. Lists of the dominant species
in each assemblage are given in Ikble 2.
The total area that each assemblage encompass-
ed through time (years) was delineated by pooling
the observations from consecutive years. Figure 4
shows an example of a representative assemblage
from the spring and fall, respectively. The groups
overlapped surprisingly little through time with the
exception of a few border stations along adjacent
assemblages.
Table 2.— Assemblage species associations from
cluster results (demersal species only).
Slope and canyon:
Silver hake
White hake
Red hake
Gulf stream flounder
Offshore hake
Fourspot flounder
Blackbelly rosefish
American goosefish
Intermediate:
Winter skate
Little skate
Red hake
Silver hake
Atlantic cod
Haddock
Sea raven
American goosefish
Ocean pout
Longhorn sculpin
Yellowtail flounder
Shallow:
Winter skate
Little skate
Silver hake
Atlantic cod
Haddock
Pollock
White hake
Red hake
Summer flounder
Yellowtail flounder
Winter flounder
Windowpane
Longhorn sculpin
Sea raven
Ocean pout
Sand lance
American goosefish
Gulf of Maine Deep:
Thorny skates
American plaice
Witch flounder
White hake
Silver hake
Atlantic cod
Haddock
Cusk
Atlantic wolfflsh
Northeast Peak:
Thorny skate
Atlantic cod
Haddock
Pollock
White hake
Winter flounder
Ocean pout
Longhorn sculpin
510
OVERHOLTZ and TYLER: DEMERSAL FISH ASSEMBLAGES
, GULF OF MAINE DEEP
■^Nj: X NORTHEAST
SHALLOW --V \ PEAK
INTERMEDIATE
SLOPE AND CANYON
FALL 1963
Figure 3.— Georges Bank assemblages for three autumn surveys
1963, 1970, 1976.
43<=
42° -
41° -
40°
43°
42° -
4r
40'
i/t'
— 1 — I — 1 —
''^' ^
\ J.. •• . •• ')
\ ,/• •• J- . . » • .* /
1
1 1 1
71'
70'
69'
68'
67'
66'
Figure 4.— Sample pooled station distributions for the Slope and
Canyon assemblage, spring 1968-73 (top panel) and the Shallow
assemblage, autumn 1963-67.
Data for all cruises were pooled by season and
used to generate composite maps of general assem-
blage areas, for the spring and autumn (Fig. 5). The
Slope and Canyon assemblage appears to encompass
a similar area regardless of season, while some of
the other assemblages changed slightly. The Shallow
assemblage covered most of Georges Bank in the
spring (Fig. 5) and was slightly smaller in the fall
(Fig. 5). The Intermediate assemblage is somewhat
larger in the fall (Fig. 5), suggesting a migration of
the species in this area to shallower water as the year
progresses. Assemblages in the spring appear to
follow depth contours resulting in the elongate shape
of the groups at this time (Fig. 5). The Northeast
Peak Interior (NPI) and Northeast Peak-Gulf of
Maine Deep (NP-GM Deep) assemblages show
definite seasonal spatial changes when compared
with the Gulf of Maine Deep (GM Deep) and North-
east Peak assemblages in the fall (Fig. 5). The
general shape and location of the fall assemblages
suggests that a different set of oceanographic and
biological forcing factors are important in deter-
511
FISHERY BULLETIN: VOL. 83, NO. 4
69°
68° 67'
66'
42'
41"
I
1
■T I
I
(
NP-GM DEEP
NPI
-V
v
>
"^^^^^^
>r\-
/
SHALLOW J
f
I
2-^:;^
^
100 m , \
s
*" "^^^••'"''^NTERMEDIATE
1
\^^
SLOPE AND CANYON
1
GEORGES BANK SPRING ASSEMBLAGES
42° -
41°
NORTHEAST PEAK,
''d^
«^
INTERMEDIATE
69° 68° 67° 66°
GEORGES BANK FALL ASSEMBLAGES
Figure 5.— Composite maps showing seasonal changes in the
Georges Bank assemblages and their approximate areas. NPI =
Northeast Peak Interior; NP-GM Deep = Northeast Peak-Gulf of
Maine Deep; GM Deep = Gulf of Maine Deep.
mining the distribution of fish. The Northeast Peak
assemblage, for instance, spans several depth zones
and encroaches on the Shallow assemblage, reducing
its area during this part of the year.
The assemblage maps presented in Figure 5 were
useful for organizing the 36 species of Ikble 1 into
their corresponding demersal subunits (Tkble 2).
Four basic species categories were defined in the
various assemblages. These included ubiquitous
species, resident species, periodics, and those resi-
dent species present in several assemblages during
different parts of their life history. Ubiquitous
species, such as ocean pout, goosefish, sea raven, and
Atlantic cod, were found with regularity in almost
all of the assemblages. Resident species, such as lit-
tle skate, winter skate, longhorn sculpin, yellow tail
flounder, winter flounder, American plaice, and
witch founder, were present in only one or two
assemblages in abundance Periodic or seasonal
migrants include bluefish, butterfish, and mackerel,
as well as short-finned squid and long-finned squid.
These species moved in and out of the various assem-
blages on a seasonal basis with temperature being
a likely dominant force, and were often highly
variable in terms of their abundance and were there-
fore not included in Ikble 2.
A number of species, including silver hake, red
hake, white hake, and haddock, were present in more
than one assemblage as different life history stages.
Silver hake, for example, are found in the Slope and
Canyon and Shallow assemblages, with adults on the
average, occurring more frequently in the Slope and
Canyon and Gulf of Maine Deep assemblage, while
juveniles are more abundant in the Shallow assem-
blage. It appears that for many of the abundant fish
species on Georges Bank, adults occupy the deeper
peripheral assemblages while juveniles of these same
species occupy the shallower zones during much of
the year.
ASSEMBLAGE TRAJECTORIES
Assemblage CPUE indices were calculated for
several of the spring and fall assemblages and used
for evaluating temporal trends in total catch and
catch by species. Assemblage CPUE declined drama-
tically in the mid-1960's to early 1970's in four of
five Georges Bank assemblages in fall (Fig. 6). In par-
ticular, research catches in the Shallow, Northeast
Peak, and Gulf of Maine Deep assemblages reached
all-time lows in the early 1970's, coincident with
large increases in international effort and landings
at that time (Figs. 6, 7). International effort, mea-
sured in thousands of days fished, increased three-
fold over the period 1960-69 (Fig. 7). Assemblage
biomass showed some signs of recovery in the late
1970's when good year classes of Atlantic cod, had-
dock, and other species occurred and international
effort declined due to the Magnuson Fishery Con-
servation and Management Act of 1976 (Figs. 6, 7).
Research catch of silver hake, fourspot flounder,
red hake, white hake, and black belly rosefish re-
mained nearly stable over the spring period
(1968-75), then increased abruptly after 1976 due to
increases in the silver hake (Fig. 8A).
Total catch for the fall time series was also stable
for most years, until 1972 when silver hake and red
hake abundance fluctuated (Fig. SB).
Figure 8C shows the trends in percent by weight
for the five species during fall indicating a change
in biomass dominance for silver hake and red haka
Blackbelly rosefish and fourspot flounder showed the
512
OVERHOLTZ and TYLER: DEMERSAL FISH ASSEMBLAGES
SLOPE AND CANYON
200 r
150
100
50
1 •_! 1 a^^-S •
200
150
100
50,
INTERMEDIATE
0
200 r
150
100
50
_l L.
SHALLOW
_1 I
200
NORTHEAST PEAK
/
150
1
— /
/
/
1
/
/
•
100
50
n
1 1 1 1
200 r
150
100
50
GULF OF MAINE DEEP
0
_i I I I
I
^
5
60 r
50
40
30
20
10
_l_
_i_
_l_
60
62 64 66
68 70 72
YEAR
74
76 78 80
63 66 69 72 73 78
TIME
Figure 7— Unstandardized effort data in thousands of days fish-
ed for the Georges Bank demersal fishery, all countries, for 1961-79,
expressed as 3-yr moving means.
same trends as in the former case, but represented
more of the catch on a percent weight basis in the
later years of the fall time series (Fig. 8C). Gulf
Stream flounder was actually one of the more im-
portant species numerically during the mid-years of
the series (Fig. 8D). The same general trend for red
and silver hake, and the other species is apparent
in the percent by numbers data (Fig. 8D).
The shallow assemblage was much more diverse
than the Slope and Canyon assemblage. The major
species of importance were Atlantic cod, winter
skate, longhorn sculpin, little skate, yellowtail
flounder, and haddock. Mean catch per tow in the
fall time series declined dramatically from 202 kg
in 1963 to 22 kg in 1972 and subsequently rose to
99 kg in 1978 or about one-half the 1963 value (Fig.
6). Winter flounder, longhorn sculpin, and winter
skate appear to have remained fairly constant in
abundance over the spring time period, while Atlan-
tic cod, windowpane flounder, and little skate
displayed an increasing trend in biomass (Fig. 9A).
Yellowtail flounder and haddock showed declining
mean catches over this interval. The fall time series,
since it is longer, clarifies some of the observed
spring trends. Cod and winter flounder CPUE re-
mained relatively stable over the fall period, while
windowpane flounder, winter skate, and little skate
appear to have increased from 1972 onward (Fig.
Figure 6.— Mean catch per tow (kg) from NEFC Georges Bank
bottom trawl surveys for autumn 1963-78 for the five assemblages.
Dashed line indicates a 3-yr moving mean of the plotted data points.
513
FISHERY BULLETIN: VOL. 83, NO. 4
ais
UJCC
i-q:
CC LU
OUJ
h-O
Q.Q
l/iZ
tnz
Ll-3
q: d
-lO
no
a, a:
Oli.
ILU.
5X t/5I
£ Q
tJ3aiAinN lN30d3d
O
o o
CM -^
S^
<1>
A
£
3
C
-o
c
c«
4J
x;
u
a;
>
>i
..Q
^-j
C
V
c;
1-.
m
a
<u
>
.w
eS
3
E
3
o
St
h
00
J=
t>-
tn
co
Q
CO
T3
I— (
§
c
F
u
rs
3
Ol
oi
•>. -^
a>
01
>
>
o
u
tv
<v
A O.
tn
m
1)
(U
"cS X! txf
S2
nj c~
OJ
aj
CO
H
>
«5
T*
■w
05
T1
OJ
T-H
i
d
E
3
C
E
3
n
o
1
to
§
a:
0)
T3
00
(^HJMOI/HDIVO NV3y\l
1H9I3M lN3Dd3d
S< be
ra m C
-" "^^ he
E ^ 1^
ni ^- ^3
CO a o
V ^ C
I 3 C
00 1^
H C cS
05 g 0)
Uh «t-i CO
514
OVERHOLTZ and TYLER: DEMERSAL FISH ASSEMBLAGES
c
B
3
O
.1
U
s
3
C
T3
C
c«
be
I
C
o
0)
S
3
I
CO
-o <x>
£ s:
o fcr
m'
(^>I)M01/H01VD NV3IAI
1H9I3M lN3D^3d
M fc. 5
W u o
OS 5* !=
§§§
515
FISHERY BULLETIN: VOL. 83, NO. 4
9B). Haddock CPUE, on the other hand, declined
dramatically from 97.3 kg in 1963 to 0 in 1972, re-
maining at very low^ levels of abundance in the later
years. Yellowtail flounder fluctuated from 15 kg in
1963 to a low of 6 kg in 1966, increased from 1966
to 1969, and declined through 1978 (Fig. 8B).
An examination of trends in cumulative percent
by weight and number trajectories for the Shallow
assemblage highlighted some interesting points.
Atlantic cod comprised a fairly constant proportion
of the species biomass for all the years except 1964
and 1965. Longhorn sculpin, yellowtail flounder, and
to a lesser extent winter flounder, made up an in-
creasing part of the biomass of this assemblage dur-
ing 1966-71 and then all declined in importance (Fig.
9C). Haddock, as previously noted, experienced a
pronounced decline in abundance from the early
1960's and was only present at very low levels from
1972 to 1978. Winter skates, little skate, and
windowpane flounder accounted for an increasing
percent of the biomass in this assemblage from the
early 1970's onward (Fig. 9C).
When cumulative percent by number was inves-
tigated, silver hake and red hake became important
(Fig. 9D). Silver hake was the numerical dominant
through most of the mid- and late 1970's. This trend
was due entirely to increased numbers of juvenile
silver hake that represented a small amount of
biomass. This same phenomenon applies to red hake,
which enjoyed several periods of increased abun-
dance as a proportion of the total numerical densi-
ty from 1963 to 1978. Winter skate numbers remain-
ed relatively unchanging from 1963 to 1976 and then
rose slightly in the late 1970's. Trends for window-
pane flounder, longhorn sculpin, little skate, yellow-
tail flounder, and haddock follow the cumulative ab-
solute and percent weight data (Fig. 9B, C, D).
The other Georges Bank assemblages were inves-
tigated using the same techniques, but on a much
less intense scale TDtal mean catch/tow for the Inter-
mediate, Gulf of Maine Deep, and Northeast Peak
assemblages is displayed in Figure 6 for the fall
surveys 1963-78. The trends in total CPUE follow
the same basic patterns for all three groups, a high
initial period followed by a decline and subsequent
recovery in the mid- to late 1970's.
General decreases in the catch of throny skates,
haddock, and cod were responsible for the downward
trend in CPUE for the Northeast Peak assemblage,
but the recovery that occurred in the late 1970's was
due primarily to increased haddock biomass (Figs.
6, 10). The Northeast Peak assemblage is fairly sim-
ple in species composition, and although some fluc-
tuations in cumulative percent by weight occurred.
NORTHEAST PEAK ASSEMBLAGE
CUMULATIVE PERCENT BY WEIGHT
FALL 1963-1978
100 r
POLLOCK
HADDOCK
1963
1967
1971
1975
Figure 10.— Reponses of species from the Northeast Peak assem-
blage demersal fish community expressed as cumulative percent
by weight for autumn 1963-78.
the same four species remained dominant over the
period (Fig. 10.)
Time sequence cluster analyses were useful as fur-
ther indicators of temporal trends in these groups.
Species biomass for the Slope and Canyon assem-
blage did not appear to follow any clear long-term
trend (Fig. 11). Enough fluctuation in CPUE oc-
curred to mask any trend, and no clear pattern was
established. This same analysis on the Shallow
assemblage showed three distinct temporal clusters,
composed of consecutive years (Fig. 11). Using this
perspective and Figure 9, there appears to have been
three periods of significant change in relative abun-
dance during the fall time series; an initial period
dominated by haddock, intermediate period with
high yellowtail, longhorn sculpin, and winter
flounder catches, and finally a group with little skate,
winter skate, and windowpane flounder as the domi-
nant species.
GRADIENT ANALYSIS
Gradient analyses of two selected Georges Bank
data sets did not prove to be as useful as was hoped,
but some information and insight were gained and
the dimensionality of the large multivariate data sets
involved was much reduced. The data set used in the
fall 1976 canonical correlation analysis accounted for
about 26% of the variation in species distribution for
32 selected species of interest. The variables included
in the analysis were latitude, longitude, depth, bot-
tom temperature, bottom salinity, and bottom oxy-
516
OVERHOLTZ and TYLER: DEMERSAL FISH ASSEMBLAGES
1.0 r
.8
.6
.4 1-
.2
I
Sr/J TION
1.0 r
.8
.6
.4
.2
r^roioiD'j-cnoo-^OCDr^tDf^infO'}-
STATION
Figure 11.— Time sequence cluster analyses for autumn 1963-78
for the Slope and Canyon (top panel) and Shallow (bottom panel)
assemblages on Georges Bank.
gen. The first three canonical axes accounted for
73.9% of this total, a cumulative redundancy of
19.0% (Ikble 3). The first canonical variable (CV)
reflects the importance of depth and to a lesser
degree bottom salinity, in determining the distri-
bution of these species. Although none of the corre-
lation loadings for CVl are particularly high, the
gadoids, as a group, show a positive trend. Many of
the shallow-water species, such as little skate, winter
skate, and most of the flounders, showed negative
correlations with this canonical variable The other
two CV's reflect the location variables of latitude and
longitude as well as bottom oxygen and salinity.
Since the gadoids and flounders appeared to show
a group response to these distribution variables, we
decided to use them in another analysis, excluding
the other species (Ikble 3, Fall 1976 II). This data
set explained 28.3% of the total variation in distri-
bution for a selected set of 14 species (Tkble 3). The
first canonical variable had a high correlation with
latitude (r = 0.904) and the gadoids, as a group, were
highly positively correlated with this CV (Ikble 3).
It appears that although Georges Bank spans only
about two degrees in total north-south latitudinal
variation, this variable is useful for defining centers
of gadoid biomass.
The third analysis did not reveal any new trends,
accounting for 32.6% of the variation in species
distribution. In general, then, although significant
orthogonal canonical axes were defined in each of
three data sets, the amount of variation that was ac-
tually explained was relatively small. There appear
to have been trends in the distribution of some
gadoid and flounder species, but the strength of
these relationships was hardly firm. Most of the
variation in species distribution was related to
latitudinal, salinity, and depth differences.
DISCUSSION
Questions of community resilience (Pimm 1984)
are meaningful because resource managers are
faced with the dilemma of making decisions that may
alter future community structure Fishery managers,
in particular, are unable to deal with the long-term
consequences of their management decisions
because they lack specific knowledge of ecosystem
reponses. This idea may apply particularly to areas
such as Georges Bank, where landings of each
species are part of a multispecies otter trawl fishery.
In this case the application of single species manage-
ment to assemblages of fishes may result in simpli-
fication of the community such that less productive
fish populations or those more vulnerable to fishing
are reduced dramatically (lyier et al. 1982). If this
occurs, important trophic linkages may be precluded,
economic viability may suffer, and management op-
tions may be removed indefinitely. At the present
time the argument of these central issues is pro-
ceeding slowly in the literature and few, if any,
management agencies are considering these types
of questions in their decisions. We need, therefore,
to begin to investigate the long-term temporal scale
of communities so that ecologists and managers can
begin to function in terms of ecological time instead
of just a framework for short-term reaction.
Declines in total finfish abundance on the conti-
nental shelf of the northeastern United States reach-
ed unprecedented levels over the period 1965-74
(Brown et al. 1976). Not only had biomass declined.
517
FISHERY BULLETIN: VOL. 83. NO. 4
Table 3.— Canonical variable (CV) loadings for fall 1976 and spring 1978 gradient analyses, with canonical correlation coefficients (Re),
amount of variation explained by each canonical axis (% variation), and total variation in species distribution explained by the environmen-
tal data.
Fall 1976 1
Fall 1976 II
Spring 1978 1
CV1
CV2
CV3
CV1
CV2
CVS
CV1
CV2
CV3
Spiny dogfish
- 0.509
0.149
0.232
-0.089
0.105
0.111
Winter skate
-0.263
0.342
-0.244
-0.176
-0.377
0.058
Little skate
-0.428
0.113
-0.163
-0.015
-0.437
0.142
Smooth skate
0.552
-0.117
-0.144
0.333
0.210
-0.204
Thorny skate
0.387
0.017
0.063
0.534
0.416
0.188
Sea herring
0.003
0.081
0.058
0.084
-0.147
0.068
Alewife
-0.023
0.097
0.161
0.433
0.086
0.104
Offshore hake
0.456
-0.408
-0.100
-0.147
0.613
0.284
Silver hake
0.285
0.203
0.536
0.607
0.332
0.027
-0.237
0.637
-0.328
Atlantic cod
0.059
0.544
0.195
0.600
-0.263
0.048
0.262
-0.534
0.177
Haddock
0.370
0.525
0.131
0.647
-0.069
-0.235
0.383
-0.300
0.072
Pollock
0.337
0.158
0.199
0.439
0.274
0.167
0.425
0.209
0.015
White hake
0.564
-0.022
0.341
0.447
0.614
0.083
-0.030
0.527
0.055
Red hake
-0.109
-0.109
0.034
-0.220
-0.043
-0.460
0.303
0.616
0.057
American dab
0.281
0.048
0.362
0.395
0.365
0.141
0.409
-0.035
-0.026
Summer flounder
-0.245
-0.124
-0.102
-0.246
-0.111
0.126
-0.427
0.309
0.303
Fourspot flounder
-0.235
-0.265
0.210
-0.326
0.051
-0.588
-0.417
0.418
0.366
Yellowtaii flounder
-0.158
0.324
-0.083
0.115
-0.419
-0.095
0.080
-0.442
0.144
Winter flounder
-0.145
0.364
0.078
0.295
-0.324
0.114
0.109
-0.301
0.040
Witch flounder
0.179
-0.267
0.140
-0.107
0.407
-0.187
0.368
0.138
-0.225
Windowpane
-0.326
0.165
-0.351
-0.087
-0.439
0.504
-0.527
0.041
0.251
Butterfish
-0.279
-0.415
0.405
Blackbelly rosefish
0.359
-0.544
0.050
-0.295
0.529
-0.199
Longhorn sculpin
-0.078
0.432
-0.136
0.101
0.478
0.068
Sea raven
-0.034
0.432
-0.092
-0.500
0.034
0.194
Gunner
-0.082
0.198
0.023
American sand lance
-0.134
0.043
-0.079
0.130
-0.125
0.224
Atlantic wolffish
0.011
0.240
0.106
0.233
0.073
0.358
Ocean pout
-0.043
0.265
0.122
-0.133
-0.316
0.034
American goosefish
0.145
-0.073
0.184
-0.261
0,414
-0.039
Short-finned squid
0.249
0.284
0.303
-0.275
0.169
0.072
Long-finned squid
-0.471
-0.239
-0.379
-0.256
0.399
-0.077
Variables
Latitude
0.306
0.922
0.074
0.904
-0.333
0.066
0.878
0.012
-0.131
Longitude
-0.458
-0.164
0.597
-0.004
0.064
0.118
0.240
-0.032
0.474
Depth
0.885
-0.432
0.049
0.030
0.849
-0.071
-0.107
0.792
-0.448
Bottom temp.
-0,179
-0.696
-0.233
-0.590
0.258
0.366
-0.252
0.720
-0.465
Bottom salinity
0.463
-0.547
0.422
-0.107
0.753
-0.586
-0.374
0.909
-0.133
Bottom oxygen
-0.316
0.450
-0.581
0.041
-0.613
0.407
0.199
-0.908
0.144
RC
0.975
0.961
0.874
0.871
0.841
0.750
0.979
0.968
0.943
% variation
8.2
7.2
3.6
11.1
9.1
4.3
9.2
11.8
2.8
Significance
P < 0.001
P < 0.001
P < 0.05
P < 0.001
P < 0.001
P < 0.05
P < 0.001
P < 0.001
P < 0.001
Total variation
25.7
28.3
32.6
but total effort on Georges Bank increased several
times (Fig. 7). The assemblage trends examined in
this paper can be linked to these high levels of effort.
During this time period, seasonal bottom trawl
surveys monitored trends in finfish abundance over
the area from the Gulf of Maine to Cape Hatteras.
This survey proved invaluable to fish stock assess-
ment work because changes in the relative abun-
dance of most of the commercial species were follow-
ed closely and were highly correlated with commer-
cial catch, effort, and other indices (Clark 1979).
Other species of ecological, perhaps not commercial
importance, were also routinely and closely
monitored over this time The spring and fall bot-
tom trawl survey provided an excellent means for
assessing community or assemblage responses over
this time period.
Cluster analysis, with the Bray-Curtis dissimilarity
index and group average fusion method, proved
helpful for defining demersal fish assemblages on
Georges Bank. Recent studies confirm the value and
applicability of the Bray-Curtis index (Bloom 1981).
This method provided a means for collapsing the
multidimensional nature of the spring and fall
Georges Bank survey cruises into smaller, more
easily interpreted, units. It was then possible to
investigate not only long-term temporal and spatial
persistence questions, but also intraspecific
responses within the particular assemblage of
interest.
518
OVERHOLTZ and TYLER: DEMERSAL FISH ASSEMBLAGES
Not only did seasonal Georges Bank assemblages
maintain their temporal integrity over the periods
1963-78 in the fall and 1968-78 in the spring, but they
also appear to have retained their spatial configura-
tion for the most part as well. The results of this
study indicate that although changes in species com-
position and relative abundance occurred in varying
degrees in all the assemblages, they remained con-
tinuous in time and spaca
Although many of the species on Georges Bank
are found in several assemblages, it appears that
each of the five groups has enough large-scale varia-
tion in biomass, species composition, and relative
abundance to make each of the assemblages uniqua
Also at least one or two dominant Georges Bank
species occupy each assemblage, for example, the
bulk of the haddock stock occurs in the Northeast
Peak group. Thus, even though some assemblages
changed dramatically in terms of species richness
and relative abundance, the spatial integrity of each
complex was preserved over tim&
The energy budget of Georges Bank can serve as
a plausible explanation for the particular species
distributions we found. Georges Bank is a dynamic
ecosystem driven by a complex and unique nutrient
advection system. Its shallow topography and geo-
graphic location, with constant mixing of the water
column and lack of stratification, does not lead to
the usual nutrient limitation of primary productivi-
ty (Sutcliffe et al. 1976; Cohen et al. 1982). Instead
of the usual spring and fall pulse in primary produc-
tion, the region is characterized by high productivi-
ty from April to November. Yearly primary produc-
tion levels are as high as 450 gC/m^ per yr in the
shallow (< 100 m) zone of Georges Bank (Cohen et
al. 1982). This shallow mixed zone encompasses the
same area as the Shallow and Intermediate assem-
blages delineated in our cluster analysis results. The
area is dominated by fish that feed on invertebrates.
Primary prey items for these species include euphau-
siids, copepods, mysids, amphipods, and other ben-
thic invertebrates. This part of the ecosystem is fairly
closely tied to primary production, and its compo-
nent species may compete for food resources dur-
ing their early life history (Pitt 1970; Bowman 1981;
Overholtz 1982). Predation, too, may be an impor-
tant biological mechanism for determing trends in
this assemblage (Overholtz 1982). The other assem-
blages that we have described in this analysis occur
along the fringes of Georges Bank at the shelf-slope
interface These shelf break groups contain the ma-
jor adult demersal fish stocks found in the area with
the exception of yellowtail flounder. These peripheral
assemblages are dominated by large predators that
are generally piscivorous, with little, if any, dietary
overlap (Langton and Bowman 1981).
The gradient analyses suggest that about 25% of
the total variation in species biomass distribution can
be explained with the variables used in the study.
This result was surprising at first, since we felt that
the variables we used would explain much more of
the variation than this. However, considering the fact
that other important biological factors, such as
predation, fishing, competition, and food preferences
were not included in the analysis, it is probably a
realistic percentage Perhaps an analysis that in-
cluded the whole east coast would account for much
more variation because a wider range of conditions
would exist.
Other studies that have successfully explained
species distributions usually occur in habitats with
very strong physical or chemical gradients, such as
mountain forests or estuaries (Whitaker 1967; Mcln-
tire 1973). Either the actual gradients were not
strong enough to explain more than a small percent-
age of the species distribution or those other factors
were more important.
The questions of resilience and stability of demer-
sal fish assemblages that were defined and inves-
tigated in this study have implications for the
management of Georges Bank. This study provides
a useful conceptual framework for managing many
of the demersal fish stocks in this area. Not only
were stable zones with specific resident fishes
delineated, but they were present over the long-term
record. Species components of fall assemblages are
indicators of general distributions that represent the
location of major fish stocks during the productive
portion of the year. Long-term responses observed
in the Georges Bank community indicate the pro-
pensity for adjustment or resilience (Rolling 1973)
that a particular assemblage might have Assem-
blages on the periphery of Georges Bank might be
less susceptible to changes in species composition
and relative abundance because their component
species are less trophically linked. The Shallow
assemblage, on the other hand, appears to be par-
ticularly vulnerable to fishing and perhaps inter-
specific interactions. This type of knowledge will be
helpful for understanding changes in fish abundance
and community structure and for effectively man-
aging fishery systems in the future
ACKNOWLEDGMENTS
We would like to dedicate this paper to the men
and women of the Northeast Fisheries Center,
Woods Hole, MA, for without their long-term plan-
519
FISHERY BULLETIN: VOL. 83, NO. 4
ning and tireless efforts in collecting the data, it
would have been impossible to complete this work.
We thank E. Beals for providing such good advice
and helping with analyses. We are grateful for the
friendship and assistance of G. Kruse, T. Hayden, and
W. Gabriel, who provided much inspiration over the
span of the last several years. We would also like to
thank B. Brown for his help, direction, and patience
LITERATURE CITED
AZAROVITZ, T. R.
1981. A brief historical re\dew of the Woods Hole Laboratory
trawl survey time series. Can. Spec Publ. Fish. Aquat. Sci.
58:62-67.
Bloom, S. A.
1981. Similarity indices in community studies: potential pit-
falls. Mar. Ecol. Prog. Ser. 5:125-128.
BOESCH, D. F., AND R. C. SWARTZ.
1977. Application of numerical classification in ecological in-
vestigations of water pollution. U.S. Environ. Prot. Agen-
cy Ecol. Res. Ser. EPA-600 3-77-033, 115 p.
Bowman, R. E.
1981. Food of 10 species of northwest Atlantic juvenile
groundfish. Fish. Bull., U.S. 79:200-206.
Brown, B. E., J. A. Brennan, M. D. Grosslein, E. G. Heyer-
DAHL, and R. C. HENNEMUTH.
1976. The effect of fishing on the marine finfish biomass in
the Northwest Atlantic from the Gulf of Maine to Cape Hat-
teras. Int. Comm. Northwest Atl. Fish. Res. Bull. 12:49-68.
Clark, S. H.
1979. Application of bottom trawl survey data to fish stock
assessment. Fisheries (Bethesda) 4(3):9-15.
Clifford, H. T., and W. Stephenson.
1975. An introduction to numerical classification. Acad.
Press, N.Y., 229 p.
Cohen, E. B., M. D. Grosslein, M. P. Sissenwine, and F.
Steimle.
1982. Energy budget of Georges Bank. In M. C. Mercer
(editor), Multispecies approaches to fishery management ad-
vice, p. 95-107. Can. Spec Publ. Fish. Aquat. Sci. No. 59,
169 p.
DeVries, T. J., AND W. G. Pearcy
1982. Fish debris in sediments of the upwelling zone off cen-
tral Peru: a late Quaternary record. Deep-Sea Res. 29:
87-109.
Gabriel, W. L., and A. V. TVler.
1980. Preliminary analysis of Pacific Coast demersal fish
assemblages. Mar. Fish. Rev. 42(3-4):83-88.
Grosslein, M. D.
1969. Groundfish survey program of BCF Woods Hole
Comm. Fish. Rev 31(8-9):22-30.
HOFF, J. G., AND R. M. iBARA.
1977. Factors affecting the seasonal abundance, composition,
and diversity of fishes in a southeastern New England
estuary Estuarine Coastal Mar. Sci. 5:665-678.
HOLLING, C. S.
1973. Resilience and stability of ecological systems. Annu.
Rev Ecol. Syst. 4:1-23.
Inglesias, J.
1981. Spatial and temporal changes in the demersal fish com-
munity of the Ria de Arosa (NW Spain). Mar. Biol. (Berl.)
65:199-208.
Keniston, J. A.
1978. Program cluster: an aid to numerical classification
using the CDC cyber computer. Greg. State Univ Sea Grant,
Pleuronectid Proj. Tfech. Rep. No 2, 32 p. OSU Mar. Sci. Ctr.,
Newport, OR.
Langton, R. H., and R. E. Bowman.
1981. Food of eight Northwest Atlantic pleuronectiform
fishes. U.S. Dep. Commer., NOAA Ifech. Rep. NMFS,
SSRF-749, 16 p.
McIntire, C. D.
1973. The distribution of estuarine diatoms along environmen-
tal gradients: a canonical correlation. Estuarine Coastal
Mar. Sci. 6:447-457.
Overholtz, W. J.
1982. Long-term temporal perspectives for the demersal fish
assemblages of Georges Bank with implications for manage-
ment and modeling. PhD. Thesis, Oregon State University,
Corvallis, 259 p.
Oviatt, C. a., and S. W. Nixon.
1973. The demersal fish of Narrangansett Bay: An analysis
of community structure, distribution, and abundance
Estuarine Coastal Mar. Sci. 1:361-378.
PiMENTEL, R. A.
1979. Morphometries: the multivariate analysis of biological
data. Kendal/Hunt Publ. Co., Dubuque, Iowa.
Pimm, S. L.
1984. The complexity and stability of ecosystems. Nature
(Lond.), 307:321-326.
Pitt, T K.
1970. Distribution, abundance, and spawning of yellowtail
flounder, Limanda ferrunginea, in the Newfoundland area
of the northwest Atlantic J. Fish. Res. Board Can.
27:2261-2271.
Richards, J., D. W Armstrong, J. R. G. Hislop, A. S. Jermyn,
and M. D. Nicholson.
1978. Trends in Scottish research vessel catches of various fish
species in the North Sea, 1922-1971. In G. Hempel (editor),
North Sea fish stocks - recent changes and their causes, p.
211-224. Rapp. P.-V. Reun. 172, 449 p.
Smith, S. H.
1972. Factors in ecological succession in oligotrophic fish com-
munities of the Laurentian Great Lakes. J. Fish. Res. Board
Can. 29:717-730.
SOUTAR, A., AND J. D. ISAACS.
1969. History of fish populations inferred from fish scales in
anaerobic sediments off California. Calif. Coop. Oceanic
Fish. Invest. Rep. 134:63-70.
Stephenson, W., and M. C. L. Dredge.
1976. Numerical analysis of fish catches from Serpentine
Creek. Proc R. Soc Queensl. 87:33-43.
Sutcliffe, W H., Jr., R. H. Loucks, and K. F. Drinkwater.
1976. Coastal circulation and physical oceanography of the
Scotian Shelf and the Gulf of Maine J. Fish. Res. Board
Can. 33:98-115.
Tyler, A. V.
1971. Periodic and resident components in communities of
Atlantic fishes. J. Fish. Res. Board Can. 28:935-946.
Tvler, a. v., W. L. Gabriel, and W J. Overholtz.
1982. Adaptive management based on structure of fish assem-
blages of northern continental shelves. In M. C. Mercer
(editor), Multispecies approaches to fishery management ad-
vice, p. 149-156. Can. Spec Publ. Fish. Aquat. Sci. No. 59,
169 p
Whittaker, R. H.
1967. Gradient analysis of vegetation. Biol. Rev. (Camb.)
42:207-264.
520
OBSERVER EFFECT ON INCIDENTAL DOLPHIN MORTALITY IN
THE EASTERN TROPICAL PACIFIC TUNA FISHERY
Bruce E. Wahlen' and Tim D. Smith^
ABSTRACT
Scientific observers placed aboard a sample of purse seine vessels collect data that are used to estimate
the total number of dolphins killed incidentally in the eastern tropical Pacific tuna fishery. If the presence
of these observers, who are not crew members, affects incidental kill levels, then the kill estimates will
be biased, lb test for the existence of such an observer effect, we compared dolphin kill data that had
been recorded by observers who differed in levels of obtrusiveness according to their purposes for data
collection. Some observers were placed on board primarily to collect data for estimating the total number
of dolphins killed annually. Other observers collected data both for that purpose and for monitoring com-
pliance with dolphin-release regulations. Our results confirm that the presence of an observer does affect
dolphin kill. The primary effect is an increase in the proportion of sets with no dolphins killed, and a
decrease in the proportion of sets with one to nine dolphins killed. While the magnitude of the effect
of observers cannot be estimated from our data, estimates of total dolphin mortality based on data col-
lected by the scientific observers are biased downward.
Schools of dolphins of several species, primarily
Stenella attenuata and 5. longirostris, have been
used since the late 1950s by purse seine fishermen
in the eastern tropical Pacific Ocean (ETP) to locate
and catch yellowfin tuna, Thunnus albacares. Per-
rin (1969) described the process of deploying, or set-
ting, the net around the tuna and dolphins, and then
releasing the dolphins while retaining the tuna.
Significant numbers of dolphins have been killed in-
cidentally in this fishery by becoming entangled in
the purse seines (Smith 1983).
The National Marine Fisheries Service (NMFS)
and the Inter-American Tropical Tbna Commission
(lATTC) place scientific observers who are not crew
members aboard a sample of tuna purse seine vessels
to collect data related to dolphin kill. Both the NMFS
and lATTC have used the data collected by these
scientific observers to estimate the total number of
dolphins killed annually by the entire tuna purse
seine fleet (Lo et al. 1982; Hammond and Tbai 1983).
Additionally, the NMFS uses these data to monitor
dolphin kills relative to annual kill limits establish-
ed for the U.S. registered fleet (Lo et al. 1982).
Periodic estimates of the cumulative numbers of
dolphins killed are compared with the annual limit.
If the limit is exceeded, U.S. vessels must stop fishing
on the affected populations for the remainder of the
year.
Data collected by the NMFS observers have also
been used to monitor compliance of vessel operators
with dolphin-release regulations, including the
release of all live dolphins from the net (Federal
Register 1977, 1980). Until recently data collected
by an NMFS observer could be used as evidence to
prosecute vessel operators for violations of these
regulations.
Observer effects have been defined in a general
context as measurement procedures which influence
and thereby change the behavior of the subject
(Johnson and Bolstad 1973, p. 38). Researchers have
encountered such effects in a variety of empirical
sciences, including psychology (Johnson and Bolstad
1973), social science (Webb et al. 1966, p. 18), and
biology (Ricker 1975, p. 87).
We defined an observer effect on the number of
dolphins killed as a differential in levels of dolphin
kill between trips made with and without a scien-
tific observer. The existence of such a differential
would introduce a bias into estimates of the total
number of dolphins killed (Smith 1983; Powers^).
Large numbers of sets involving dolphins (dolphin
sets) are made each year (Punsly 1983), so even a
moderate observer effect could result in a substan-
'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA 92038.
^Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA; pres-
ent address: Northeast Fisheries Center Woods Laboratory, Na-
tional Marine Fisheries Service, NOAA, Woods Hole, MA 02543.
Manuscript accepted November 1984.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
^Powers, J. E. 1979. A discussion of incidental mortality by
unobserved United States purse seiners. Unpubl. manuscr., 7
p. Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA 92038.
521
FISHERY BULLETIN: VOL. 83, NO. 4
tial bias in the estimates of annual dolphin kill.
Directly testing for the existence of an observer
effect on dolphin kills would require comparison of
covert observations with observations by NMFS and
lATTC observers. Based on the large difference be-
tween the kill rate observed covertly by one crew
member and the kill rates recorded by NMFS
observers during other fishing trips made by the
same operator and vessel, Smith (1983) speculated
that a large observer effect existed. We investigated
the significance of the difference in kill rates
reported by Smith (1983) by grouping NMFS-
observed trips into sequences of trips with common
operator and vessel. A few of these sequences of
NMFS-observed trips revealed between-trip kill rate
differences as large or larger than in the sequence
that included the covert observations.
The existence of an observer effect can be indirect-
ly tested without relying on data from covert
observers. Johnson and Bolstad (1973) established
the existence of an observer effect by comparing
measurements made by observers with various levels
of obtrusiveness to the human subjects whose
responses were being measured. They concluded that
the differences in the responses measured by
observers with different levels of obtrusiveness im-
plied that the observer's presence had affected the
subjects' behavior. They noted, however, that the
magnitude of an observer effect cannot be estimated
using this approach.
Following this indirect approach, we tested for the
existence of an observer effect on the numbers of
dolphins killed by comparing dolphin kill data col-
lected by scientific observers who differed in their
purposes of data collection, and hence, in their levels
of obtrusiveness.
DATA
The scientific observers were placed aboard a ran-
dom sample of U.S. registered tuna purse seine
vessels (Lo et al. 1982). Assignment of an NMFS or
lATTC observer to vessels in the sample was also
made randomly, subject to the constraint that any
vessel sampled twice within a calendar year would
be accompanied by an NMFS observer on at most
one trip (Ikble 1).
Information collected for each NMFS- or lATTC-
sampled fishing trip included departure date and
data pertaining to each set (such as set type, date,
and location), and for dolphin sets, the number of
dolphins killed. Data available to the authors from
NMFS-sampled trips included all of this information.
However, data available from lATTC-sampled trips
did not include departure date, and set dates were
available only to the quarter of the year.
While the data items collected by both types of
scientific observer have been similar over the years,
for NMFS observers the purposes of the data col-
lection changed after March 1981. The primary pur-
poses of data collection, as explained to each vessel
operator at a placement meeting held prior to depar-
ture, were as follows: 1) On NMFS-sampled trips
begun from 1978 through March 1981, data were col-
lected for estimating the annual kill of dolphins and
for monitoring compliance with dolphin-release
regulations; 2) on NMFS-sampled trips begun after
March 1981 through the end of 1982, the data were
still used for estimating dolphin kills but were no
longer used to monitor compliance with dolphin-
release regulations''; 3) on all lATTC-sampled trips,
since the inception of that sampling program in 1979,
data were collected for estimating total kill but were
never collected for monitoring compliance with
dolphin-release regulations.
As described above, the data collected by both
NMFS and lATTC observers to estimate total
dolphin kill can be used by the NMFS to halt fishing
by U.S. vessels on specific dolphin populations for
the remainder of the year. The data collected before
March 1981 by the NMFS observers for monitoring
compliance with dolphin-release regulations,
however, can be used by the NMFS as evidence to
prosecute operators who failed to comply. Thus, the
operators are likely to be more conscious of the
presence of an observer who is collecting data both
for estimating dolphin kill and for monitoring com-
■*The change in data collection purposes of NMFS observers after
March 1981 was prompted by a court order forbidding the NMFS
from using data collected by observers for monitoring compliance
with dolphin-release regulations. No NMFS observers were
placed on fishing trips begun from 1983 through part of 1984
because of a subsequent court order forbidding placement of NMFS
observers without a search warrant.
Table 1. — Number of observed fishing trips which made
at least one dolphin set from 1978 through 1982, by
observer type and year. NMFS totals are subdivided ac-
cording to departure date of trips (previous year, Jan.-IVIar.,
Apr-Dec.) and exclude trips in which fishing gear research
was conducted.
Observer type
1978
1979
1980
1981
1982
NMFS
Previous
year
5
4
3
3
7
Jan.-Mar.
44
33
15
7
13
Apr.-Dec.
56
32
28
28
18
Total
105
69
46
38
38
lATTC
0
31
57
58
44
Total
105
100
103
96
82
522
WAHLEN AND SMITH: OBSERVER EFFECT ON INCIDENTAL DOLPHIN MORTALITY
pliance with dolphin-release regulations than an
observer who is collecting data only for estimating
dolphin kill. That this is the case is implied by the
constraint in the sampling procedure that any vessel
sampled twice within a calendar year may be accom-
panied by an NMFS observer on at most one trip.
METHODS
We tested for the existence of an observer effect
on dolphin kills by comparing the number of killed
dolphins recorded by more obtrusive observers with
the number recorded by less obtrusive observers. We
considered observers who collected data both for
estimating dolphin kill and for monitoring com-
pliance with dolphin-release regulations to be more
obtrusive to vessel operators than observers who col-
lected data only for estimating dolphin kill. Thus,
we compared kills recorded by (la) NMFS observers
before and after March 1981, and (lb) NMFS and
lATTC observers before March 1981. As a control,
we compared the number of killed dolphins record-
ed by observers of equal obtrusiveness. That is, we
compared kills recorded by (2a) lATTC observers
before and after March 1981, and (2b) NMFS and
lATTC observers after March 1981.
The frequency distributions of numbers of dolphins
killed were extremely skewed, with very long right
tails (Fig . 1). Normality assumptions were violated
so strongly by these skewed distributions that
ANOVA tests for differences in means, particularly
one-sided tests, would be difficult to interpret (Glass
et al. 1972). Therefore, we tested for differences in
the percent of dolphin sets in which no dolphins were
killed (zero-kill sets). This percent relates directly to
the regulation requiring release of all live dolphins,
and is a dominant feature of the dolphin kill
distributions.
When comparing frequency distributions, we
entertained the null hypothesis of equality of per-
cent zero-kill sets. When comparing observers of dif-
ferent obtrusiveness levels, we tested this hypothesis
against a one-sided alternative that distributions
from more obtrusive observers had a higher percent
Before
After
>■
o
z
111
3
O
Ui
oc
u.
lU
>
<
lit
flC
Ma
r. 1981
Mar
. 1981
TRIPS
215
59
DOLPHIN SETS
4.780
1,634
MEAN
3.24
5.21
STD. DEV.
22.83
21.79
MAXIMUM
854
387
^
^ ■ — ^ — p^^ . — p
i—V/Z/i
1-9 10-19 20-29 30-39 40-49 50-99 ^100
NUMBER OF DOLPHINS KILLED
Figure L— Relative frequency distributions of number of dolphins killed incidentally during sets
of NMFS-observed trips, 1978 through 1982, by trip departure data
523
FISHERY BULLETIN: VOL. 83, NO. 4
of zero-kill sets than distributions from less obtrusive
observers. When comparing distributions from
observers of equal obtrusiveness, we tested the null
hypothesis against the two-sided alternate of in-
equality (Tkble 2). Results from all of our tests are
reported at the 0.05 significance level.
Table 2. — Alternate hypotheses to the null hypothesis of
equality of percent zero-kill sets for each of tour comparisons,
where Before and After refer to before or after March 1981.
See text for details.
Comparison
Alternate hypothesis
1a. NMFS before vs NMFS after Before > After
2a. lATTC before vs lATTC after Before # After
lb. NMFS before vs lATTC before NMFS > lATTC
2b. NMFS after vs lATTC after NMFS # lATTC
For two-sided tests of differences in percents, we
used the standard chi-square (x^) statistic with
one degree of freedom (df). For one-sided tests,
we used the square root of the chi-square statistic
(Z), which is approximately normal (Snedecor and
Cochran 1980, p. 126-127). In some instances, the
expected cell frequencies were less than the tradi-
tionally accepted minimum of five. However,
recent Monte Carlo results (Fienberg 1980, p. 172)
suggest that the chi-squared distribution is an ade-
quate approximation at the 0.05 significance level
even when minimum expected values are as low as
one.
While the sampling of vessels was nearly random,
the actual sample obtained may not have been
representative of factors affecting dolphin kills. It
has been demonstrated that within the ETP, dolphin
kills vary among three geographic areas^ (Fig. 2) and
by periods within the year (Lo et al. 1982). We
divided the year into two periods: January-March
and April-December. This division corresponds to
the date of the change in data collection purposes
of NMFS observers in 1981, and also tends to
equalize sample size since vessels in this fishery are
more active in the early part of the year.
We stratified the data by area and period of the
year to account for biases due to possible non-
representativeness of the sample with respect to
these two factors. When data on numbers of dolphins
killed were available in all six area-period strata, we
made overall two-sided tests for differences in per-
^K-T. T^ai, Inter-American IVopical Thna Commission, c/o Scripps
Institute of Oceanography, La Jolla, CA 92093, pers. commun.
December 1983.
40°N
20" -
20° -
ACS
1
e
\
1
)
-
NORTH
20"
\
N.
^Vv/7
-
OUTSIDE
5
o
O
5"N.
N0RTH^~-1 ")
INSIDE S!^
/ -
3
0
C
T
►
»
1
SOUTI
1
H
1
/
lecw
140°
120"
100°
80°
Figure 2.— The three areas of the eastern tropical Pacific used to stratify the data, bounded
by lat. 40°N., long. 160°W., lat. 40°S., and the western coastline of the North and South
American Continents.
524
WAHLEN AND SMITH: OBSERVER EFFECT ON INCIDENTAL DOLPHIN MORTALITY
cent zero-kill sets (conditional on period of the year
and geographic area) by summing chi-square values
and degrees of freedom from each stratum. When
observations were not available in one of the strata,
or when the alternative was one-sided, an overall test
based on the chi-square statistic was not possible
In those cases, results of the tests within each
stratum were considered separately.
RESULTS
The first two comparisons of frequency distribu-
tions test for differences in the percent of zero-kill
sets in data collected by observers on trips begun
before compared with trips begun after the change
in NMFS observer data collection purposes in March
1981 (Comparisons la and 2a, Tkble 2). The last two
comparisons test for differences in the percent of
zero-kill sets in data collected by observers on trips
begun during the same time period (Comparisons
lb and 2b, Table 2).
Before versus After
The percent of zero-kill sets for NMFS-observed
trips was higher before March 1981 than after that
date (Fig. 1), and within all area-period strata with
complete data, the percent of zero-kill sets was larger
before March 1981 (Tkble 3). The one-sided test of
this difference (Comparison la, Tkble 2) was signi-
ficant within four of the five area-period strata which
had complete data, and was very nearly significant
within the fifth (Tkble 3). Thus, the percent of zero-
kill sets recorded by NMFS observers was signifi-
cantly larger before March 1981.
The significant difference in percent of zero-kill
sets for NMFS observers before compared with after
March 1981 could be due to the change in data collec-
tion purposes of NMFS observers which occurred
then. Alternatively, the difference could be due to
a temporal decline begun before that date.
Allowing for period, the data prior to March 1981
do not show a pronounced trend for any of the three
areas (Fig. 3). Although there appears to be a decline
in the South for Period 2, this is unreliable as it
depends entirely on the 1980 and 1981 data points
representing a total of only 17 sets. Similarly, there
seems to be a declining trend for the two northern
areas. However, for the North Inside area the Period
1 points show no decline, and the possible decline
of Period 2 points depends on the 1980 Period 2
point. A 95% confidence interval about this point
(observed percent +2 x standard error), however,
is large relative to the difference between it and the
Period 2 point of 1979. Further, any such declining
trend in Period 2 points for the North Inside area
is not reflected in the low 1978 point. A similar argu-
ment can be made for North Outside area data to
reject the alternative explanation of the difference
in percent zero-kill sets before and after March 1981
being the result of a temporal trend begun prior to
March 1981.
That the differences in percent of zero-kill sets for
NMFS-observed trips was not due to a temporal
trend was also tested by comparing the percent of
such sets for lATTC-observed trips before and after
March 1981. The percent of zero-kill sets for lATTC-
observed trips was higher before March 1981, but
within the six area-period strata the differences were
not consistent (Tkble 4). The two-sided test (Com-
parison 2a, Tkble 2) was significant within only one
of the six area-period strata (Period 1, South), and
the sample size within that stratum was very small
(Tkble 4). The overall conditional test given area and
period was not significant. Thus, I ATTC -observed
trips with dolphin sets from 1979 through 1982 did
Table 3.— Numbers of dolphin sets (n) made during NMFS-observed trips, 1978 through 1982. Sets are classified by trip departure date
relative to March 1981 (before or after) and to period (1 - Jan.-Mar, 2 = Apr-Dec), by area of set (North Inside, North Outside, South),
and by numbers of dolphins killed (0, X)). Percents of column totals (%), expected frequencies (e), and the statistic Z are also tabulated.
Values of Z > 1.64 are significant, as indicated by an asterisk.
Period 1
Period 2
Tol
North Inside
Before After
North Outside
Before After
South
North Inside
Before After
North Outside
Before After
South
tal
Kill
Before
After
Before
After
Before
After
0
n
1,498
226
0
21
107
0
972
421
591
229
86
33
3,254
930
%
72.9
62.1
—
52.5
61.1
0.0
69.4
62.7
60.4
55.7
50.6
23.1
68.1
56.9
e
1,464.7
259.3
0
21
104.0
3.0
941.9
451.1
577.4
242.6
64.6
54.4
—
—
>0
n
558
138
0
19
68
5
429
250
387
182
84
110
1,526
704
%
27.1
37.9
—
47.5
38.9
100.0
30.6
37.3
39.6
44.3
49.4
76.9
31.9
43.1
e
591.3
104.7
0
19
71.0
2.0
459.1
219.9
400.6
168.4
105.4
88.6
—
—
Total
n
2,056
364
0
40
175
5
1,401
671
978
411
170
143
4,780
1,634
Z
4.18*
2.75*
3.0-
1*
1.63
4.99*
.1
'Computation of overall test statistic not possible because of one-sided alternative, and because of lack of data in one stratum (Period 1, North Outside).
525
FISHERY BULLETIN: VOL. 83, NO. 4
532 528 978 527 403 346 143 326 364 345 NIS
0 534 0 263 0 181 0 270 40 141 NOS
45 64 75 92 55 14 0 3 5 140 S
80 I-
O
K
lU
o.
1978
Figure 3— Number of dolphin sets (upper portion) and percent of zero-kill dolphin sets (lower
portion) for each of 3 areas (NIS = North Inside, NOS = North Outside, S = South) by period
within year (open symbol = Jan.-Mar., closed symbol = Apr.-Dec). Data are from NMFS-observed
trips, 1978 through 1982. Vertical line separates data before and after March 1981.
Table 4.— Numbers of dolphin sets (n) made from 1979 through 1982, during lATTC-observed trips. Sets are classified by date of set
relative to March 1981 (before or after) and to period (1 = Jan.-Mar., 2 = Apr.-Dec), by area of set (North Inside, North Outside, South),
and by numbers of dolphins killed (0, X)). Percents of column totals (%), expected frequencies (e), and the statistic x^ with degrees
of freedom (df) are also tabulated. Values of x^ > 3.84 (1 df) or 12.59 (6 df) are significant, as Indicated by an asterisk.
Period 1
Period 2
To
North Inside
Before After
North Outside
Before After
South
North Inside
Before After
North Outside
Before After
South
tal
Kill
Before
After
Before
After
Before
After
0
n
537
188
9
3
13
3
709
721
291
328
5
35
1,564
1,278
%
67.1
71.2
26.5
14.3
38.2
12.0
70.0
70.1
58.7
55.6
33.3
24.1
65.4
61.6
e
545.1
179.9
7.4
4.6
9.2
6.8
709.8
720.2
282.7
336.3
3.8
36.2
—
—
>0
n
263
76
25
18
21
22
304
307
205
262
10
110
828
795
%
32.9
28.8
73.5
85.7
61.8
88.0
30.0
29.9
41.3
44.4
66.7
75.9
34.6
38.4
e
254.9
84.1
26.6
16.4
24.8
18.2
303.2
307.8
213.3
253.7
11.2
108.8
—
—
Total
n
800
264
34
21
34
25
1,013
1,028
496
590
15
145
2,392
2,073
X2
1.53
1.
13
5.02*
0.01
1.04
0.61
9.34
df
1
1
1
1
1
1
6
526
WAHLEN AND SMITH: OBSERVER EFFECT ON INDICENTAL DOLPHIN MORTALITY
not differ significantly in their percent of zero-kill
sets before or after March 1981.
Same Time Period
Before March 1981 the percent of zero-kill sets was
higher for NMFS-observed trips than for lATTC-
observed trips (Fig. 4), and within all area-period
strata with complete data, the percent of zero-kill
sets was larger for the NMFS observers (Ikble 5).
The one-sided test (Comparison lb, Ikble 2) was
significant within four of the five area-period strata
which had complete data (Tkble 5). Thus, for trips
making dolphin sets from 1979 through March 1981,
NMFS observers recorded a significantly higher per-
cent of zero-kill sets than did lATTC observers.
According to our hypothesis, the difference in per-
cent of zero-kill sets between NMFS- and lATTC-
observed trips before March 1981 should have disap-
peared after March 1981 when the purposes for data
collection of NMFS observers became nearly the
same as for lATTC observers. After March 1981 the
percent of zero-kill sets was higher for lATTC-
observed trips than for NMFS-observed trips (Fig.
5), but within the six area-period strata the dif-
ferences were not consistent (Table 6). The two-sided
test (Comparison 2b, Tab\e 2) was significant within
only one of the six area-period strata (Period 1,
North Inside), yet this one chi-square statistic was
so large that the overall conditional test for all six
strata was also significant (Ihble 6). It is difficult to
interpret the overall result in this situation because
of the extraordinary influence of one stratum.
However, after March 1981 the percent of zero-kill
sets on NMFS-observed trips was clearly not higher
than on lATTC-observed trips.
While one would expect the mean number of
dolphins killed to decrease when the percent of zero-
kill sets increases, this is not necessarily so because
of the sensitivity of the mean of a sample to the max-
imum value in the sample For instance, in Figure
4 the NMFS maximum is nearly twice that of the
lATTC, resulting in a larger NMFS mean despite the
higher percent of zero-kill sets in the NMFS sample
>■
O
z
Ui
o
lU
e
11.
lU
>
UI
flC
NMFS
lATTC
w
TRIPS
119
104
DOLPHIN SETS
3,080
2,392
MEAN
2.87
2.75
STD. DEV.
21.58
16.28
MAXIMUM
854
447
I ^ . — p^
T
=p
=f
0 1-9 10-19 20-29 30-39 40-49 50-99 ^100
NUMBER OF DOLPHINS KILLED
Figure 4.— Relative frequency distributions of number of dolphins killed incidentally during sets
made from 1979 through March 1981, by observer type
527
FISHERY BULLETIN: VOL. 83, NO. 4
>-
u
z
lU
3
o
lU
tr
u.
UJ
>
u
c
NMFS
lATTC
m
TRIPS
64
85
DOLPHIN SETS
1,675
2,073
MEAN
6.16
3.60
STD. DEV.
21.98
13.97
MAXIMUM
387
268
J yf/!A [ W— ~
1-9 10-19 20-29 30-39 40-49 60-99 ^100
NUMBER OF DOLPHINS KILLED
Figure 5.— Relative frequency distributions of number of dolphins killed incidentally during sets
made after March 1981 through 1982, by observer type
Table 5.— Numbers of dolphin sets (n) made from 1979 through March 1981. Sets are classified by observer type (NMFS, lATTC), by area
of set (North Inside, North Outside, South), by date of set relative to period (1 = Jan.-Mar., 2 = Apr.-Dec), and by numbers of dolphins
killed (0, >0). Percents of column totals (%), expected frequencies (e), and the statistic Z are also tabulated. Values of Z > 1.64 are signifi-
cant, as indicated by an asterisk.
Period 1
Period 2
North Inside
NMFS lATTC
North Outside
NMFS lATTC
South
North Inside
North Outside
NMFS lATTC
South
Total
Kill
NMFS
lATTC
NMFS
lATTC
NMFS
lATTC
NMFS lATTC
0
n
820
537
0
9
96
13
942
709
267
291
62
5
2,187 1,564
%
72.7
67.1
—
26.5
53.9
38.2
76.8
70.0
60.1
58.7
59.6
33.3
71.0 65.4
e
793.9
563.1
0
9
91.5
17.5
904.0
747.0
263.6
294.4
58.6
8.4
— —
>0
n
308
263
0
25
82
21
284
304
177
205
42
10
893 828
%
27.3
32.9
—
73.5
46.1
61.8
23.2
30.0
39.9
41.3
40.4
66.7
29.0 34.6
e
334.1
236.9
0
25
86.5
16.5
322.0
266.0
180.4
201.6
45.4
6.6
— —
Total
n
1,128
800
0
34
178
34
1,226
1,013
444
496
104
15
3,080 2,392
Z
2.64*
-
1.68*
3.66*
0.46
1.92*
1
'Computation of overall test statistic not possible because of one-sided alternative, and because of lack of data In one stratum (Period 1, North Outside).
DISCUSSION AND CONCLUSIONS
We established the existence of an observer effect
on the number of dolphins killed incidentally in the
ETP yellowfin tuna fishery by following two lines
of argument. First, we demonstrated a decrease in
the percent of sets with no dolphins killed on NMFS-
observed trips after March 1981, when monitoring
compliance with dolphin-release regulations was
removed as a data collection purpose (Ikble 3). We
further showed that this difference was not due to
a temporal trend in fishing conditions by examin-
528
WAHLEN AND SMITH: OBSERVER EFFECT ON INCIDENTAL DOLPHIN MORTALITY
Table 6.— Numbers of dolphin sets (n) made from April 1981 through 1982. Sets are classified by observer type (NMFS, lATTC), by area
of set (North Inside, North Outside, South), by date of set relative to period (1 = Jan.-f\/lar., 2 = Apr-Dec), and by numbers of dolphins
killed (0, >0). Percents of column totals (%), expected frequencies (e), and the statistic x^ with degrees of freedom (df) are also tabulated.
Values of x^ > 3.84 (1 df) or 12.59 (6 df) are significant, as Indicated by an asterisk.
Period 1
Period 2
To
North Inside
NMFS lATTC
North Outside
NMFS lATTC
South
North Inside
NMFS lATTC
North Outside
NMFS lATTC
South
tal
Kill
NMFS
lATTC
NMFS
lATTC
NMFS
lATTC
0
n
193
188
1
3
1
3
455
721
249
328
13
35
912
1,278
%
55.6
71.2
14.3
14.3
10.0
12.0
66.4
70.1
56.1
55.6
15.9
24.1
57.9
61.6
e
216.4
164.6
1.0
3.0
1.1
2.9
470.3
705.7
247.8
329.2
17.3
30.7
—
—
>0
n
154
76
6
18
9
22
230
307
195
262
69
110
663
795
%
44.4
28.8
85.7
85.7
90.0
88.0
33.6
29.9
43.9
44.4
84.1
75.9
42.1
38.4
e
130.6
99.4
6.0
18.0
8.9
22.1
214.7
322.3
196.2
260.8
64.7
114.3
—
—
Total
n
347
264
7
21
10
25
685
1,028
444
590
82
145
1,575
2,073
X2
15.53*
0.00
0.03
2.63
0.02
2.16
20.37*
df
1
1
1
1
1
1
6
ing the data by period (Fig. 3) and by demonstrating
the lack of a corresponding change in data collected
by lATTC observers (Tkble 4).
Second, we demonstrated that before March 1981
the percent of sets with no dolphins killed was higher
for NMFS observers collecting data both for esti-
mating dolphin kill and for monitoring compliance
with dolphin-release regulations than for lATTC
observers collecting data only for estimating dolphin
kill (Tkble 5). Tb validate this comparison we also
demonstrated that the difference disappeared, or
perhaps was reversed, following March 1981 when
monitoring compliance with dolphin-release regula-
tions was removed from the NMFS observers'
responsibilities (Tkble 6). Following Johnson and
Bolstad (1973), these differences in the data collected
by observers differing in their purposes of data col-
lection, and hence in their obtrusiveness, imply the
existence of an observer effect.
In making these comparisons, we stratified the
data to account for possible differences in fishing
conditions in different geographic areas and
throughout the year because both area and time of
year are important determinants of dolphin mor-
tality. Thus, the differences in the percent of zero-
kill sets which we identified cannot be attributed to
nonrepresentativeness of the data with respect to
area and time of year.
We did not attempt to test for other differences
in the frequency distributions of kills, such as
changes in the percent of moderate or large kill sets.
Sets with large numbers of dolphins killed are rare,
and are generally associated with unusual circum-
stances, such as mechanical failures. The percent of
sets v^th 1-9 dolphins killed appears to vary inversely
with the percent of sets with zero dolphins killed
(Figs. 1, 4, 5).
Powers et al.^ showed that the use of some dolphin-
release procedures significantly reduces dolphin
mortality. Thus, more time and effort expended by
the operator on release of dolphins could result in
an increase in the frequency of sets with no dolphins
killed, and a corresponding decrease in the frequency
of sets with 1-9 dolphins killed. A greater tendency
for vessel operators to take the additional time in
the presence of an observer collecting data for
monitoring compliance with dolphin-release regula-
tions could account for the differences we have
demonstrated.
The significantly different relative frequency of
zero-kill sets recorded by NMFS observers after
March 1981 (Tkble 6) was not expected under our
hypothesis. As noted above, this difference was
localized to one area-period stratum, and the other
five strata were consistent with the null hypothesis
of no difference Either this difference is merely a
sampling anomaly, or there are differences between
observers in more recent years that we have not
taken into account.
Gulland (1983, p. Ill) described a method of
testing for the existence of a tagging effect that is
analogous to our indirect method of testing for an
observer effect. He suggested comparing the pro-
portions of tags returned from fish tagged under
poor and good conditions. In both Gulland's and our
methods, the absolute magnitude of the effects can-
not be estimated. For instance, in Gulland's exam-
ple improvement in the conditions under which tags
are applied is unlikely to eliminate entirely the tag-
ging effect. Similarly, the reduction in observer ob-
«Powers, J. E., N. C. H. Lo, and B. E. Wahlen. 1979. A statis-
tical analysis on effectiveness of porpoise rescue procedures in
reducing incidental mortality. Southwest Fish. Cent. La JoUa Lab.,
Natl. Mar. Fish. Serv., NOAA, Admin. Rep. LJ-79-7, 29 p.
529
FISHERY BULLETIN: VOL. 83, NO. 4
trusiveness after March 1981 is unlikely to have
eliminated entirely the observer effect because the
data collected by scientific observers after 1981 were
still used to monitor dolphin kills relative to annual
kill limits. Observers collecting data that could not
be used for monitoring kill limits would be even less
obtrusive than the scientific observers, and covert
observers would be, of course, completely unobtru-
sive
Based on our analysis, we would expect that the
frequency of zero-kill sets would be lower on
unobserved vessels than on vessels with a scientific
observer. This lower frequency of zero-kill sets, cou-
pled with an increased frequency of sets with 1-9
dolphins killed, suggests that the average kill rate
on unobserved vessels would be higher. Estimates
of total kill, based on the average kill rates from the
scientific observers, would therefore be underesti-
mated.
ACKNOWLEDGMENTS
We gratefully acknowledge the assistance of M.
M. Groom in providing data and in early discussions
of the problem. We also acknowledge the assistance
of K. E. Wallace and J. S. Cole in providing data.
We are indebted to D. G. Ghapman and W. F. Perrin
for suggesting analytical methods. We also ap-
preciate the helpful reviews by F. G. Alverson, I. Bar-
rett, P. S. Hammond, R. S. Holt, N. G. H. Lo, N. A.
Mendes, J. M. Michalski, G. T. Sakagawa, and K.-T.
'Rai, as well as the reveiws by two anonymous
individuals.
LITERATURE CITED
Federal Register.
1977. Department of Commercei NOAA, Ikking of marine
mammals incidental to commercial fishing operations; final
decision and final regulations. Fed. Regist. 42(247);64548-
64560.
Federal Register.
1980. Department of Commerce, NOAA, Taking of marine
mammals incidental to commercial fishing operations-
permits, eta Fed. Regist. 45(213):72178-72196.
Fienberg, S. E.
1980. The analysis of cross-classified categorical data. 2d ed.
MIT Press, Cambridge, MA, 198 p.
Glass, G. V., R D. Peckham, and J. R. Sanders.
1972. Consequences of failure to meet assumptions under-
lying the fixed effects analyses of variance and covariance
Rev. Edua Res. 42(3):237-288.
Gulland, J. A.
1983. Fish stock assessment: a manual of basic methods.
John Wiley and Sons, N.Y., 223 p.
Hammond, P. S., and K.-T I^ai.
1983. Dolphin mortality incidental to purse-seining for tunas
in the eastern Pacific Ocean, 1979-81. Rep. Int. Whaling
Comm. 33:589-597.
Johnson, S. M., and 0. D. Bolstad.
1973. Methodological issues in naturalistic observation: some
problems and solutions for field research. In L. A.
Hamerlynck, L. C. Handy, and E. J. Mash (editors). Behavior
change: methodology, concepts, and practice, p. 7-67.
Research Press, Champaign, IL.
Lo, N. C. H., J. E. Powers, and B. E. Wahlen.
1982. Estimating and monitoring incidental dolphin mortali-
ty in the eastern tropical Pacific tuna purse seine
fishery. Fish. Bull., U.S. 80:396-401.
Perrin, W F
1969. Using porpoise to catch tuna. World Fishing 18(6):
42-45.
PUNSLY, R. G.
1983. Estimation of the number of purse-seiner sets on tuna
associated with dolphins in the eastern Pacific Ocean dur-
ing 1959-1980. [In Engl, and Span.] Inter-Am. Trop. TUna
Comm. Bull. 18:229-299.
RiCKER, W E.
1975. Computation and interpretation of biological statistics
of fish populations. Bull. Fish. Res. Board Can. 191, 382 p.
Smith, T D.
1983. Changes in size of three dolphin (Stenella spp.) popula-
tions in the eastern tropical Pacific Fish. Bull., U.S. 81:1-13.
Snedecor, G. W, and W. G. Cochran.
1980. Statistical methods. 7th ed. Iowa State University
Press, Ames, lA, 507 p.
Webb, E. J., D. T. Campbell, R. D. Schwartz, and L. Sechrest.
1966. Unobtrusive measures: a survey of non-reactive research
in the social sciences. Rand McNally, Chic, 225 p.
530
FOOD HABITS OF JUVENILE ROCKFISHES (SEBASTES)
IN A CENTRAL CALIFORNIA KELP FOREST
Michael M. Singer^
ABSTRACT
The diets and feeding morphology of juveniles of seven rockfish species (Scorpaenidae: Sebastes) were
investigated in a kelp forest at Stillwater Cove, Carmel Bay, CA. The seven species could be divided into
two groups, those which fed primarily on open water prey in the water column and those which fed on
substrate-associated prey. Substrate-associated prey were generally larger than open water prey and were
eaten by predators with relatively larger heads and mouths and shorter gill rakers. Comparison of juvenile
diets and foraging patterns with those of adults showed that both foraged in similar manners and in the
same general habitats. The absence of aggressive interactions within or among species and high intra-
specific variability of foraging patterns suggests that little interference or exploitative competition was
present.
Most of the literature on rockfishes deals mainly with
aspects of either adult or larval biology (DeLacey
et al. 1964; Phillips 1964; Miller and Geibel 1973;
Westrheim 1975; Larson 1980a, b, c). Little of this
literature deals with the juvenile stage. Juvenile rock-
fishes often use nearshore kelp beds as nursery
grounds and, during certain times of the year, are
the most abundant members of the kelp-forest fish
community (Burge and Schultz 1973). The change
from pelagic life to a nearshore, reef-dwelling ex-
istence represents a major ecological transition.
With so many juvenile rockfish species co-occurring
in kelp forests, the potential for competitive inter-
action is great. Gaining an understanding of these
fishes' patterns of resource utilization (eg., food or
space) may be important in assessing the
mechanisms that affect their survival.
The purpose of this study was threefold: 1) to in-
vestigate the food habits of juvenile rockfishes oc-
curring in a nearshore kelp forest, 2) to determine
the extent to which diet differed within and among
the various species present, and 3) to compare the
relationship between diet and morphology in juvenile
and adult forms.
The juveniles of seven rockfish species were
studied. The adults of six of these species usually
occur nearshore, in association with rock reefs: blue
rockfish, S. mystinus; black rockfish, S. melanops;
olive rockfish, S. serranoides; copper rockfish, S.
caurinus; gopher rockfish, S. camatus; and kelp
rockfish, S. atrovirens (Hallacher 1977; Roberts
1979). Adults of the seventh species, the canary rock-
fish, S. pinniger, occur deeper and usually offshore
(Miller and Lea 1972). For purposes of this study,
an individual was designated a juvenile upon first
appearance in the kelp forest, where fish were usual-
ly 25 to 30 mm SL. The fish used in this study
generally ranged from 30 to 70 mm SL.
Sebastes mystinus and S. pinniger are among the
earliest species to recruit, usually appearing as early
as April. Sebastes mystinus usually occurs in the
water column above 6 m while S. pinniger occurs
on the substrate usually near sand/rock interfaces.
Sebastes caurinus begins recruiting around late
April or May and is found initially among kelp fronds
and near the surface Next to arrive are S. ser-
ranoides and S. melanops which first appear in May
and June Both these species occur mostly in the mid-
water within the kelp forest. Sebastes camatus usual-
ly begins to recruit in late June and July and, like
S. caurinus, is found initially among kelp fronds at
the surface Both S. caurinus and S. camatus move
down from the canopy and take positions near the
bottom after a couple of months (around June or July
for S. caurinus and late August or September for
S. camatus). The last of these species to recruit is
S. atrovirens, which begins to appear in late July
and August and occurs in the surface kelp canopy.
METHODS AND MATERIALS
^Moss Landing Marine Laboratories, Moss Landing, CA; present
address: VANTUNA Research Group, Occidental College, Moore
Laboratory of Zoology, 1600 Campus Road, Los Angeles, CA 9004L
Manuscript accepted November 1984.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
Study Site
All observations and samples were taken between
531
May 1980 to October 1981 at a rock reef at Arrow-
head Point in Stillwater Cove, Carmel Bay, CA (about
lat. 36°33.6'N, long. 121°56.3'W). Bottom depths at
the study site averaged about 12.5 m below MLLW
(mean low low water). The reef was roughly tri-
angular, bounded by sand flats which sloped into
deeper water on all but the nearshore side (Fig. 1).
The reef substrate was composed of both high and
low relief basaltic rock interspersed with areas of
coarse, granitic sand and a few patches of worm
tubes (Diopatra sp.). Stillwater Cove is protected
from the prevailing north and northwest swells and
winds. However, it is exposed to the most severe
southerly storms which commonly occur from Oc-
tober to February.
The rock substrate was covered with an extensive
mat of coralline algae and sessile invertebrates. The
dominant algal form was the giant kelp, Macrocystis
pyrifera, which became very thick in the summer
months and represented a major structural compo-
nent of the reef. Except for corallines, understory
algae (Pterogophora californica, Cystoseira osmun-
dacea, and seasonally dense patches of Desmarestia
ligulata) were relatively sparse and patchy. Des-
marestia abundance increased in the fall as the sur-
face kelp canopy decreased. Drift algae of several
types entered the reef at times and often became
a major microhabitat. It usually occurred along the
sand/rock interface or in low patches in the interior
of the reef.
Field Collections
All fish used for stomach content analysis were
collected with almxlmxl.Sm opening-closing,
diver-held net. The net was constructed of 1/8-in
stretch-mesh nylon netting on a 1/4-in PVC frame
mouth. The mouth of the net was hinged in the mid-
dle with tygon tubing. This allowed easy operation
by a single diver in close spaces. Collected fish were
brought to the surface and the stomachs injected
with 10% Formalin^. The fish were then preserved
whole in 10% Formalin, then washed in freshwater,
and stored in 70% ethanol.
The majority of fish collected for gut analysis were
taken from June to August of both 1980 and 1981
with some supplemental collections occurring in Oc-
tober and November of 1980. Collections were made
during both day and night.
^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
FISHERY BULLETIN: VOL. 83, NO. 4
Laboratory Methods
Each fish was blotted dry and weighed to the
nearest 0.01 g. The entire visceral mass was re-
moved, and the stomach and intestine were then
separated from the remaining viscera. The contents
of each stomach were emptied into a small dish and
examined under a binocular dissecting scopa Food
items were separated by general taxonomic category
(eg., calanoid copepods, zoea larvae, mysid shrimp,
etc). These general categories were used because not
all prey items found were in good enough condition
to identify to species, thus identifying some items
further than others could be misleading. Each
category was enumerated by number and percent
volume The percent of the total stomach volume of
each prey type was estimated by spreading the con-
tents to a uniform thickness over a background grid
and then estimating the area represented by each
type Since contents were spread to an equal thick-
ness, area and volume were considered directly pro-
portional. Digestive state of contents was estimated
on a subjective one to five scale (DeWitt and Cailliet
1972). In addition, a subset of each prey type was
taken from stomach contents and measured along
its longest axis to the nearest 0.005 mm using an
ocular micrometer for later estimation of mean sizes
of each prey type
Analytical Methods
A plot of cumulative number of prey types against
randomly pooled number of stomachs was con-
structed for each species in order to assess adequacy
of sample sizes. An asymptotic leveling of this type
of plot indicates a sufficient sample size The mean
percent by estimated volume (%V) and by number
(%N) of each prey type were calculated for each fish
species as an average of all values for individual
specimens. The mean frequency of occurence (%F0)
was also calculated for each prey type in each
predator as the number of times the prey type
was seen divided by the total of stomachs exam-
ined. The importance of each prey type was
calculated using the index of relative importance
(IRI) described by Pinkas et al. (1971). The IRI
used the proportion by amount (%N), volume
(%V), and occurrence (%F0) of each prey type
(IRI = (%N + %V) X %F0). The diets of the
seven species studied were compared using the
percent similarity index (PSI) (Whittaker
1952): PSI = 1 - 0.5 I pih - pjh. Where pi and
pj are the proportions by IRI of each prey type (h)
in the two predators being compared. In calculating
532
SINGER: FOOD HABITS OF ROCKFISH
Figure 1— Map of vicinity of sampling area showing
Stillwater Cove and the location of the study reef.
ASILOMAR
STILLWATER
COVE
4
()
30 m
J I
ARROWHEAD
POJNT
Cormel
533
overlap values %IRI values were used as the propor-
tion, p.
Morphological Comparison
Several measurements were taken on a subsam-
ple of fish of each species covering all sizes en-
countered in this study. These included standard
length, head length, and gape Mean length of the
five gill rakers nearest the angle on the ventral limb
of the first gill arch, and the gap between them, were
also measured.
The feeding related morphological characteristics
chosen for statistical comparison were head length,
gape, gill raker length, and gill raker spacing. Gape
and gill raker spacing were compared as absolute
measurements. Gill raker lengths were standardized
to a proportion of head length and head length was
standardized as a proportion of standard length for
comparison.
Gape was compared using a one-way analysis of
covariance (ANCOVA). This analysis regressed the
natural log of the ga]je against the natural log of fish
standard length to allow comparison over a range
of fish sizes and to achieve linearity (Sokal and Rohlf
1969; Chen 1971). Relative head length, gill raker
spacing, and relative gill raker length were compared
among species with a Model I, one-way analysis of
variance (ANOVA).
Multiple range comparisons were then made be-
tween individual species to detect groupings. Regres-
sion lines resulting from the ANCOVA were sub-
jected to Newman-Keuls pairwise comparisons.
Mean values obtained from ANOVAs were subjected
to Student-Newman-Keuls (SNK) multiple range
tests. All statistical procedures used followed those
presented in Sokal and Rohlf (1969) and Snedecor
and Cochran (1980).
Prey Abundance
Qualitative assessment of prey abundances was
made from zooplankton tows done in the kelp forest.
A standard 0.5 m diameter net with 0.333 ^m mesh
was used. Tbws were done in sets of three, 3 min
each: one within 0.5 m of the canopy, one in mid-
water, and one within 0.5 m of the bottom. These
were done during both day and night. Generally, only
presence or absence of plankton types was noted,
along with relative daytime vs. nightime differences
in abundances. Absolute abundances were not
estimated. Zooplankton samples were taken once in
mid- June 1980 and once in mid- July 1981. A total
of 12 samples were collected.
FISHERY BULLETIN: VOL. 83, NO. 4
RESULTS
A total of 265 juveniles of the seven species was
examined for stomach content analysis: 27 S.
melanops (53 to 67 mm SL, x = 57.9); 51 S. ser-
ranoides (44 to 63 mm; x = 51.8); 63 5. pinniger (28
to 56 mm, x = 43.7); 23 S. mystiniis (46 to 72 mm,
X = 59.1); 38 S. atrovirens (38 to 64 mm, x = 47.1);
42 S. caurinus (35 to 62 mm, x = 48.7); and 21 S.
camatus (33 to 65 mm, x = 44.4). An often co-
occuring cogener of S. camatus, S. chrysomelas, was
not found during this study.
Diet Analysis
The cumulative prey type curves versus number
of stomachs examined leveled off asymptotically, in-
dicating that sample sizes for all species were suffi-
cient to characterize their food arrays. All species
were found to be zooplanktivores, consuming both
open water and substrate-associated prey. Open
water prey, which mainly float free in the water
column, consisted mostly of juvenile copepods, zoea,
and juvenile spionid polychaetes, while substrate-
associated prey, which were generally found direct-
ly associated (<0.5 m away) with a physical struc-
ture (rock, kelp, eta), consisted mainly of gammarid
amphipods, mysid and caridean shrimp, and two
species of isopod (Ikble 1).
A wide variety of prey sizes were encountered
(Tkble 2). Prey found in open water, such as calanoid
and harpacticoid copepods, zoea, and larvaceans,
were mostly < 1 mm in length, whereas substrate-
associated prey, such as amphipods and decapods,
were 3 to 4 mm or larger.
Mean number of prey items and prey taxa per in-
dividual were highly variable within and among
species (Tkble 3). As would be expected, species
which fed on small open water prey had higher
numbers of prey per stomach. Conversely, those
species which fed on large substrate-associated prey,
which were often large enough to fill a stomach with
a single prey item, had much lower numbers of prey
items per stomach.
Sebastes mystimis fed mainly on the larvacean
Oikopleura sp., with high occurrence of copepods,
zoea, and juvenile polychaetes (Fig. 2). They had the
most cosmopolitan diet and the highest intraspecific
variability of prey types (a mean of almost six dif-
ferent prey types per individual) (Tkble 3). Because
its diet was composed mainly of small open water
prey, this species also had the highest mean number
of prey items per individual.
Sebastes serranoides and S. melanops had very
534
SINGER: FOOD HABITS OF ROCKFISH
Table 1.— Taxa of prey identified in the stonnachs of juvenile rockfish; names in all-capitals are categories
used in stomach content analysis. (?) signifies incomplete or unsure identification. Microhabitat
associations: OW = open water prey, S = substrate oriented prey.
Open water or
Prey type
substrate association
Algae
Mostly reproductive Cystociera osmundacea
S
Occasional pieces of Macrocystis fronds
Invertebrates
Molluscs
- Macoma sp.
S
Copepods
- CALANOIDS: unidentified juveniles
OW
HARPACTICOIDS: unidentified juveniles
OW/S
OSTRACODS
- Unidentified
OW
POLYCHAETES
- larval/juvenile Spionidae
OW
Cirripidea
- unidentified BARNACLE LARVAE
OW
ISOPODS
- Dimonella globera; Idothea resicata
S
Amphipods
- GAMMARIDS: Aoroides columbiana
Ampithoe sp.
fiafea transversa
Najna kitmata (?)
S
CAPRELLIDS: Caprella sp.
S
Unidentified Protocerid
HYPERIIDS: Unidentified
S
MYSIDS
- Acanthomysis sp.; Neomysis sp.
S
Decapods
- SHRIMP: Heptocarpus sp.
Hippolyte sp. (?)
S
ZOEA LARVAE: unidentified decapods and
OW
brachyurans
ANOMURANS: unidentified JUVENILE
S
HERMIT CRAB
Larvaceans
- Oikopleura sp.
OW
FISH
unidentified hard parts
s
unidentified fish
eggs
OW
Table 2. — Mean (+95% confidence interval) sizes of individuals of
the nine major prey types of juvenile rockfishes. Measured items
were taken from stomach samples.
Size (mm)
Species
N
X
95% C.I.
Open water prey
Oikopleura sp.
50
0.69
0.04
Harpacticoid copepods
50
0.88
0.05
Calanoid copepods
50
0.96
0.03
Juvenile polychaetes
35
1.47
0.71
Zoea larvae
50
1.63
0.11
Substrate-associated prey
Mysids
35
3.48
1.16
Gammarid amphipods
35
4.01
0.77
Isopods
30
4.29
0.89
Caridean shrimp
30
13.95
1.47
similar diets (Fig. 2, Tkble 4). Both species ate mainly
open water prey: calanoid copepods, harpacticoid
copepods, and zoea larvae in order of importance
These species also showed fairly high intraspecific
diet variability— 5.3 and 4.4 prey taxa per individual
for melanops and serranoides, respectively.
The two species which showed major microhabitat
shifts (Carr 1983), S. caurinus and S. camatus, also
showed large dietary changes. While in the canopy
(generally <45 mm in SL), 5. caurinus ate
predominantly calanoid copepods, with harpacticoids
and zoea also eaten fairly consistently (Fig. 2).
However, after moving out of the canopy and down
to the bottom near kelp stipes and rocks, its diet
shifted to primarily caridean shrimp, with gammarid
amphipods being the second most important prey
(Fig. 2). Sebastes camatus showed much the same
type of dietary shift accompanying its large habitat
shift. While in the canopy, smaller S. camatus ate
nearly exclusively calanoid copepods (92% of the
diet), while large individuals, which were found on
the bottom, fed on caridean and mysid shrimp and
isopods (Fig. 2). This marked change in diet can also
be seen in Tkble 4. Within each of these species, the
diet similarity between size classes was low. However,
similarities between the two species within each size
class was quite high.
Sebastes atrovirens was found in the kelp canopy
and among kelp throughout all depths during the
entire study (Carr 1983). This species fed mainly on
gammarid amphipods, with calanoid and harpac-
ticoid copepods and mysid shrimp also being very
535
FISHERY BULLETIN: VOL. 83, NO. 4
Table 3.— Mean (+95% confidence interval) number of prey items and prey taxa per stomach
and total number of prey types for the seven species of juvenile rockfishes.
Items
Taxa
S
Species
N
X
95% C.I.
X
95% C.I.
Total
Open water predators
Sebastes mystinus
23
142.6
74.9
5.8
0.4
13
S. caurinus (<45 mm)
17
136.4
64.7
3.4
0.7
8
S. carnatus (<45 mm)
12
101.4
79.6
1.9
0.7
5
S. serranoides
50
100.2
33.5
4.4
1.7
9
S. melanops
27
87.0
31.2
5.3
2.3
8
Substrate-oriented predators
S. pinniger
59
35.5
18.3
4.3
1.6
15
S. atrovirens
33
34.9
20.3
2.2
0.4
8
S. caurinus (>45 mm)
21
2.5
1.3
1.5
0.3
9
S. carnatus (>45 mm)
11
2.3
1.2
1.6
0.7
5
Table 4.— Percent similarity (PSI) overlap values of juvenile rockfish diets. Proportions used for calculations are %IRI.
serranoides melanops mystinus caurinus carnatus pinniger
<45 mm <45 mm
atrovirens
caurinus
>45 mm
carnatus
>45 mm
Sebastes serranoides
S. melanops
S. mystinus
S. caurinus (<45 mm)
S. carnatus (<45 mm)
S. pinniger
S. atrovirens
S. caurinus (>45 mm)
S. carnatus (>45 mm)
0.787
0.455
0.874
0.602
0.653
0.389
0.091
0.090
0.402
0.732
0.516
0.734
0.318
0.094
0.019
—
0.384
0.127
0.458
0.239
0.097
0.043
—
0.668
0.573
0.427
0.185
0.204
—
0.297
0.259
0.043
0.034
0.468
0.174
0.218
0.169
0.258
0.634
important in their diet (Fig. 2). Thus, this spe-
cies' diet was similar to most other species
{Table 4).
Sebastes pinniger had a very diverse diet (highest
number of overall prey taxa found; Ikble 3). In-
dividuals were found mainly over sand areas and the
sand/rock interface at the edge of the kelp forest,
generally within a few meters of the bottom. This
species' diet consisted mainly of copepods and zoea
larvae (open water prey), but gammarid amphipods
and mysid shrimp (substrate-associated prey) were
also important (Fig. 2).
Figure 2 shows that these seven species can be
split into two basic categories: open water and
substrate-associated predators (this categorization
can also be seen in microhabitat differences [Carr
1983]). Open water predators— S. melanops, S.
mystinus, S. serranoides, and small S. caurinus and
S. carnatus— axQ those that ate mainly copepods and
zoea larvae. Substrate-oriented predators— S.
atrovirens and larger 5. caurinus and 5. carnatus—
are those that ate predominantly amphipods and
decapods. Sebastes pinniger is intermediate between
these categories. Its microhabitat and behavior are
that of a substrate-associated predator, but its
diet is more similar to the open water predators
(Tkble 4).
Prey Distribution
Midwater organisms such as copepods, zoea lar-
vae, and polychaetes were very abundant in all parts
of the water column. Calanoid copepods were the
most abundant type during the day at all depths,
while both calanoids and harpacticoids were very
abundant at night. Amphipods, mysids, caridean
shrimp, and isopods were very abundant in and
around all substrate types (kelp canopy, stipes, rocks,
and drift algae). Isopods and amphipods were most
abundant in the canopy and stipes, while amphipods,
mysids, and carideans were more often abundant
near rock and drift algae and around kelp holdfasts.
These invertebrates remained near substrate dur-
ing the day, moving farther away at night.
Morphological Comparisons
ANOVAs of relative head length, relative gill raker
length, and gill raker spacing among species were
all significant at the P < 0.001 level (Tkble 5).
Generally, the open water and substrate-associated
classifications also held true for groupings by
morphology.
In general, open water predators had smaller
heads and larger gill rakers. Sebastes mystinus, S.
536
SINGER: FOOD HABITS OF ROCKFISH
en
X
a
c
o
o
cS
o
>
-a
c
0)
a.
>»
u
o
c
>
3
a
o
c
o
'to
C
<u
0)
a
d^ iP
537
FISHERY BULLETIN: VOL. 83, NO. 4
Table 5. — Results of Student-Newman-Keuls multiple range comparisons on head length and
gill raker length and spacing of juvenile rockfishes (Sebastes). Numbers in parentheses are
significance levels of analyses of variance (ANOVA).
Relative head length (P < 0.0001)
Groupings at a = 0.05 level (mean head lengths)
mystinus serranoides melanops atrovirens
caurinus
pinniger
carnatus
0.3368 0.3620 0.3660 0.3808
0.3882
0.3890
0.3908
Relative gill raker length (P < 0.001)
Groupings at a = 0.05 level (mean raker lengths)
camatus caurinus atrovirens serranoides
pinniger
mystinus
melanops
0.1008 0.1070 0.1165 0.1185
0.1222
0.1296
0.1322
Gill raker spacing (P < 0.001)
Groupings at a = 0.05 level (mean spacing)
pinniger melanops atrovirens carnatus
mystinus
caurinus
serranoides
0.226 0.234 0.238 0.248
0.262
0.312
0.316
serranoides, and S. melanops, which all have relative-
ly long, slender bodies, had significantly smaller
heads than S. caurinus, S. camatus, and S. pinniger
(Ikble 5). Sebastes mystinus and S. melanops also had
significantly longer gill rakers than S. caurinus and
S. camatus, with S. serranoides having intermediate
length rakers. Sebastes atrovirens was relatively in-
termediate in both measurements, but tended to be
more like the predators with larger heads and
shorter gill rakers. Groupings for gill raker spacing
were less distinct. The open water/substrate-
associated classifications also broke down with this
measurement. Sebastes pinniger, melanops, and
atrovirens had more closely spaced rakers, while S.
caurinus and serranoides had the widest spaced
rakers. Sebastes mystinus had an intermediate value
(Ikble 5). Regression lines obtained from the
ANCOVA showed that gape grew isometrically with
length in all seven species, but that there were
significant differences in the size of gape relative to
body size among the species (Ikble 6). The slopes of
the lines of In (gape) on In (SL) were all statistically
indistinguishable from unity, but the intercepts did
show a significant difference (P < 0.001, ANCOVA).
Much of this significant difference was likely due to
S. caurinus, which had a much larger mouth than
the other species. Sebastes serranoides also had a
fairly large mouth. All other species had very similar-
sized mouths (Ikble 6).
DISCUSSION
Many species of fish change diet as they grow (Ross
1978; MacPherson 1981). This may be because of
changes in habitat, thus changing available food
sources, or it may simply be a functional response
Table 6.— Results of the one way analysis of covariance (ANCOVA)
performed on regressions of In (gape) versus In (SL) of juvenile
rockfishes.
Regression statistics
Species
Slope
Intercept
r
Sebastes
caurinus
0.6745
-0.4173
0.8259
S. serranoides
0.8332
-1.2024
0.8363
S. pinniger
0.9876
- 1 .6759
0.9640
S. melanops
0.9761
- 1 .7070
0.9614
S. mystinus
0.9555
- 1 .7470
0.9224
S. carnatus
1 .0482
-1.8439
0.9652
S. atrovirens
1.0561
-2.0053
0.9661
ANCOVA statistics
MSnum
df MSdenom
df F
P
Slope 0.01
7 0.0057
155 1.76
MS
Intercept 0.16
6 0.039
161 40.68
P < 0.001
to changes in fish size and/or metabolic needs.
Although there are dietary differences between the
juveniles and adults of the species studied here, their
foraging patterns and habitats are very much the
same
Species who were water column feeders as
juveniles remain water column feeders as adults.
Juvenile S. serranoides ate primarily copepods and
zoea larvae (Hobson and Chess 1976; this study).
Adults also feed in the water column, eating primar-
ily small fish and euphausiids (Love 1978). Juvenile
S. melanops fed in the open water (on copepods), as
do the adults, which eat small fish, euphausiids, and
polychaetes (Hallacher 1978; Roberts 1979). This
trend also holds for S. mystinus. Juveniles foraged
in the water column, mostly on Oikopleura and
copepods. Adults also aggregate and feed in the open
water, but eat mostly tunicates and crustaceans
(Hallacher 1977; Roberts 1979).
538
SINGER: FOOD HABITS OF ROCKFISH
The ontogenetic similarity in foraging was also
seen in substrate-oriented feeders. Juvenile S.
atrovirens ate mostly large, demersal, gammarid am-
phipods. However, copepods ranked second in their
diet, presumably because of small individuals feeding
in the open water below the kelp canopy. Adults of
this species feed on amphipods, shrimp, and crabs
which can be either demersal or free swimming
(Quast 1968; Hobson and Chess 1976; Roberts 1979).
Small juvenile S. caurinus and 5. carnatus fed in
the open water, while larger juveniles foraged demer-
sally. The adults of these species also feed demer-
sally. Sebastes carnatus is known to eat juvenile
rockfish, ophiuroids, and crustaceans (Hallacher
1977; Roberts 1979), while adult S. caurirms eat
mostly brachyurans and shrimp (Prince 1975; Prince
and Gotshall 1976). Juveniles also seem to exhibit
the same microhabitat preference as adults. Sebastes
serranoides, mystinus, and melanops were found
mainly in the midwater, while S. caurinus, carnatus,
and atrovirens were generally seen to associate more
closely with some physical substrate (kelp plants,
rocks, etc.) (Carr 1983; pers. obs.). Thus, in these
species it seems that once an individual has survived
its life as a pelagic larva and entered the kelp forest,
it assumes the general habitat and foraging
characteristics of an adult.
Sebastes pinniger was the only species which show-
ed different foraging patterns between juveniles and
adults. Juvenile 5. pinniger were generally found
close to the bottom over sand or in association with
the rock/sand interface at the edge of the reef (Carr
1983; pers. obs.) while adults occur higher in the
water column in deep water offshor& Juveniles fed
demersally on copepods over sand and drift algae
very near the kelp forest. Adults feed in the water
column on euphausiids and small fish (Phillips 1964).
Recently, adults have been found to be more demer-
sal feeders than other offshore rockfish (Brodeur
1982).
In assessing the mechanisms which might lead to
the observed diet differences, several factors must
be considered, such as prey distribution and abun-
dance, prey availability, predator morphology, prey
and predator activity patterns, and predator
distribution.
Qualitative analysis of plankton samples, combined
with underwater observations, showed that plankton
were very abundant. Although the diel behavior pat-
terns of shallow, inshore zooplankton are highly
variable with respect to specific habitats, species,
seasons, and latitudes, the patterns of plankton
distribution observed were quite comparable with
reported accounts in kelp forests (Hobson and Chess
1976; Coyer 1979; Hammer 1981).
Predator morphology is an important factor deter-
mining prey size in planktivorous fish. Certain
features distinguish water column foraging fish, such
as long, slender bodies, sharp head profiles, fine den-
tition on jaws and pharyngeal bones, and long, close-
ly spaced gill rakers (Yasuda 1960; Davis and Bird-
song 1973). Of the seven species studied, the water
column feeders— 5. mystinus, S. serranoides, and S.
melanops— ha.d smaller heads with longer gill rakers.
Water column foragers and substrate-associated
foragers could be separated by both morphology and
prey siza The water column foragers— S. mystinus,
S. serranoides, and S. melanops— a.\\ had relatively
long, slender bodies, small heads, and long gill
rakers. This agrees with predictions, especially since
the adults of these species are also water column
foragers. Water column feeders also ate substantially
smaller prey than did substrate predators (see Fig-
ure 2, Tkble 2). The substrate-associated feeders—
S. caurinus, S. carnatus, and 5. atrovirens, which
ate larger prey— all had stouter bodies, larger heads,
and shorter, less ornamented gill rakers.
Juveniles of S. pinniger were somewhat inter-
mediate in feeding morphology. Their heads were
large and stout, indicative of substrate-oriented
feeding. However, they had long, thin bodies and
long, fairly closely spaced gill rakers, which is in-
dicative of water column foraging, as is displayed by
adults. This intermediate situation may be indicative
of the fact that S. pinniger may go through a second
ecological transition from a reef-dwelling, substrate-
associated juvenile form back to a more pelagic off-
shore situation as an adult.
Differing diel patterns can be one way for co-
occurring predators to exploit similar resources
while keeping interspecific interactions low (Keast
and Webb 1966; Schoener 1974; Bray and Ebeling
1975). In zooplanktivores diel patterns of both
predators and prey are important (Hobson and Chess
1976; Robertson and Howard 1978). Most juveniles
were active only during the day, with the possible
exceptions of S. pinniger and S. serranoides (Singer
1982). This was also reflected in greater stomach
fullness of most species in the afternoon and early
evening, indicating diurnal feeding patterns (Singer
1982). Plankton abundances were high during both
day and night. However, more species were found
in the water column at night. Thus, while some of
these fish could do well feeding at night, daytime
abundances of food seemed sufficient for their needs.
Juveniles were indeed found to be most active and
to feed most frequently during daylight hours, but
intraspecific variability was high (Singer 1982).
539
FISHERY BULLETIN: VOL. 83, NO. 4
Digestion was fairly slow in all species, taking at
least 9 to 12 h for a full stomach of food to be half
digested (Singer 1982). Ibgether, these indicate that
individuals may not need to feed every day and that
both within and among species these populations
may feed with a high degree of asynchrony (Singer
1982).
Do the observed differences in diets suggest inter-
specific competition? Central to competition theory
is the presumption that individuals or populations
use the same or a very similar resource and that this
resource is in short supply (Pielou 1975; Pianka
1978). Abundances of all types of plankton used by
these fishes are high. The fact that individuals can
probably fill their stomachs in a very short time
period (Singer 1982) indicates that their needs are
easily met. This suggests that competition for food
does not play an important role in the foraging pat-
terns of these species. Other factors, such as the lack
of observed aggressive interactions within or among
the species studied in over 1,100 min of in situ
feeding observations, high overlap in time of feeding,
generally low similarity of diet, and high intraspecific
variability within foraging patterns suggest there
is little food competition (Singer 1982).
Similarly, available evidence suggests little com-
petition for space among juveniles (Carr 1983).
When juveniles enter the kelp forest system, they
immediately occupy habitats characteristic of adults;
thus, habitat preference may be under some genetic
control. Close spatial co-occurrence with the absence
of agonistic interactions suggests that competition
for space is minimal in these fish. Also, within the
kelp forest studied, juvenile rockfishes are the
predominant planktivores, and are thus relatively
free of other possible competitors. Other kelp forest
planktivores such as Chromis punctipinnis, Oxy-
julius califomica, and Brachyistius frenata are pres-
ent, but in very low numbers, and often only for short
periods of time
Thus, the differences in diet seen in this study ap-
pear to be the consequences of these species ex-
ploiting localized food resources encountered in dif-
ferent microhabitats. Competition for food does not
seem to be a strong ecological influence among these
juveniles.
ACKNOWLEDGMENTS
I thank Greg Cailliet, Milton Love, and Ralph Lar-
son for their guidance and suggestions throughout
this study. Many friends at Moss Landing assisted
me throughout this project including Gilbert Van
Dykhuizen, Bruce Welden, John Heine, Tim Herr-
linger, and John Oliver, who gave helpful comments.
Mark Carr and Tbdd Anderson gave much needed
help and support in diving, stimulating comments,
and general assistance. Mark Silberstein and Peter
Slattery helped with invertebrate identification.
Statistical services were provided by Moss Landing
Marine Laboratories' HP9825 computers. The Peb-
ble Beach Corporation graciously allowed diving ac-
cess to Stillwater Cova Partial funding for equip-
ment came from the D & L Packard Foundation.
Thanks also to Sara Warschaw and Waheedah
Muhammad for typing this manuscript.
Literature Cited
Bray, R. N., and A. W. Ebeling.
1975. Food activity, and habitat of three "picker-type"
microcarnivorous fishes in the kelp forest off Santa Barbara,
California. Fish. Bull., U.S. 73:815-829.
Brodeur, R. D.
1982. Food habits, dietary overlap and gastric evacuation rates
of rockfish (Genus Sebastes). M.S. Thesis, Oreg. State Univ.,
Corvallis, 98 p.
BURGE, R. T., AND S. A. Shultz.
1973. The marine environment in the vicinity of Diablo Cove
with special reference to abalones and bony fishes. Calif.
Dep. Fish Game, Mar. Res. Tbch. Rep. 19, 433 p.
Carr, M. A.
1983. Spatial and temporal patterns of recruitment of young-
of-the-year rockfishes (genus Sebastes) into a Central Califor-
nia kelp forest. M.A. Thesis, San Francisco State Univ., San
Francisco, 122 p.
Chen, L. C.
1971. Systematics, variation, distribution, and biology of the
subgenus Sebastomus (Pisces, Scorpaenidae, Sebastes). Univ.
Calif. Press, Berkeley 107 p.
Coyer, J. A.
1979. The invertebrate assemblage associated with
Macroq/stis pyrifera and its utilization as a food source by
kelp forest fishes. Ph.D. Thesis, Univ. Southern California,
Los Angeles, 364 p.
Davis, W. P., and R. S. Birdsong.
1973. Coral reef fishes which forage in the water column, a
review of their morphology, behavior, ecology and evolu-
tionary implications. Helgo. Wiss. Meersunters. 24:292-306.
DeLacey, A. C, K. R. Hitz, and R. L. Dryfoos.
1964. Maturation, gestation and birth of rockfish (Sebastodes)
from Washington and adjacent waters. Wash. State Dep.
Fish. Res. Pap. 2(3):51-67.
Dewitt, F. A., Jr., and G. M. Cailliet.
1972. Feeding habits of two bristlemouth fishes, Cydothone
acclinidens and C. signata (Gonostomatidae). Copeia
1972:868-871.
Hallacher, L. E.
1977. Patterns of space and food use by inshore rockfishes
(Scorpaenidae; Sebastes) of Carmel Bay California. Ph.D.
Thesis, Univ. California, Berkeley, 119 p.
Hammer, R. M.
1981. Day-night differences in the emergence of demersal
zooplankton from a sand substrate in a kelp forest. Mar.
Biol. (Berl.) 62:275-280.
HoBSON, E. S., and J. R. Chess.
1976. Trophic interactions among fishes and zooplankters
540
SINGER: FOOD HABITS OF ROCKFISH
near shore at Santa Catalina Island, California. Fish. Bull.,
U.S. 74:567-598.
Keast. a., and D. Webb.
1966. Mouth and body form relative to feeding ecology in the
fish fauna of a small lake, Lake Opinicon, Ontaria J. Fish.
Res. Board Can. 23:1845-1874.
Larson, R. J.
1980a. Tferritorial behavior of the black and yellow rockfish
and gopher rockfish (Scorpaenidae; Sebastes). Mar. Biol.
(Berl.) 58:111-122.
1980b. Influence of territoriality on adult density in two rock-
fishes of the genus Sebastes. Mar. Biol. (Berl.) 58;123-132.
1980c Competition, habitat selection, and the bathymetric
segregation of two rockfish (Sebastes) species. Ecol. Monogr.
50:221-239.
Love, M. S.
1978. Aspects of the life history of the olive rockfish, Sebastes
serranoides. Ph.D. Thesis, Univ. California, Santa Barbara,
183 p.
MacPherson, E.
1981. Resource partitioning in a Mediterranean demersal fish
community. Mar. Ecol. Prog. Ser. 4:183-193.
Miller, D. J., and J. J. Geibel.
1973. Summary of blue rockfish and lingcod life histories; a
reef ecology study; and giant kelp, Macrocystis pyrifera, ex-
periments in Monterey Bay, California. Calif. Dep. Fish.
Game, Fish Bull. 158, 137 p.
Miller, D. J., and R. N. Lea.
1972. Guide to the coastal marine fishes of California. Calif.
Dep. Fish Game, Fish Bull. 157, 235 p.
Phillips, J. B.
1964. Life history studies on ten species of rockfish (genus
Sebastodes). Calif Dep. Fish Game, Fish Bull. 126, 70 p.
Pianka, E. R.
1978. Evolutionary ecology. Harper and Row, N.Y., 397 p.
Pielou, E. C.
1975. Ecological diversity. Wiley-Interscience, N.Y., 165 p.
Pinkas, L., M. S. Oliphant, and I. L. K. Iverson.
1971. Food habits of albacore, bluefin tuna, and bonito in
California waters. Calif. Dep. Fish Game, Fish Bull. 152, 105
P-
Prince, E. D.
1975. Pinnixid crabs in the diet of young-of-the-year copper
rockfish (Sebastes caurinus). Trans. Am. Fish Soc.
104:539-540.
Prince, E. D, and D. W. Gotshall.
1976. Food of the copper rockfish, Sebastes caurimis Richard-
son, associated with an artificial reef in South Humboldt Bay,
California. Calif Fish Game 62:274-285.
QUAST, J. C.
1968. Observations of the food of the kelp-bed fishes. In W.
J. North and C. L. Hubbs (editors), Utilization of kelp-bed
resources in Southern California, p. 109-142. Calif Dep.
Fish Game, Fish Bull. 139.
Roberts, D. A.
1979. Food habits as an ecological partitioning mechanism in
the nearshore rockfishes (Sebastes) of Carmel Bay, Califor-
nia. M.A. Thesis, San Francisco State Univ., San Francisco,
74 p.
Robertson, A. I., and R. K. Howard.
1978. Diel trophic interactions between vertically-migrating
zooplankton and their fish predators in an eelgrass communi-
ty. Mar. Biol. (Berl.) 48:207-213.
Ross, S. T
1978. Trophic ontogeny of the leopard searobin, Prionotus
scitulus (Pisces: Triglidae). Fish. Bull, U.S. 76:225-234.
Schoener, T W.
1974. Resource partitioning in ecological communities.
Science (Wash., DC.) 185:27-39.
Singer, M. M.
1982. Food habit and activity patterns of juvenile rockfishes
(Sebastes) in a central California kelp forest. M.A. Thesis,
Moss Landing Marine Laboratories, Moss Landing, CA, 75 p.
Snedecor, G. W., and W. G. Cochran.
1980. Statistical methods. 7th ed. Iowa State Univ. Press,
Ames, 507 p.
Sokal, R. R., and F. J. ROHLF.
1969. Biometry. The principals and practice of statistics in
biological research. W. H. Freeman, San Franc, 776 p.
Westrheim, S. J.
1975. Reproduction, maturation, and identification of larvae
of some Sebastes (Scorpaenidae) species in the Northeast
Pacific Ocean. J. Fish. Res. Board Can. 32:2399-2411.
Whittaker, R. H.
1952. A study of the summer foliage insect communities in
the Great Smokey Mountains. Ecol. Monogr. 22:1-44.
Yasuda, F.
1960. The relationship of the gill structure and food habits
of some coastal fishes in Japan. Rec Oceanogr. Works Jpn.
New Ser. 5(2):139-152.
541
RADIO TRACKING THE MOVEMENTS AND ACTIVITIES OF
HARBOR PORPOISES, PHOCOENA PHOCOENA (L.), IN
THE BAY OF FUNDY, CANADA
Andrew J. Read and David E. Gaskin^
ABSTRACT
Eight harbor porpoises were radio-tagged (172-173 MHz) and released in the western Bay of Fundy between
August 1981 and August 1983. The duration of contact with radio-tagged animals ranged from 0.3 to
22.4 days. One harbor porpoise was tracked for 22.4 days and utilized a home range area of 210 km^.
In all observed cases, the movement of radio-tagged porpoises coincided with the direction of tidal flow
in the major channels and passages of the region. Analysis of 39.2 hours of ventilation sequences revealed
that radio-tagged porpoises were relatively inactive from midnight until 0600 and more active during
other periods.
This report documents the results of a study on the
movements and activities of radio-tagged harbor
porpoises, Phocoena phocoena, in the Bay of Fundy,
Canada. The primary objective of this research was
to determine the home ranges of individual harbor
porpoises during the summer months. The study
also provided insights into the behavior and ac-
tivities of radio-tagged animals.
Studies of cetacean home ranges often rely on
resightings of tagged or naturally marked animals
(Irvine et al. 1981; Bigg 1982; Dorsey 1983). These
methods are of limited value if individual animals
travel outside the area under observation and may
result in underestimation of the utilized range. A
more effective means of estimating home range area
is to monitor the movements of radio-tagged in-
dividuals (McDonald et al. 1979). Several recent
studies have successfully employed radio-tracking
techniques in field studies of cetacean species (see
review by Leatherwood and Evans 1979). Notable
among these are investigations of Delphinus delphis
by Evans (1971), of Tursiops truncatus by Irvine
et al. (1981), and of Lagenorhynchus obscurus by
Wursig (1982).
In a preliminary study of harbor porpoise move-
ments (Gaskin et al. 1975), we demonstrated that
radio-tracking techniques could be successfully ap-
plied to this species. Although this initial research
was promising, we felt that the transmitters
available at that time were too large to be carried
by these small porpoises (see Watson and Gaskin
1983). The recent development of smaller transmit-
'Department of Zoology, University of Guelph, Guelph, Ontario
NIG 2W1 Canada.
ters and the continuing availability of live porpoises
from herring weirs (Smith et al. 1983) have enabled
us to undertake the present study.
METHODS
The study area encompases Passamaquoddy Bay,
the channels and passages around Deer Island, and
waters further offshore to Grand Manan Island (Fig.
1). During the summer, mean monthly water tem-
peratures for the upper 25 m of the water column
range from 6.4° in June to 11.0°C in September
(Bailey et al. 1954). The oceanography of the region
is dominated by large semidiurnal tides, which have
a mean amplitude of 5.5 m at North Head, Grand
Manan (Anonymous 1982). The large tides generate
strong currents, with velocities reaching a maximum
of 2.4 m/s in Letite Passage (Forrester 1960). Fur-
ther information regarding the oceanography of the
region may be found in Smith et al. (1984).
Harbor porpoises were seined from herring v/eirs
(Smith et al. 1983), placed on a sheet of open cell
foam, sexed, and measured. The porpoises were
liberally sprinkled with seawater throughout the
tagging procedure to prevent overheating. Two 0.64
cm diameter holes were bored through the dorsal
fin with a laboratory cork borer, cleansed in alcohol
prior to use. The holes were immediately cold-
cauterized with a histological freezing spray.
Transmitters were attached to the dorsal fin with
two 0.64 cm diameter stainless steel bolts, each
covered with a thin sleeve of teflon (see Figure 2).
A thin, neoprene-lined plastic plate was placed
between the transmitter and dorsal fin and an iden-
tical plate was positioned on the opposite side of the
Manuscript accepted November 1984.
FISHERY BULLETIN: VOL. 83, No. 4, 1985.
543
FISHERY BULLETIN: VOL. 83, No. 4
Figure 1.— The harbor porpoise study area with place names mentioned in text. The inset shows the study
area in relation to the rest of the Bay of Fundy.
fin. The teflon-covered bolts, passed through the
transmitter and plastic plates, were fastened with
corrodable, low grade steel nuts.
The radio transmitters measured 3.2 x 3.8 x 6.0
cm and weighed about 170 g in air (Model 4-A,
Telonics,^ Mesa, AZ). The transmitting antennae
544
consisted of 43 cm semiflexible whips, designed
specifically for use with marine mammals.
Transmitted VHF signals (172-173 MHz) consisted
^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
READ and GASKIN: RADIO TRACKING HARBOR PORPOISES
of 20-60 ms pulses at intervals of 0.4 s. Lithium bat-
teries provided a maximum power output of 0.75
mW and an expected transmitting life of 1.6-6.0 mo.
The maximum transmitting range across open water
was about 15-20 km.
We used a Telonics TR-2 telemetry receiver with
a two-element, hand-held directional antenna. The
approximate direction of the transmitter was deter-
mined by rotating the antenna and noting the
strongest signal. A digital data processor (Telonics
TDP-2) provided a visual display of signal strength.
The position of a tagged porpoise was determined
either by tracking the animal until visual contact was
established, or by triangulation from shore. In the
latter method, the receiving system was moved
along the shore, and signal bearings at two or more
locations were noted. The intersection point of these
bearings was then used to approximate the position
BOLT
— ANTENNA
PLATE
TRANSMITTER
NEOPRENE
NUT
DORSAL FIN
Figure 2.— The transmitter package used in radio-tracking studies of harbor porpoises in the Bay of Fundy.
The bolts attaching the transmitter to the dorsal fin were covered by thin teflon sleeves.
545
FISHERY BULLETIN: VOL. 83, NO. 4
of the porpoise. To ensure bearing accuracy, a series
of readings were taken at each location, and the
average used in triangulation (Springer 1979). Each
sighting or radio location was assigned to a 1 km
grid square of the Universal Transverse Mercator
System. Derived radio locations were discarded if
the triangulation could not place a porpoise within
a 1 km square; the time elapsed between fixes and
bearing error (± 5°) precluded more precise estima-
tion. Positional data were collected at least once a
day, but usually on a more frequent basis.
The radio signal was received only when the trans-
mitting antenna was exposed, allowing the duration
of both submergence and surface periods to be
recorded. Such ventilation data were collected on
an opportunistic basis throughout the tracking
period of each porpoise.
A detailed analysis of the methods used in this
study is presented in Read and Gaskin (1983).
RESULTS
Movements
Eight harbor porpoises were released carrying
transmitters over the course of the study (Table 1).
During the attachment procedure, porpoises were
out of the water for a mean of 6.6 min (SD + 1.4,
n = 8), during which time most animals remained
fairly still. Only two porpoises exhibited any trauma
while being handled; RT-5 vomited briefly, and RT-7
(a 110 cm calf) repeatedly lashed its flukes. The lat-
ter porpoise appeared momentarily disoriented
when returned to the water, but quickly resumed
swimming and surfacing normally after being join-
ed by a larger porpoise. The larger animal, presum-
ably the calf's mother, had also been trapped in the
weir, but escaped overnight and remained in the
vicinity until the calf's release.
Duration of radio contact ranged from 0.30 (RT-5)
to 22.4 d (RT-2), with a mean of 5.1 d (SD ± 7.1,
n = 8). In some instances, loss of radio contact may
Table 1. — Data summary for harbor porpoises radio-tagged and
released in the western Bay of Fundy.
Porpoise
Length
Frequency
Date of
Duration of
code
(cm)
Sex
(MHz)
Release
contact (d)
RT-1
132
M
173.350
05 08 81
3.05
RT-2
119
M
173.550
20 08 81
22.4
RT-3
145
M
173.500
29 07 82
5.32
RT-4
131
F
173.100
31 08 82
3.16
RT-5
114
M
173.000
31 08 82
0.30
RT-6
116
M
173.700
01 09 82
2.72
RT-7
110
M
173.650
03 09 82
1.83
RT-8
114
M
172.600
09 08 83
2.25
have been due to the premature release of the
transmitter package. The rear bolt attaching the
transmitter to the dorsal fin of RT-3 was missing
when the porpoise was photographed 5 h before
signal loss occurred. The radio signals of RT-3 and
RT-7 were being monitored when contact was lost,
and in both cases termination of the signal was
abrupt, a pattern compatible with the hypothesis of
transmitter loss. In our limited observations of
radio-tagged porpoises (see below), we did not see
any evidence of displacement of the transmitter
package (Irvine et al. 1982).
Over the course of the study, three porpoises were
released from the same weir in Whale Cove, Grand
Manan. Attempts to relocate RT-1, the first porpoise
released in Whale Cove, were frustrated by fog and
heavy seas which persisted for the entire 3-d track-
ing period. In addition, the shoreline configuration
of northern Grand Manan prevented accurate
triangulation. However, the strength and direction
of the signal received from shore indicated that the
porpoise remained in the vicinity of northern Grand
Manan until signal loss occurred. The movements
of the other two porpoises released in Whale Cove
(RT-3 and RT-7) are illustrated in Figure 3 A and B.
On 30 August 1982, four porpoises were reported
trapped in a weir in Back Bay, mainland New
Brunswick. A female (RT-4), accompanied by a 101
cm calf, and a young male (RT-5) were released on
31 August. The remaining porpoise, another young
male (RT-6), was tagged and released the following
day. RT-4 and RT-5 remained together for at least
7 h, after which contact was lost with RT-5. The
movements of RT-4 and RT-6 are depicted in Figure
3C and D.
The longest tracking sequence recorded in this
study was that of RT-2, released near St. Andrews,
mainland New Brunswick. This porpoise spent the
majority of its 22-d tracking period within Passa-
maquoddy Bay, although occasional excursions were
made to the east of Deer Island (Fig. 4). The home
range of RT-2, calculated using the convex polygon
method, was about 210 km^ (excluding land
masses).
RT-8, the only porpoise to be radio-tagged in 1983,
travelled from its release point in northern Passa-
maquoddy Bay to West Quoddy in about 48 h.
Logistical constraints prevented more precise deter-
mination of the movements of this animal.
Figure 3.— Movements and positions of radio-tagged harbor por-
poises in the Bay of Fundy. The release point of each porpoise is
indicated by a star. A) Position of porpoise RT-3 at 1200 of each
day of tracking period; B) Movements of porpoise RT-7; C)
Movements of porpoise RT-4; D) Movements of porpoise RT-6.
546
READ and GASKIN: RADIO TRACKING HARBOR PORPOISES
02 September
r2250
547
FISHERY BULLETIN: VOL. 83, NO. 4
Figure 4.— Position of porpoise RT-2 at 1200 of each day of tracicing period in the western Bay of Fundy.
548
READ and GASKIN: RADIO TRACKING HARBOR PORPOISES
The movements of three radio-tagged porpoises
(RT-2, RT-4, RT-6) were tracked through the ma-
jor passages around Deer Island on seven occasions.
In all cases, the direction of movement coincided
with the direction of tidal flow. The strong correla-
tion between porpoise movements and current direc-
tion in these areas was demonstrated on 30 August
1981, when RT-2 moved up Western Passage with
the flood tide, turned at slack high water and moved
out with the ebb.
Two radio-tagged porpoises were resighted on
several occasions. RT-2 was observed resting at the
surface in the approaches to Head Harbour Passage
on 22 August 1981. Although the porpoise was
alone, several groups of resting animals were pres-
ent in the vicinity. RT-3 was resighted on six occa-
sions; during five of these sightings the radio-tagged
animal was accompanied by a single large porpoise.
These observations gave no indication that the
transmitter packages affected the behavior of tag-
ged porpoises.
Attempts to relocate radio-tagged animals
demonstrated some of the inherent problems in-
volved in censusing harbor porpoise populations.
Even with the aid of directional receivers and bright-
ly painted transmitters, it was difficult to sight a
tagged porpoise or to follow its movements after it
had been located. It proved particularly difficult to
see radio-tagged porpoises while they lay motion-
less at the surface.
distance from porpoises swimming just below the
surface (see also Frost et al.^).
Radio-tagged porpoises exhibited two readily
discernible activity states (Fig. 5). Low activity (or
relative inactivity) was characterized by frequent sur-
face resting periods interspersed with rolls; resting
periods accounted for over 55% of all signals in this
activity state Porpoises were considered active (high
activity) when resting periods were absent or infre-
quently recorded. It is important to note that por-
poises did not rest at the surface when wave height
was >30 cm and winds speeds exceeded 13 km/h (see
also Dudok van Heel 1962; Andersen and Dziedzic
1964).
^Frost, K. J., L. F. Lowry, and R. R. Nelson. 1983. Investi-
gations of belukha whales in coastal waters of western and north-
ern Alaska, 1982-1983; marking and tracking of whales in Bristol
Bay. Final Report, Contract NA 81 RAC 00049, 104 p.
J__J LI-
ACTIVITY LEVEL HIGH
u.
■ 11
■ ■
J I I I L
JJ I l—L
_■_■ I L
Patterns of Activity
In total, 39.2 h of ventilation sequences were
recorded from four radio-tagged porpoises (RT-2,
RT-3, RT-4, RT-7). These sequences comprised 4,680
individual dives, lasting from 2 to 195 s.
Two types of signals were received from radio-
tagged animals. The most common signal was brief
(1-3 s) and indicated that the porpoise had surfaced
and submerged in a continuous motion. Such action
patterns are commonly referred to as rolls (Amun-
din 1974; Smith et al. 1976). Other signals were more
prolonged (4-100 s) and are referred to here as sur-
face periods.
Prolonged signals received from radio-tagged har-
bor porpoises have previously been interpreted as
near-surface swimming (Gaskin et al. 1975).
However, visual observations of radio-tagged animals
RT-2 and RT-3 indicated that such signals originated
from porpoises resting motionless at the surface. The
strength of the transmitted signal attenuated rapidly
as the length of exposed antenna decreased, making
it unlikely that signals could be received at any
■ ■ ■ ■
-60 seconds-
ACTIVITY LEVEL LOW
-60 secoods-
FlGURE 5.— Examples of signal patterns used to derive activity
states of radio-tagged harbor porpoises (each example represents
a continuous record). Activity level was considered high when
signals were dominated by rolls (signal duration 1-3 s). Activity level
was considered low when signals were dominated by surface resting
intervals (signal duration >3 s). The signal pattern used to
demonstrate the high activity level (top) is characteristic of Pat-
tern B respiration (Watson and Gaskin 1983).
549
FISHERY BULLETIN: VOL. 83. NO. 4
Radio-tagged porpoises exhibiting the high activity
state expressed two ventilation patterns; these are
described using the terminology of Watson and
Gaskin (1983). Most data recorded in this activity
state consisted of Pattern B, a series of long dives,
each followed by a sequence of several rolls (see
Figure 5). Less commonly observed was Pattern A,
in which single rolls followed relatively short
submergences (seldom exceeding 30 s in duration).
Pattern A was exhibited for brief periods only (5-16
min) and comprised <4% of all signals recorded dur-
ing high activity sequences.
Ventilation data recorded from RT-2 and RT-4 were
dominated by low activity sequences. However, low
activity sequences were not recorded from either
RT-3 or RT-7. Although RT-3 was frequently observed
resting at the surface, the loose transmitter package
(see above) caused the antenna to reflect backwards,
allowing signal reception only during rolls. Thus, it
was not possible to accurately monitor the duration
of resting periods for this porpoise Data from RT-7
were acquired only during periods of high winds and
heavy seas which precluded surface resting behavior.
Because surface resting was the criterion on which
determinations of activity levels were based, it was
impossible to ascertain the activity level of radio-
tagged porpoises in periods of high vdnds and heavy
seas. Tb construct an activity budget, therefore, it
was necessary to exclude data recorded during
periods when surface resting was not possible A
total of 10.5 h of ventilation sequences were record-
ed under such conditions. In addition, data acquired
from RT-3 were excluded because of the bias imposed
by the transmitting system. After these data had
been deleted, 24.5 h of ventilation sequences record-
ed from RT-2 and RT-4 remained.
Both RT-2 and RT-4 were relatively inactive from
midnight until 0600, spending over 90% of this
period in the low activity state Both porpoises spent
a considerable portion of this time resting at the sur-
face (Ikble 2). During this period of reduced activity,
the porpoises were seldom located in nearshore
areas, although they frequented such areas during
other periods. The two porpoises were highly active
for 35% (RT-2) and 36% (RT-4) of daylight and even-
ing hours (0600 until midnight) (Ikble 2).
DISCUSSION
Movements and Ranges
Radio-tagged harbor porpoises demonstrated con-
siderable mobility within the study area, often
moving distances of 15-20 km in a 24-h period. These
results are similar to those previously reported from
radio-tagged harbor porpoises in the region (Gaskin
et al. 1975). Other inshore odontocete species exhibit
daily movements of a similar magnitude For exam-
ple, dusky dolphins, Lagenorhynchus obscurus, track-
ed by Wiirsig (1982), travelled a "mean minimum
distance" of 19.2 km each day. However, pelagic
species apparently travel over much greater
distances. A pelagic spotted dolphin, Stenella at-
tenuata, tracked by Leatherwood and Ljungblad
(1979), travelled over 100 km in a 12-h period, while
common dolphins, Delphintcs delphis, may cover
distances of 70-140 km each day (Evans 1971).
The mobility exhibited by the majority of radio-
tagged porpoises suggest that the ranges of these
animals were similar to that calculated for RT-2 (210
km^). Only one other study has examined the areas
of home ranges utilized by odontocete cetaceans.
Wells et al. (1980) used resightings of naturally mark-
ed animals to estimate the size of bottlenose dolphin,
Tursiops truncatus, ranges in the coastal waters of
western Florida. The mean home ranges of these
dolphins varied with age and sex, and ranged from
15 to 41 km^. It is possible that the apparent dif-
ference in the size of home ranges of these two
species reflects the exploitation of different prey
species. In the Bay of Fundy, harbor porpoises feed
predominantly on juvenile herring, Clupea harengvs
(Smith and Gaskin 1974), which exhibit a high degree
of mobility (Jovellanos and Gaskin 1983). In contrast,
Florida bottlenose dolphins are opportunistic
predators on species such as mullet Mugil cephalus,
which may be more sedentary in nature (Irvine et
al. 1981).
Patterns of Activity
The patterns of activity observed in the present
Table 2.— Activity patterns of radio-tagged harbor porpoises RT-2
and RT-4 in the western Bay of Fundy. The low activity state was
characterized by frequent surface resting periods, which were in-
frequent or absent in the high activity state. Only data recorded dur-
ing calm conditions have been included.
Observation
Activity:
Activity:
At
time
high
low
surface
Porpoise Time
(min)
(%)
{%)
(0/0)
RT-2 0000-0559
352.9
2.0
98.0
31.4
0600-1159
274.8
14.9
85.1
18.8
1200-1759
435.2
46.0
54.0
11.2
1800-2359
165.2
41.0
59.0
12.2
Total
1,228.5
25.7
74.3
18.8
RT-4 0000-0559
116.0
7.0
93.0
18.5
0600-1159
37.0
100.0
0.0
0.0
1200-1759
0.0
—
—
—
1800-2359
90.7
9.9
90.1
13.6
Total
243.7
22.2
77.8
13.9
550
READ and GASKIN: RADIO TRACKING HARBOR PORPOISES
study do not support previous contentions that the
metaboHc requirements of harbor porpoises (see
Kanwisher and Sundnes 1965) are such that in-
dividuals must spend a large proportion of each day
engaged in foraging behavior (Smith and Gaskin
1974; Watson and Gaskin 1983).
Herbers (1981) has hypothesized that behavioral
inactivity is a product of predation efficiency. As
predation efficiency increases, less time is spent
searching for and capturing prey, and more time is
available for other behavior, including inactivity.
Therefore, if harbor porpoises are efficient predators,
it seems reasonable to suggest that only a small por-
tion of their day would be spent engaged in foraging
behavior.
Many other mammalian predators are inactive for
large portions of the day. For example, Serengeti
lions, Panthera leo, are inactive for about 85% of
each day (Schaller 1972). Similarly, spotted hyaenas,
Crocuta crocuta, are inactive for 84% of the day
(Kruuk 1972). Even the sea otter, Enhydra lutris,
with a metabolic rate 2.4 times that predicted for
a terrestrial mammal of equal size (Costa and
Kooyman 1982), spends only 34% of each day for-
aging (Loughlin 1979).
The ventilation sequences recorded from RT-2 and
RT-4 suggest that these harbor porpoises restricted
the majority of their activity to daylight and even-
ing hours (Tkble 2). If a circadian pattern of activity
exists, it may be related to the schooling behavior
of prey species. The structure of herring schools
breaks down after dusk, as the visual cues used to
maintain school structure become inoperative
(Brawn 1960). Thus, the fish exhibit a dispersed
distribution at night, presumably limiting prey cap-
ture by predators such as the harbor porpoises,
which rely on dense schools to maintain maximum
capture efficiency.
Other odontocete species exhibit various circadian
patterns of activity. Observations of captive bottle-
nose dolphins indicate that, like the harbor porpoise,
Tursiops is relatively inactive at night (McBride and
Hebb 1948; McCormick 1969; Saayman et al. 1973).
In contrast, Hawaiian spinner dolphins, Stenella
longirostris, rest during the day and feed almost ex-
clusively at night (Norris and Dohl 1980). The prey
of spinner dolphins undertake extensive vertical
migrations (Perrin et al. 1973) and may be more
available to the dolphins at night.
We were interested in observing the nocturnal
behavior of harbor porpoises (when they were
presumably relatively inactive) under conditions of
strong winds and heavy seas, when surface resting
was not possible Ventilation data recorded from RT-7
during a 5-h period (0000-0500, 5 September 1982)
of heavy seas consisted almost exclusively of Pattern
B sequences. Watson and Gaskin (1983) have sug-
gested that this ventilation pattern is expressed
primarily by foraging porpoises, but it seems unlikely
that RT-7 (a calf) was foraging for 5 consecutive
hours at night. An alternative explanation is that the
porpoise was resting underwater and rising to the
surface for a series of breaths (see similar observa-
tions by McBride and Hebb 1948; Layne 1958;
McCormick 1969; Condy et al. 1978). It is possible,
therefore, that harbor porpoises engaged in diverse
behavioral activities may exhibit similar ventilation
patterns.
During the period of reduced activity (from 0000
to 0600) radio-tagged porpoises were often located
in open water some distance from shore This may
reflect a tendency for porpoises to rest in areas
where the hazards of swift currents and shallow
waters are minimized. Observations made in the in-
shore waters of the Deer Island region confirm that
porpoises seldom rest at the surface in nearshore
environments (Watson and Gaskin 1983).
ACKNOWLEDGMENTS
We thank W. Kozak and the members of the Fundy
Weir Fishermen Association for their assistance in
this study. Sterling field assistance was provided by
C. Thomson and members of the Fundy Cetacean
and Seabird Research Group. Constructive criticism
of earlier versions of this paper were provided by B.
Braune, L. Murison, P. Watts, L. White, and two
anonymous reviewers. This research was supported
by Joint Contract UP-G-152 (Departments of Sup-
ply and Services and Fisheries and Ocean Canada).
Harbor porpoises were tagged under a permit issued
by Fisheries and Oceans Canada.
LITERATURE CITED
Amundin, M.
1974. Functional analysis of the surfacing behaviour in the
harbour porpoise, Phocoena phocoena (L.). Z. Saugetierkd.
Bd. 39:313-318.
Andersen, S., and A. Dziedzic.
1964. Behaviour patterns of captive harbour porpoise Pho-
coena phocoena L. Bull. Inst. Oceanogr. Monaco 63(1316):
1-20.
Anonymous.
1982. Canadian tide and current tables. Vol. 1. The Atlantic
coast and Bay of Fundy. Department of Fisheries and
Oceans Canada, Ottawa.
Bailey, W. B., D. G. MacGregor, and H. B. Hachey
1954. Annual variations in temperature and salinity in the Bay
of Fundy. J. Fish. Res. Board Can. 11:32-47.
551
FISHERY BULLETIN: VOL. 83, NO. 4
Bigg, M. A.
1982. An assessment of killer whale {Orcinus orca) stocks off
Vancouver Island, British Columbia. Rep. Int. Whaling
Comm. 32:655-666.
Brawn, V. M.
1960. Seasonal and diurnal vertical distribution of herring
(Clupea harengiis L.) in Passamaquoddy Bay, N.B. J. Fish.
Res. Board Can. 17:699-711.
CONDY, P. R., R. J. VAN AaRDE, AND M. N. BESTER.
1978. The seasonal occurrence and behaviour of kOler whales,
Orcinus orca, at Marion Island. J. Zool. (Lond.) 184:449-464.
Costa, D. P., and G. L. Kooyman.
1982. Oxygen consumption, thermoregulation, and the effect
of fur oiling and washing on the sea otter, Enhydra lutris.
Can. J. Zool. 60:2761-2767.
DORSEY, E. M.
1983. Exclusive adjoining ranges in individually identified
minke whales (Balaenoptera acutorostrata) in Washington
State Can. J. Zool. 61:174-181.
DuDOK VAN Heel, W H.
1962. Sound and Cetacea. Neth. J. Sea Res. 1:407-507.
Evans, W. E.
1971. Orientation behavior of delphinids: radio telemetric
studies. Ann. N.Y. Acad. Sci. 188:142-160.
Forrester, W. D.
1960. Current measurements in Passamaquoddy Bay and the
Bay of Fundy J. Fish. Res. Board Can. 17:727-728.
Gaskin, D. E., G. J. D. Smith, and A. P. Watson.
1975. Preliminary study of harbor porpoises {Phocoena pho-
coena) in the Bay of Fundy using radiotelemetry. Can. J.
Zool. 53:1466-1471.
Herbers, J. M.
1981. Time resources and laziness in animals. Oecologia
49:252-262.
Irvine, A. B., M. D. Scott, R. S. Wells, and J. H. Kaufmann.
1981. Movements and activities of the Atlantic bottlenose
dolphin, Tursiops truncatus, near Sarasota, Florida. Fish.
Bull., U.S. 79:671-688.
Irvine, A. B., R. S. Wells, and M. D. Scott.
1982. An evaluation of techniques for tagging small odon-
tocete cetaceans. Fish. Bull., U.S. 80:135-143.
Jovellanos, C. L., and D. E. Gaskin.
1983. Predicting the movements of juvenile Atlantic herring
{Clupea harengus harengus) in the SW Bay of Fundy using
computer simulation techniques. Can. J. Fish. Aquat. Sci.
40:139-146.
Kanwisher, J., and G. Sundnes.
1965. Physiology of a small cetacean. Hvalradets Skr.
48:45-53.
Kruuk, H.
1972. The spotted hyaena. A study of predation and social
behaviour. Univ. Chicago Press, Chia, 335 p.
Layne, J. N.
1958. Observations on freshwater dolphins in the upper
Amazon. J. Mammal. 39:1-22.
Leatherwood, S., and W E. Evans.
1979. Some recent uses and potentials of radiotelemetry in
field studies of cetaceans. In H. E. Winn and B. L. Olla
(editors). Behavior or marine animals. Vol. 3: Cetaceans, p.
1-31. Plenum Press, N.Y.
Leatherwood, S., and D. K. Ljungblad.
1979. Nighttime swimming and diving behavior of a radio-
tagged spotted dolphin, Stenella attenuata. Cetology 34, 6 p.
LOUGHLIN, T. R.
1979. Radiotelemetric determination of the 24-hour feeding
activities of sea otters, Enhydra lutris. In C. J. Amlaner
and D. W Macdonald (editors), A handbook on biotelemetry
and radio tracking, p. 717-724. Pergamon Press, Oxf.
Macdonald, D. W, F. G. Ball, and N. G. Hough.
1979. The evaluation of home range size and configuration
using radio tracking data. In C. J. Amlaner and D. W Mac-
donald (editors), A handbook on biotelemetry and radio track-
ing, p. 405-424. Pergamon Press, Oxf.
McBride, a. F, and D. 0. Hebb.
1948. Behavior of the captive bottlenose dolphin, Tursiops
truncatus. J. Comp. Physiol. Psychol. 41:111-123.
McCoRMiCK, J. G.
1969. Relationship of sleep, resj; iration, and anesthesia in the
porpoise: a preliminary report. Proc Nat. Acad. Sci., U.S.
62:697-703.
NoRRis, K. S., and T R Dohl.
1980. Behavior of the Hawaiian spinner dolphin, Stenella
longirostris. Fish Bull., U.S. 77:821-849.
Perrin, W F., R. R. Warner, C. H. Fiscus, and D. B. Holts.
1973. Stomach contents of porpoise, Stenella, spp., and
yellowfin tima, Thunnus albacares, in mixed-species aggrega-
tions. Fish. Bull, U.S. 71:1077-1092.
Read, A. J., and D. E. Gaskin.
1983. The application of radio tracking techniques to the study
of harbour porpoises {Phocoena phocoena) in the Bay of
Fundy. In D. G. Pincock (editor). Proceedings of the Fourth
International Conference on Wildlife Biotelemetry, p.
346-352. Halifax, Nova Scotia.
Saayman, G. S., C. K. Tayler, and D. Bower.
1973. Diurnal activity cycles in captive and free-ranging
bottlenose dolphins {Tursiops aduncus Ehrenburg).
Behaviour 44:212-233.
SCHALLER, G. B.
1972. The Serengeti lion. A study of predator-prey relations.
Univ. Chicago Press, Chic, 480 p.
Smith, G. J. D., K. W. Browne, and D. E. Gaskin.
1976. Functional myology of the harbour porpoise, Phocoena
phocoena (L.). Can. J. Zool. 54:716-729.
Smith, G. J. D., and D. E. Gaskin.
1974. The diet of harbour porpoises {Phocoena phocoena (L.))
in coastal waters of eastern Canada, with special reference
to the Bay of Fundy Can. J. Zool. 52:777-782.
Smith, G. J. D., C. L. Jovellanos, and D. E. Gaskin.
1984. Near-surface bio-oceanographic phenomena in the
Quoddy region. Bay of Fundy. Can. Itech. Rep. Fish. Aquatic
Sci. No. 1280, 124 p.
Smith, G. J. D., A. J. Read, and D. E. Gaskin.
1983. Incidental catch of harbor porpoise, Phocoena phocoena
(L.), in herring weirs in Charlotte County, New Brunswick,
Canada. Fish. Bull., U.S. 81:660-662.
Springer, J. T.
1979. Some sources of bias and sampling error in radio tri-
angulation. J. Wildl. Manage 43:926-935.
Watson, A. P., and D. E. Gaskin.
1983. Observations on the ventilation cycle of the harbour por-
poise Phocoena phocoena (L.) in coastal waters of the Bay of
Fundy Can. J. Zool. 61:126-132.
Wells, R. S., A. B. Irvine, and M. D. Scott.
1980. The social ecology of inshore odontocetes. In L. M.
Herman (editor), Cetacean behavior: mechanisms and func-
tions, p. 263-317. John Wiley and Sons, N.Y.
WiJRSiG, B.
1982. Radio tracking dusky porpoises in the South Atlantic
In Mammals in the seas, Vol. 4, p. 145-160. FAO Fisheries
Series No. 5.
552
EARLY POSTNATAL GROWTH OF
THE SPOTTED DOLPHIN, STENELLA ATTENUATA, IN
THE OFFSORE EASTERN TROPICAL PACIFIC
Aleta a. Hohn' and p. S. Hammond^
ABSTRACT
Estimates of length at birth and early postnatal growth are made for the northern and southern popula-
tions of the offshore spotted dolphin in the offshore eastern tropical Pacific Length at birth is estimated
to be 85.4 cm for the northern population and 83.2 cm for the southern population. Analyses of series
of monthly distributions of length revealed two cohorts born each year in the northern population, at
least in the northern inshore part of its geographic range, but only one cohort born each year in the southern
population. Growth curves fitted to the means of the monthly distributions of length gave estimates of
length at 1 year of 126.2 and 132.6 cm and length at 2 years of 154.3 and 154.9 cm for the two cohorts
in the northern population, and length at 1 year of 127.9 cm for the southern population. A growth curve
fitted to lengths and ages (in dental growth layer groups) from the northern population gave estimates
of lengths at 1 and 2 years of 123.0 and 143.0 cm, respectively.
The average growth rate of individual animals in a
population is an important characteristic because of
its correlation with other population parameters. In
fisheries biology, two commonly employed techniques
used to estimate growth rates are the aging of a sam-
ple of fish of known length and the following of a
series of length distributions through time These
techniques allow the relationship between length and
age (or relative age) to be applied to a much larger
sample of fish, provided that the aged sample is a
representative ona
For most species of fish, length-age relationships
may be appropriate for the entire life of the animals,
or at least for the period of interest to a commer-
cial fishery. In marine mammals, however, length
changes little, if at all, after attainment of physical
maturity. Growth rates may change markedly even
while the animal is maturing, being high for an ini-
tial period after birth and then declining quite rapid-
ly. In delphinids, the growth rate has been found to
be high in the first year, with animals typically in-
creasing by 50-70% of their birth length (Sergeant
1962; Kasuya et al. 1974; Kasuya 1976; Miyazaki
1977; Hohn 1980; Perrin and Henderson 1984), but
then declined rapidly in the second year. During this
'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, J^OAA, P.O. Box 271, La Jolla, CA 92038.
^Inter-American Tropical Tlina Commission, Scripps Institution
of Oceanography, La Jolla, CA 92098; present address: Sea Mam-
mal Research Unit, c/o British Antartic Survey, Madingley Road,
Cambridge CBS OET, United Kingdom.
period, growth rates are high relative to the varia-
bility in age-at-length so that length distributions are
distinguishable as separate age groups. Consequent-
ly, length-age relationships for these animals are
most useful from birth until about 2 yr.
In this paper, we have used both the technique of
following a series of length distributions from month
to month and the technique of aging a sample of
dolphins of known length to estimate the rate of
growth in the spotted dolphin, Stenella attenuata,
in the offshore eastern tropical Pacific (hereafter
referred to as the offshore spotted dolphin). In
neither of these two techniques did we have an ab-
solute measure of age. Consequently, we have esti-
mated length at birth independently and used this
to fix time at birth. Growth curves were fitted to the
length data by relative age and then length at birth
was substituted in order to predict length-at-
age
THE SAMPLE
The field data and specimens used in the follow-
ing analyses were collected by National Marine
Fisheries Service (NMFS) and Inter-American
Tropical lUna Commission (lATTC) scientific techni-
cians aboard commercial tuna purse seiners from
1968 to 1982. Procedures for collecting sample data
and specimens have been described by Perrin et al.
(1976). In all the following analyses, the data have
been stratified into northern and southern popula-
Manuscript accepted December 1984.
FISHERY BULLETIN: VOL. 83. NO. 4, 1985.
553
FISHERY BULLETIN: VOL. 83, NO. 4
tions divided by lat. 1°S, based on a division selected
by Perrin et al. (1S79). Areas 1 and 2 in Figure 1
correspond to the region occupied by the southern
offshore spotted dolphin and areas 3-8 correspond
to the region occupied by the northern offshore spot-
ted dolphin.
ESTIMATION OF LENGTH AT BIRTH
An accurate estimate of length at birth is impor-
tant because it establishes a point through which any
growth curve should pass. This extra degree of
freedom allows greater accuracy in fitting growth
curves and estimating growth rates. Neither of our
methods of relating length to age, described below,
allows us to fix absolute age so it is essential here
for us to calculate an independent estimate of length
at birth.
A commonly used method of estimating length at
birth when a sufficient sample is available is to re-
gress the percent postnatal at each length interval
on length and to calculate the length at which 50%
of the specimens are predicted to be postnatal. This
method, using a linear model, has been employed to
estimate length at birth for spotted dolphins (Per-
rin et al. 1976), for striped dolphins, S. coeruleoalba,
(Miyazaki 1977), and for spinner dolphins, S.
longirostris, (Perrin et al. 1977), and using a
nonlinear model for spinner dolphins (Perrin and
Henderson 1984). Another method commonly
employed when a small sample is available is to
estimate the average length at birth as the mean
length of known neonates or the mean length of full-
term fetuses and small calves combined. This method
has been used to estimate length at birth for long-
finned pilot whales (Sergeant 1962), for spotted
dolphins (Kasuya et al. 1974), for bottlenose dolphins,
Tursiops truncatus, (Ross 1977; Hohn 1980), and for
I'll
\tO lEE lED MS MO tSS 130 IZS IZO IIS 110 lOE 100 35
Figure L— Areas inhabited by the offshore spotted dolphin. The numbered regions refer to strata investigated in analyses of monthly
distributions of length. In all analyses, the southern population is from areas 1 and 2, and the northern population is from areas 3 through 8.
554
HOHN and HAMMOND: POSTNATAL GROWTH OF SPOTTED DOLPHIN
the franciscana dolphin, Pontoporia blainvillei,
(Kasuya and Brownell 1979).
Methods
The data used in this analysis were from all fetuses
and calves sampled between 1973 and 1981 except
for three specimens <68 cm identified as calves and
one specimen of 91 cm identified as a fetus {n = 609).
These four specimens were judged to have been
misidentified. The data were stratified by area, north
and south of lat. 1°S, and the northern sample was
further stratified by the size of kill in each net set.
Powers and Barlow (1979^) have shown that in net
sets in which the kill of spotted dolphins from the
northern offshore regions was <40 (small-kill sets),
about twice as many calves were killed as a propor-
tion of the total kill as in sets where the kill was >40
(large-kill sets). This would introduce a bias in the
estimate of length at birth in the regression pro-
cedure because about 90% of all northern specimens
were from small-kill sets. The effect would be to
underestimate length at birth because the ratio of
calves to fetuses was too high in most of the sam-
ple Td investigate the extent of the bias, we
calculated average length at birth for all northern
specimens, for specimens from sets with kill <40 and
>40, and for specimens from sets with kill <30 and
>30 because the sample size for sets with kill >40
was small. The small sample available for southern
specimens prevented any further stratification of the
data.
Length at birth was estimated by fitting a logistic
model to the percent postnatal at each length inter-
val, weighted by the inverse of the binomial variance
of each percentage, and estimated by calculating
from the fitted curve the length at which 50% of the
specimens were predicted to be postnatal. We also
investigated linear and asymmetric logistic-type
models.
improve the fit and gave similar results.
Ikble 1 shows that the estimates of length at birth
for northern specimens using the unstratified data
(82.0 cm) and using specimens from sets with kill
<30 (81.6 cm) or <40 (81.6 cm) are lower than the
estimates using specimens from sets with kill >30
(84.6 cm) or >40 (85.4 cm), demonstrating that the
bias resulting from an overrepresentation of calves
in small-kill sets is significant. Furthermore, the
estimate for kill >40 is higher than that for kill >30,
indicated that the proportion of calves in the sam-
ple may still be a function of kill-per-set at this level.
Further stratification to investigate whether or not
estimates of length at birth continue to rise at higher
thresholds of kill-per-set was not possible because
of small sample siz&
The estimate of length at birth for southern
specimens is 83.2 cm. No stratification was possible
because of the small sample
Estimates of standard deviations of the estimates
of length at birth are not given because, in fitting
the logistic model, sums of squares were minimized
for differences between observed and predicted per-
cent postnatal and it was unclear how to calculate
the standard deviations.
Table 1.— Estimates of length at birth stratified by number of
offshore spotted dolphins killed per set. The range of length
classes includes the last 0% postnatal length class and the first
100% postnatal length class.
Length at birth
predicted from the
Sample
Range
logistic model
size
(cm)
(cm)
Northern offshore spotted dolph
in
Unstratified data
586
71-92
82.0
Sets with kill <30
321
73-92
81.6
Sets with kill <40
384
71-92
81.6
Sets with kill >30
105
71-89
84.6
Sets with kill >40
36
78-89
85.4
Southern offshore spotted dolph
lin
Unstratified data
23
78-85
83.2
Results
Figure 2 shows the length-frequency data for
northern specimens from sets with kill <40, and the
logistic model fitted to the data. Figure 3 is the
equivalent for northern specimens from sets with
kill >40. Tkble 1 gives the results for all stratifica-
tions described above using the logistic model. Using
the linear or asymmetric logistic-type models did not
^Powers, J. E., and J. Barlow. 1979. Biases in the tuna-net
sampling of dolphins in the eastern tropical Pacific Doc
SOPS/79/31, Status of Porpoise Stocks Workshop, La Jolla, CA,
27-31 August 1979. Unpubl. MS.
Discussion
Our estimate of length at birth of 82.0 cm from
the unstratified northern data is similar to that of
Perrin et al. (1976), who estimated length at birth
at 82.5 cm, based on a sample of 73 northern
specimens (calves and fetuses) grouped into 3 cm in-
tervals from 74 to 92 cm.
Estimates of length at birth in large-kill sets are
less biased because of the overrepresentation of
calves in small-kill sets. A future larger sample from
large-kill sets may allow for additional stratification
by kill-per-set, enabling estimates to be calculated
555
FISHERY BULLETIN: VOL. 83, NO. 4
>
o
z
UJ
o
HI
cc
u.
26 r
20 -
I FETUSES
0 CALVES
10
70 72 74 76 78 80 82 84 86 88 90 92 94
LENGTH (cm)
100 r
80
<
<
Z
0)
o
LU
o
K
U
a.
60
40
20
Average length
at birth
I I I I I I I
I T I t I T I I I I I I'l I I I I I
70 72 74 76 78 80 82 84 86 88 90 92 94
LENGTH (cm)
Figure 2.— Length-frequency data for specimens from sets with Itill <40 grouped in 1 cm inter-
vals for 163 fetuses and 221 calves from the northern offshore population of spotted dolphins,
and the logistic model fitted to the percentage of animals that were postnatal.
using specimens from sets with higher levels of kill.
It may then be possible to determine at what level
of kill-per-set the estimate ceases to increase. Until
additional data are available, we consider 85.4 cm to
be the best estimate of length at birth in northern
offshore spotted dolphins.
Our estimate of length at birth in the southern off-
shore spotted dolphin of 83.2 cm is more ques-
tionable because we were unable to stratify by kill-
per-set. As adults, southern specimens are about 2.5
cm shorter than their northern counterparts (Per-
rin et al. 1979). This small, but statistically signifi-
cant, difference may or may not imply that length
at birth is smaller in the southern population. The
small sample of 23 specimens used in our calcula-
tion of length at birth raises doubts concerning the
556
HOHN and HAMMOND: POSTNATAL GROWTH OF SPOTTED DOLPHIN
>■
o
z
UJ
o
UJ
DC
12
8
4
0
- I FETUSES
CALVES
Ira
70 72 74 76 78 80 82 84 86 88 90 92 94 96
LENGTH (cm)
100 r
<
<
0)
o
a.
LU
o
UJ
a
Average length
at birth
I I I I I I i"r I f I f I f ri I I I I I I I I I I
70 72 74 76 78 80 82 84 86 88 90 92 94 96
LENGTH (cm)
Figure 3— Length-frequency data for specimens from sets with kill >40 grouped in 1 cm intervals
for 21 fetuses and 15 calves from the southern offshore population of spotted dolphins, and the logistic
model fitted to the percentage of animals that were postnatal.
accuracy of this estimate For these reasons, we take
the estimate from all southern specimens of 83.2 cm
as our provisional best estimate of length at birth
for southern offshore spotted dolphins while
recognizing that this estimate may be biased
downwards because of a possible overrepresentation
of calves in the sample.
ESTIMATION OF LENGTH-AT-AGE
USING ANALYSES OF
MONTHLY DISTRIBUTIONS OF LENGTH
Perrin et al. (1976) used the technique of fitting
a growth curve to the means of normal distributions
fitted to length-frequency data by month to estimate
the length of the offshore spotted dolphin at 1 yr
of age Perrin and Henderson (1984) used the same
technique for the spinner dolphin. The technique is
based on the assumption that breeding in these
dolphins is seasonal and that a cohort of animals
born at approximately the same time is characterized
by a distribution of lengths, identifiable as a mode
in the overall length distribution, which can be
followed from month to month as mean length of the
cohort increases. If there are sufficient data in each
month, mean lengths can be followed from birth until
557
growth slows to an extent that distributions of
lengths from different cohorts cannot be distinguish-
ed. A growth curve can then be fitted to the month-
ly mean lengths.
Since the analysis of Perrin et al. (1976), the sam-
ple of measured lengths from offshore spotted
dolphins has increased from about 3,500 to over
15,000. Consequently, we were able to analyze the
available data more extensively than had been done
previously.
Methods
Length measurements from all postnatal
specimens, made between 1968 and 1982, were used
in the analyses except for three specimens <68
cm which were judged to have been erroneously
identified as calves. The data were stratified
into eight areas based upon apparent hiatuses in
distribution from examination of sightings and ef-
fort data (Fig. 1). Areas 1 and 2 comprise the
southern population and areas 3-8 the northern
population.
For the northern data, no consistency could be
found in preliminary analyses of lengths when data
from all areas were included. When area 3 was ex-
cluded, consistency was much improved. When areas
4 and 5 were also excluded, consistency was improved
further for the months of February through June
This indicated that there were nonseasonal or
seasonal but asynchronous elements in areas 3, 4,
and 5 at least at certain times of the year. Conse-
quently, in our analyses of northern data we used
lengths from areas 6, 7, and 8 only for February
through June and lengths from areas 4-8 for January
and July through December. A similar situation
occurred for the southern data where the elimina-
tion of area 2 improved consistency for January
through May. In our analyses of southern data,
therefore, we used lengths only from area 1 for these
months.
The data were grouped in interval widths of 4 cm.
This gave four possible ways of grouping the data
because lengths were measured to the nearest whole
centimeter. Each of these four groupings were in-
vestigated, there being no reason to prefer a start-
ing point of the first interval as, for example, 76, 77,
78, or 79 cm.
A mixture of normal distributions was fitted to
each data set using a version of the computer pro-
gram NORMSEP (Hasselblad 1966). The program
requires the number of distributions to be specified,
and this was varied in order to determine the most
likely number of distributions present. The model
FISHERY BULLETIN: VOL. 83, NO. 4
selected as most representative of the length-
frequency data was that which gave the highest x"
value, and therefore the highest probability that a
greater ^ value could be obtained by chance alone,
and also gave biologically feasible results based on
prior knowledge of delphinid growth. (Some model
fits had a very high probability of a greater ^, but
the mean lengths could not be accounted for by any
reasonable regime of growth.)
We chose Laird's (1969) form of the Gompertz
(1825) growth equation to fit to the monthly mean
lengths. A linear model is clearly inadequate to
describe growth except over a very short time period.
We also investigated the use of the von Bertalanffy
(1934) growth equation but found it to be less flexi-
ble than the Gompertz model.
Each model of growth was fitted to the mean
lengths using the midpoint of the first month as time
zero. In fact, this is not necessarily the time of birth
so we fixed time of birth by substituting our estimate
of length at birth into the fitted equation. Lengths
at age were then calculated by substituting that age
plus the difference between the midpoint of the first
month and our calculated time of birth into the fit-
ted equation.
Results
Northern Population
Figure 4 shows, as examples, the fitted mixture
of normal distributions to the length-frequency data
for August and October. The arrows indicate the
positions of the means of the fitted distributions.
Ihble 2 shows the estimates of mean length of the
fitted normal distributions for each month. The
estimates are presented so that the increases from
month to month can be clearly seen. The two final
columns of Tkble 2 are mean lengths of the two
distributions to the right of the length-frequency
plots. These mean lengths are consistent from month
to month. The table shows that there are actually
two series of mean lengths: one beginning at 86.7
cm in September and continuing through columns
2 and 4 of the mean lengths, and the other begin-
ning at 84.5 cm in April (the estimate of 92.7 cm for
March is an anomaly for which we have no explana-
tion) and continuing through columns 1, 3, and 5.
These represent two cohorts born each year about
6 mo apart in the spring and autumn. Note that each
series of mean lengths continues only for about 24
mo. This is because after this time growth has slow-
ed to an extent that it is not possible to distinguish
distributions of length from different cohorts. The
558
HOHN and HAMMOND: POSTNATAL GROWTH OF SPOTTED DOLPHIN
60-1
70
SO 110 130 150 170 ISO
LEhGTH (Cn)
^0
>
u
z
o
UJ
u.
120n
100-
80-
60-
40-
20-
70 90 110
130150 170
LEhGTH <Cn)
Figure 4— Histograms of length and the fitted mixture of normal distributions for data for the north-
ern offshore spotted dolphin in (A) August and (B) October. The arrows indicate the positions of the
means of the fitted distributions.
559
FISHERY BULLETIN: VOL. 83, NO. 4
mean length of 105.9 cm for June was not included
in further analyses because its inclusion more than
doubled the residual sums of squares for the model
fit. We consider it an outlier.
Figure 5 shows Gompertz models of growth fit-
ted separately to the mean lengths, excluding the
92.7 cm point for March, from columns 1, 3, and 5
(curve A) and, excluding the 105.9 cm point for June,
from columns 2 and 4 (curve B) of Ikble 2. Time at
birth and lengths at 1 and 2 yr were calculated as
Table 2.— Mean lengths of the fitted normal distributions for the northern
offshore spotted dolphin.
Sample
Month
size
Mean lengths of fitted distributions (cm)
September
536
86.7 105.0 129.4 161.3 186.9
October
1,159
87.9 106.3 129.4 142.7 163.1 188.8
November
616
91.9 113.9 129.6 145.7 159.4 187.7
December
223
97.5 127.7 149.9 187.4
January
2,926
102.9 142.4 161.9 187.4
February
2,772
104.1 140.7 151.8 161.5 186.3
March
866
192,7
113.2 131.4 160.7 188.7
April
700
84.5
113.6 146.0 163.6 188.5
May
423
84.5
108.7 133.9 147.5 165.9 187.9
June
300
90.7
n05.9 135.5 165.2 189.5
July
266
91.8
118.0 136.1 150.8 164.5 190.1
August
486
105.7
125.1 151.8 162.6 190.5
'These mean lengths were not Included in further analyses.
160
Lt = 82.0e
E 140
u
H
O
z
120
<
g 100
80
0.059
"•"^^ ri_e-o.o79n
0.079 U ® J
0.057 L' ** -J
MAMJ
I I I I I I I
J ASOND J
I I I I I I
FMAM J J
ASOND J FM AMJ J ASO
MONTH
Figure 5.— Mean values of monthly distributions of length from data for the northern offshore spotted dolphin. The
two curves represent two annual cohorts fitted separately by the Gompertz model of growth. NOTE: The equations
were fitted using relative time and are not therefore accurate models of growth, lb obtain such growth models, relative
time can be converted to absolute time using the estimate of length at birth and the equation refitted to these data.
560
HOHN and HAMMOND: POSTNATAL CROWTH OF SPOTTED DOLPHIN
described above with the following results:
Growth
Growth
curve A
curve B
85.4 cm
85.4 cm
May 9
September 11
132.6 cm
126.2 cm
154.9 cm
154.3 cm
Fi.xed length at birth
(estimated in this paper)
Estimated time of birth
Estimated length at 1 yr
Estimated length at 2 yr
Rates of growth as centimeters per month for the
two fitted curves adjusted for length at birth are as
follows:
Rate
of growth
iths after
birth
Curve A
Curve B
0
5.03
3.80
6
3.94
3.43
12
2.76
2.89
18
1.81
2.33
24
1.14
1.82
Southern Population
Thble 3 shows the estimates of mean length of the
fitted normal distributions for each month. For these
data it is clear, apart from the mean lengths of 105.0
cm in January and 127.5 cm in May, that there is
only one cohort born each year in the southern sum-
mer. As a result of this and the much smaller sam-
ple sizes, distributions of length could only be
distinguished up to about 18 mo. The two final
columns of Tkble 3 show the mean lengths of the two
distributions to the right of the length-frequency
plots. These are quite consistent from month to
month, as with the northern data.
Figure 6 shows the Gompertz model of growth fit-
ted to the mean lengths from columns 1 and 3 of
Tkble 3. Time at birth and length at 1 yr were
calculated as described above with the following
results:
Fixed length at birth
(estimated in this paper)
Estimated time of birth
Estimated length at 1 yr
83.2 cm
6 January
127.9 cm
Rates of growth for this fitted curve do not
decrease from birth as they do for the northern
population because, the curve has a point of inflec-
tion at approximately 50 mo. The rates of growth
at 0, 6, 12, and 18 mo after birth are 3.29, 3.72, 4.12,
and 4.47 cm/mo, respectively.
Table 3.— Mean lengths of the fitted normal distributions for
the southern offshore spotted dolphin.
Sample Mean lengths
of fitted distributions
Month
size
(cm)
December
47 81.0
123.5
165.7 187.9
January
254 87.0 M05.0
131.0
164.5 187.8
February
412 85.1
134.9
165.6 188.0
March
57 90.0
139.3
189.7
April
43 97.9
140.8
163.3 189.5
May
212 97.1 '127.5
144.3
157.7 182.6
June
42 99.0
163.8 185.3
'These mean lengths were not included
in further analyses.
Discussion
There are several sources of variability in the
estimates of mean length by month to which the
growth models have been fitted. There is individual
variation in time of birth, length at birth, and growth
rate The calving season may vary from year to year
and area to area. The specimens which were
measured are subject to the usual sampling varia-
tion. Sampling in a particular year may not have been
random with respect to time in each month. Given
these sources of variability, it is interesting that the
results should appear so consistent.
The growth curves were fitted to the unweighted
mean lengths. If the variation in the mean length
of a distribution is considered to be due largely to
sampling error, then there is a justification for a
weighted regression. We believe that this is not
necessarily the case and that the unweighted regres-
sions represent the best descriptions of growth for
these data. When weighted regressions were per-
formed the fitted curves changed negligibly.
The most important potential problem is that the
method relies upon being able to analyze a sample
of data in which reproduction is seasonal and in
which the timing of seasonality is constant. This
analysis has shown that this may be difficult to
achieve. Only by stratification of the data by area
could consistent results be obtained. Stratification
of the data by area improves the consistency of the
series of mean lengths because offshore spotted
dolphins appear to have different calving seasons
depending upon the area of capture In probability,
this seasonality is not actually a function of area but
of schools or groups of schools which tend to inhabit
different areas with different environmental condi-
tions. Thus, even with the best stratification scheme,
there may always be asynchronous seasonal elements
in a sample of data from any given area affecting
the estimation of the mean lengths of the cohorts.
In this analysis we pooled the data from several
years for our monthly samples, rather than attempt-
561
FISHERY BULLETIN: VOL. 83, NO. 4
160
E 140
u
X
I-
0.040
Lt = 81.0e 0017 V ^ J
I I I
ND J
I I I I I I
FMAMJ
I I I I i I
J ASON D J
I I I I I
FMAMJ
MONTH
Figure 6— Mean values of monthly distributions of length from data for the
southern offshore spotted dolphin. The curve represents one annual cohort
fitted by the Gompertz model of growth. The open circles were not included
in the fitting of the curve. NOTE: The equations were fitted using relative
time and are not therefore accurate models of growth, lb obtain such growth
models, relative time can be converted to absolute time using the estimate of
length at birth and the equation refitted to these data.
ing to follow actual cohorts of animals from in-
dividual years as did Perrin et al. (1976) in their
analyses. Combining the data from several years in-
troduces additional variation in the data if the timing
of the calving season varies from year to year, but
it increases sample sizes and minimizes bias caused
by nonrandom timing of sampling within months.
In addition, we are mainly interested in an average
growth rate which is best estimated from several
years of data.
Perrin et al. (1976) fitted a linear model to mean
lengths estimated in the months of October 1972,
January, February, March, and April through June
1973 from which they extrapolated to obtain an
estimate of length at 1 yr of 147.5 cm for the north-
ern offshore spotted dolphin. The authors recognized
that this estimate was biased upwards because
growth rates of delphinids do decrease in the first
year and revised this estimate downwards based on
aged specimens. We believe our analyses to be more
accurate than those of Perrin et al. (1976) and our
results to be a substantial improvement.
Barlow (1984) found an indication of two peak
calving seasons for spotted dolphins north of the
Equator, in the spring and autumn, but that the
animals were born throughout the year. South of the
Equator he found a single season peaking around
April. These results are similar to ours but the timing
of the southern season does not agree The difference
can be explained by Barlow's use of Perrin et al.'s
(1976) growth curve which predicted a mean length
of 138.0 cm for 1-yr-old animals. Our growth equa-
tions predict animals of this length to be from 14
to 16 mo old.
The two growth curves fitted to the mean lengths
from the two cohorts in the northern region predict
different lengths-at-age and are characterized by
very different growth rates. It is possible that these
two cohorts actually grow at different rates because
of environmental factors, but we believe that the dif-
562
HOHN and HAMMOND: POSTNATAL GROWTH OF SPOTTED DOLPHIN
ferences are more likely a result of variability in the
data. We suggest, therefore, that the mean of the
estimates from both growth curves be used for
estimates of lengths-at-age for the northern offshore
spotted dolphin.
For the southern population, the mean lengths of
105.0 and 127.5 cm for January and May, respec-
tively, suggest that there may be two calving sea-
sons in this area. At present, the sample size is
too small to assess whether or not this is the
casa
ESTIMATION OF
LENGTH-AT-AGE USING
GROWTH-LAYER-GROUP (GLG) AGING
Increments of tissue are deposited in teeth as a
function of time The most important incremental
pattern in odontocete teeth is comprised of growth
layer groups (GLGs), defined as "a repeating or semi-
repeating pattern of adjacent groups of incremen-
tal growth layers within the dentine, cementum, or
bone which is defined as a countable unit" (Perrin
and Myrick 1980, p. 48-49). These GLGs are used
for age determination in many species of odon-
tocetes, as well as pinnipeds and sirenians (see
review by Scheffer and Myrick 1980), but in most
species no calibration of GLGs with absolute time
is available However, a few known-age captive and
minimum-known-age captive bottlenose dolphins
(Sergeant 1959; Sergeant et al. 1973; Hui 1978) and
captive tetracycline-marked specimens of other
species {Lagenorhynchus obscurus, Best 1976;
Delphinus delphis, Gurevich et al. 1980; 5. longi-
rostris, Myrick et al. 1984) have provided evidence
that the GLG as defined and calibrated by these
workers represents an annual deposition pattern. In
the absence of any known-age specimens of spotted
dolphins, we have assumed that a GLG pattern
similar to that described in the above species
represents the same amount of time
Methods
A sample of 800 males and 800 females, selected
randomly from the specimens collected between
1973 and 1978, and all 312 female specimens col-
lected in 1981 made up the sample of animals from
which teeth were aged.
The teeth were decalcified in RDO^, a commercial
decalcifying agent, cut longitudinally into 24 ^m thin
sections using a freezing microtome, stained in
■•Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
haematoxylin, and mounted in 100% glycerin. Detail-
ed procedures for the preparation technique and
interpretation of GLGs are described by Myrick et
al. (1983).
Tfeeth from each of the 1,600 specimens collected
between 1973 and 1978 were "read" for age at least
three times, to the nearest 0.1 GLG in young animals,
by each of two readers over a period of 2 yr. The
series of age estimates was averaged for each reader,
and the resulting two mean age estimates were again
averaged to produce a pooled mean age estimate (see
Reilly et al. 1983). Only one age reading was made
by each reader for the 312 specimens collected in
1981, and the mean of these two readings deter-
mined. For lack of a preference for one reader's
estimates, growth rate analyses used the pooled
mean and mean age estimates. Growth models were
fit to the age-length data for males and females
separately.
Growth rate was estimated by regressing length
on number of GLGs (age) using Laird's (1969) form
of the Gompertz model. The data were truncated at
<3.0 GLGs in order to reduce the effects of older
animals on our estimates of growth in the first 2 yr,
in case the chosen model failed to describe growth
adequately over a wider range of ages. Length at
birth was fixed at the independently estimated value
of 85.4 cm (see above).
Results
There was no difference in growth between males
and females at this age Therefore, the data were
pooled. Figure 7 shows the Gompertz model of
growth fitted to the pooled data. The model gives
a predicted length of 123 cm (SD = 0.7 cm) at 1 yr
and a predicted length of 143 cm (SD = 0.6 cm) at
2 yr. These standard deviations are underestimates
because they do not incorporate variability in the age
of individual specimens resulting from between
reader differences.
Figure 7 also shows that lengths predicted by this
model may be underestimated up to about 8 mo and
overestimated from about 8 to 13 mo. For com-
parison with predicted length at 1 yr from the model,
the mean length of specimens aged between 0.9 and
1.1 yr (n = 24) is 121 cm with a range of 101-140 cm.
The estimated monthly growth rate is 3.84 cm/mo
initially, falling to 3.11 cm/mo at 6 mo, 2.33 cm/mo
at 12 mo, 1.67 cm/mo at 18 mo, and 1.15 cm/mo at
24 mo.
Discussion
The accuracy of these length-at-age estimates
563
FISHERY BULLETIN: VOL. 83. NO. 4
depends upon the representativeness of the sample,
the accuracy of the readings, the assumptions that
1 GLG equals 1 yr, and the adequacy of the growth
model.
The sample analyzed w^as a simple random sam-
ple, stratified only by sex, taken from all specimens
collected betw^een 1973 and 1978. These were them-
selves a sample of the animals killed incidental to
fishing operations, which were a sample of the
population. Although Powers and Barlow (fn. 2) have
shown a bias towards a higher proportion of calves
killed in purse seine nets, we have no reason to
believe that the relationship between length and age
is different in our sample than in the population.
Teeth were read as accurately as possible Reilly
et al. (1983) have investigated the precision of the
readings but, without known-age animals, it is not
possible to validate their accuracy.
Our assumption that 1 GLG equals 1 yr is based
on captive, tetracycline-marked Hawaiian spinner
dolphins (Myrick et al. 1984) a distantly related
species. Known-age, captive or marked spotted
dolphins are not available for direct GLG calibration.
If differences are found between GLG in spotted and
spinner dolphin teeth when data from known-age
spotted dolphins are available, these estimates of
growth based on GLGs will need to be revised.
It is often assumed that when one GLG is
deposited each year the first GLG begins with the
neonatal line immediately at birth and ends precisely
1 yr later. Yet it is possible, as suggested by Perrin
et al. (1977) for S. longirostris, that the first GLG
is not always complete Teeth from young, known-
age dolphins from the same stock born at different
times during the year are needed to address this
question.
It is also possible that the neonatal line may not
be deposited immediately at the time of birth. In
bottlenose dolphins, stranded on the mid-Atlantic
coast of the United States, variability has been found
in the time of deposition of the neonatal line in 18
neonatal specimens (Hohn unpubl. data). These
specimens were identified as neonates because they
lacked the umbilicus (indicating that the calf was not
stillborn) and their dorsal fin and flukes were fold-
ed (Ikvolga and Essapian 1957). Some of these
stranded specimens showed no neonatal line while
others had part of a neonatal line deposited. Similar-
ly, in our sample of offshore spotted dolphins from
northern areas there is not neonatal line in some
postnatal specimens so that the amount of time since
birth is unknown. This difference in timing of
neonatal line deposition may be due to individual
variation in tooth growth and mineralization or small
difference in gestation time
The precise timing of the deposition of the first
180
Figure 7.— Length-age [GLGs, (growth
layer groups), pooled mean estimates] data
for northern offshore spotted dolphins up
to 3.0 GLGs, and the fitted Gompertz model
of growth.
2.0
AGE (years)
3.0
4.0
564
HOHN and HAMMOND: POSTNATAL GROWTH OF SPOTTED DOLPHIN
GLG (beginning with the neonatal Hne) is important
in estimates of age in young animals. For a specimen
estimated to be 0-yr-old based on GLGs but which
is known not to be a neonate, the age must neces-
sarily be an underestimate of the actual age of that
specimen, and, consequently, the average length of
"0-yr-olds" would be greater than the average length
of new-born specimens. When the Gompertz model
(with L„ not fixed) is fitted to the age data, the
predicted length at age 0 is 89.6 cm, 4.2 cm higher
than the length-at-birth estimate The age at which
the predicted length is 89.6 cm when Lq is fixed at
85.4 cm is about 0.1 GLGs. This indicates a possible
bias of about 0.1 GLGs for young animals. However,
this difference between predicted length for fits of
the model with fixed and floated Lq diminishes
rapidly and at 0.7 GLGs predicted length is 114.0
cm for both models.
The Gompertz model appears to be generally
suitable in describing the early growth of the off-
shore spotted dolphin based on GLG readings.
However, the pattern of points around the fitted line
in Figure 7 up to about 1.1 GLGs indicates that
growth during this period may not be adequately
described by a single curve This pattern may be a
result of either sampling variation or errors in
reading, but it may be due to changes in growth rate
during this period resulting from changes in food
intake Perrin et al. (1976) have estimated that wean-
ing occurs at about 11 mo in the offshore spotted
dolphin so that during the period from about 8 to
13 mo, milk intake will be decreasing and the intake
of solid food will be increasing. Growth rates may
well reflect these changes. If this is the case, a two-
cycle model may describe growth more accurately
during this period. Such an approach was used by
Perrin et al. (1976, 1977) in spotted and spinner
dolphins, respectively, to describe a secondary surge
in the growth of pre-adult animals.
CONCLUDING REMARKS
Our analyses have produced different estimates of
growth rates and lengths-at-age from two different
techniques. The reliability of fitting growth curves
to series of means of identifiable distributions of
length by month depends primarily upon being able
to select a sample in which breeding is both seasonal
and synchronous from year to year. The reliability
of fitting growth curves to length-age data as deter-
mined by counting GLGs depends primarily upon the
validity of the assumption that 1 GLG is equivalent
to 1 yr. We believe that neither technique is suffi-
ciently reliable to be labelled as the "best" method
or to try to calibrate the other. Rather, our analyses
underline the need for the analysis of data collected
from known-age animals of these populations.
However, we do believe that the estimates of growth
rates and lengths-at-age presented here are the best
currently available for offshore spotted dolphins
from the eastern tropical Pacific
ACKNOWLEDGMENTS
Teeth were prepared by P. Sloan, M. Kimura, and
D. Stanley. Age determination readings were made
by A. Myrick and the first author. J. Barlow offered
advice on growth models and W. Perrin made sug-
gestions during the course of the analyses. Most of
the illustrations were prepared by R. Allen. R.
Hankins and S. Chivers were particularly helpful in
data editing, computer programming, and some data
analysis. We would like to thank R. Brownell, Jr., D.
Chapman, F. Hester, and D. Siniff and colleagues at
the SWFC and lATTC, especially J. Barlow, D.
DeMaster, A. Myrick, W. Perrin, M. Scott, and A.
Wild for critical reviews of an earlier version of the
manuscript.
LITERATURE CITED
Barlow, J.
1984. Reproductive seasonality in pelagic dolphins, {Stenella
spp.): Implications for measuring rates. In W. F. Perrin, D.
P. DeMaster, and R. L. Brownell (editors), Reproduction in
cetaceans, p. 191-198. Rep. Int. Whaling Comm. Spec Issue
6.
Best, R B.
1976. Tfetracycline marking and the rate of growth layer for-
mation in the teeth of a dolphin, Lagenorhynchus obscu-
rus. S. Afr. J. Sci. 72:216-218.
Gompertz, B.
1825. On the nature of the function expressive of the law of
human mortality, and on a new mode of determining the
value of Life Contingencies. Philos. Trans. R. Soc Lond.
115:513-585.
GuREVicH, V. S., B. S. Stewart, and L. H. Cornell.
1980. [1981]. The use of tetracycline in age determination of
common dolphins, Delphinus delphis. In W. F. Perrin and
A. C. Myrick, Jr. (editors). Age determination of toothed
whales and sirenians, p. 165-170. Rep. Int. Whaling Comm.
Spec Issue 3.
Hasselblad, V.
1 966. E stimation of parameters for a mixture of normal distri-
butions. Tfechnometrics 8:431-444.
HoHN, A. A.
1980. Age determination and age related factors in the teeth
of western North Atlantic bottlenose dolphins. Sci. Rep.
Whales Res. Inst., Tbkyo 32:39-66.
HUL C.
1978. Reliability of using dentine layers for age determination
in Tursiops truncatus. U.S. Dep. Commer., Natl. Tfech. Inf.
Serv, PB288444, 25 p.
565
FISHERY BULLETIN: VOL. 83, NO. 4
Kasitwv, T.
1976. Reconsideration of life history parameters of the spot-
ted and striped dolphins based on cemental layers. Sci. Rep.
WTiales Res. Inst., Ibkyo 28:73-106.
Kasuya, T, and R. L. Brownell, Jr.
1979. Age determination, reproduction, and growth of Fran-
ciscana dolphin Pontoporia blainvillei. Sci. Rep. Whales
Res. Inst., Ibkyo 31:45-67.
Kasuya, T., N, Miyazaki, and W. H. Dawbin.
1974. Growth and reproduction of Stenella attenuata in the
Pacific coast of Japan. Sci. Rep. Whales Res. Inst., Ibkyo
26:157-226.
Laird, A. K.
1969. The dynamics of growth. Res. Dev. 2b(8):28-31.
Miyazaki, N.
1977. Growth and reproduction of Stenella coeruleoalba off
the Pacific coast of Japan. Sci. Rep. Whales Res. Inst., Ibkyo
29:21-48.
Myrick, a. C., Jr., E. W. Shallenberger, I. Kang, and D. B.
MacKay.
1984. Calibration of dental layers in seven captive Hawaiian
spinner dolphins, Stenella longirostris, based on tetracycline
labeling. Fish. Bull., U.S. 82:207-225.
Myrick, A. C., Jr., A. A. Hohn, P. A. Sloan, M. Kimura, and
D. Stanley.
1983. Estimating age of spotted and spinner dolphins,
(Stenella attenuata and Stenella longirostris) from teeth.
U.S. Dep. Commer., NOAA-TM-NMFS-SWFC-30, 17 p.
Perrin, W. F., J. M. Coe, and J. R. Zweifel.
1976. Growth and reproduction of the spotted porpoise,
Stenella attenuata, in the offshore eastern tropical Pacific
Fish. Bull., U.S. 74:229-269.
Perrin, W F., and J. R. Henderson.
1984. Growth and reproductive rates in two populations of
spinner dolphins, Stenella longirostris, with different
histories of exploitation. In W F. Perrin, D. P. DeMaster,
and R. L. Brownell (editors), Reproduction in cetaceans, p.
417-430. Rep. Int. Whaling Comm. Spec Issue 6.
Perrin, W. F., D. B. Holts, and R. B. Miller.
1977. Growth and reproduction of the eastern spinner dolphin,
a geographical form of Stenella longirostris in the eastern
tropical Pacific Fish. Bull. U.S. 75:725-750.
Perrin, W F., and A. C. Myrick, Jr. (editors).
1980. [1981]. Age determination of toothed whales and sire-
nians. Rep. Int. Whaling Comm. Spec Issue 3, 229 p.
Perrin, W. F., P. A. Sloan, and J. R. Henderson.
1979. Tkxonomic status of the 'south-western stocks' of spin-
ner dolphin Stenella longirostris and spotted dolphins S. at-
tenuata. In W F. Perrin and A. C. Myrick, Jr. (editors). Age
determination of toothed whales and sirenians, p.
175-184. Rep. Int. Whaling Comm. 29.
Reilly, S. B., a. a. Hohn, and A. C. Myrick, Jr.
1983. Precision of growth layer group ageing of spotted
dolphins. U.S. Dep. Commer., NOAA-TM-NMFS-SWFC-35,
27 p.
Ross, G. J. B.
1977. The taxonomy of bottlenosed dolphins Tursiops species
in South African waters, with notes on their biology. Ann.
Cape Prov. Mus. (Nat. Hist.) 11:135-194.
ScHEFFER, V. B., and A. C. Myrick, Jr.
1980. [1981]. A review of studies to 1970 of growth layers in
the teeth of marine mammals. In W. F. Perrin and A. C.
Myrick, Jr. (editors), Age determination of toothed whales
and sirenians, p. 51-64. Rep. Int. Whaling Comm. Spec Issue
3.
Sergeant, D. E.
1959. Age determination of odontocete whales from dentinal
growth layers. Norsk Hvalfangst-Tid. 48:273-288.
1962. The biology of the pilot or pothead whale Globicephala
melaena (Traill) in Newfoundland waters. Fish. Res. Board
Can., Bull. 132, 84 p.
Sergeant, D. E., D. K. Caldwell, and M. C. Caldwell.
1973. Age, growth, and maturity of bottlenose dolphin (Tur-
siops truncatus) from northeast Florida. J. Fish. Res. Board
Can. 30:1009-1011.
Tavolga, M. C, and F. S. Essapian.
1957. The behavior of the bottle-nosed dolphin (Tusiops trun-
catus): Mating, pregnancy, parturition and mother-infant
behavior. Zoologica (N.Y.) 42(1):11-31.
VON Bertalanffy, L.
1 934. Untersuchungen iiber die Gesetzlickeit des Wachstums.
Wilhelm Roux' Arch. Entwichlungsmech. Org. 131:613.
566
FACTORS AFFECTING THE GROWTH OF UNDERSIZE WESTERN
ROCK LOBSTER, PANULIRUS CYGNUS GEORGE,
RETURNED BY FISHERMEN TO THE SEA
R. S. Brown and N. Caputi^
ABSTRACT
The Western Australian fishery for the western rock lobster, Panulirus cygnus, yielded about 12,400 t,
valued at $A1G0 million, in 1982-83. It is the largest single species fishery in Australia and one of the
largest rock lobster fisheries in the world.
During a season, between 16 and 20 million undersize rock lobsters are brought aboard the vessels
by normal fishing operations, despite the escape gaps in all professional and amateur pots. All undersize
animals must be returned by fishermen to the sea, but to accomplish this it took from a few minutes
to hours, depending on the sorting technique used. The negative effects of handling on the survival of
the undersize lobsters have been previously reported, but another important aspect is the effect of handling
(damage, exposure, and displacement) on the growth rate of returned undersize rock lobsters.
Two laboratory experiments showed that growth increment at the first molt after air exposure was
significantly reduced, and in one of the experiments it was also significantly reduced for the second molt
after exposure
Three field tagging trials were conducted with 6,700 undersize rock lobsters. One trial showed that
exposure had a significant detrimental effect; the other trial in which exposure was tested, there was
a negative, but not significant, trend. Damage (number of appendages lost) and displacement from the
home range significantly reduced the growth increment in each of the three tagging trials. The growth
increment of damaged animals was inversely proportional to the number of appendages lost by the animal
with sizes ranging from 0.33 to 0.48 mm smaller per appendage missing. The losses to the fishery and
other associated problems caused by the reduced growth of the undersize lobsters are discussed.
The fully exploited stocks of western rock lobster,
Panulirus cygnus George, support the largest single
species fishery in Australia and one of the largest
rock lobster fisheries in the world, averaging 10,000
t for the last 9 yr to 1982-83. In 1982-83 the fishery
recorded its best season; the 12,400 t worth about
$A100 million, were landed by 780 boats licensed to
participate in the industry. The amateur catch from
the fishery, estimated at 1.6% of the professional
catch (Norton 1981), is considered to be a relatively
insignificant component of the total fishery, though
it may be locally important and occurs in shallow
areas where large numbers of undersize rock
lobsters (i.a, those with a carapace length <76 mm
and referred to below as undersize) are caught.
Fishing pressure on the rock lobster stock has
been increasing steadily during the past 20 yr, even
though it has been a Hmited entry fishery since 1963
(Morgan 1980a, b; Hancock 1981). This has led to
the need for constant monitoring of the fishery and
the updating of management procedures and regula-
Western Australian Marine Research Laboratories, Department
of Fisheries and Wildlife, P.O. Box 20, North Beach 6020, Western
Australia.
tions to ensure the stability and viability of the rock
lobster stock (Bowen 1980; Morgan 1980a, b; Han-
cock 1981; Morgan et al. 1982). An important com-
ponent of management of a fully exploited stock is
to reduce waste, ag., by predation and poor handling
techniques.
Two of the most important regulations that aid in
conservation of the western rock lobster stock per-
tain to undersize:
1) Compulsory use of a 54 x 305 mm escape gap
in each of the 76,000 professional and all amateur
pots (traps) in the fishery allows many undersize
animals to escape before the pot is pulled (Bowen
1963).
2) Undersize lobsters that do not escape and are
brought aboard must be returned to the sea.
Although use of escape gaps reduces the retention
of undersize lobsters by over 50% (Bowen 1963;
Brown unpubl. data), between 16 and 20 million
undersize animals are still handled each season by
professional fishermen (Brown and Caputi 1983).
The latter authors found that the handling practices
of fishermen, which cause exposure, damage
Manuscript accepted December 1984.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
567 -
FISHERY BULLETIN: VOL. 83, NO. 4
(number of legs and antennae missing), and displace-
ment of undersize lobsters, resulted in a drop in
recapture (mainly due to mortality) of 14.6%. After
allowing for the natural mortality expected before
the undersize lobsters would reach legal size, the ef-
fective reduction that could be expected was 11.4%.
For the 1982-83 season, the loss to the fishery could
have been in the vicinity of $A8 million.
An aspect of undersize lobster mortality and loss
of commercial production that was not discussed by
Brown and Caputi (1983) concerns the effect of
handling on the growth of these animals. If the
growth rate of the undersize lobster is reduced by
exposure, damage, and displacement, then it could
affect the rock lobster stock and the commercial
fishery in a number of important ways as discussed
by Davis (1981): 1) The time taken for undersize
lobsters to reach legal size would be increased; 2)
these animals would enter the commercial fishery
at a smaller size than those with unhindered growth;
and 3) the size at which these animals would attain
maturity would be reduced.
Other researchers have shown that the growth rate
of crustaceans generally and rock lobsters in par-
ticular is affected by a variety of environmental
factors such as food availability, temperature, photo-
period, molt phase, injuries, shelter availability,
salinity, and others (Chittleborough 1974a, 1975,
1976; Aiken 1980). Far less information is available
on the effects of commercial and recreational fishing
practice on the growth rates of exploited rock lobster
or other crustacean populations (Davis and Dodrill
1980; Davis 1981). Information that is available deals
almost exclusively with the injury (damage) compo-
nent of fishing activities or experimentation. Injury,
recorded as the loss of appendages, has been shown
to affect significantly the growth of rock lobsters P.
cygnus (Chittleborough 1975) and P. argus (Davis
1981) and the shore crabs Hemigrapsus oregonen-
sis and Pachygrapsus crassipes (Kuris and Mager
1975).
This paper reports effects of three major com-
ponents of the capture and release experience (i.e,
damage, exposure, and displacement) on the growth
rate of undersize lobsters caught from commercial-
ly fished populations of P. cygnus. The effect of the
various components was examined by tagging
lobsters that were exposed for various periods and
were displaced at different distances from their place
of capture, with any damage being recorded. Growth
of experimental animals between release and subse-
quent recapture was compared with that of control
lobsters which had not been exposed, damaged, or
displaced. Laboratory experiments were also con-
ducted in which undersize lobsters were exposed for
various periods and their growth rates subsequent-
ly monitored over the next two molts.
Consequences to the industry of any reduction in
growth rate are discussed in the light of results from
this research and the findings reported by Brown
and Caputi (1983).
LABORATORY EXPERIMENTS
Materials and Methods
Exposed undersize lobsters were maintained
under otherwise near optimal growing conditions of
excess food, adequate shelter, and protection from
potential predators (see also Chittleborough 1975)
and their molt increment and intermolt period com-
pared with those of unexposed animals.
Undersize lobsters (72-75 mm carapace length)
were collected from the field and transported in
aerated seawater tanks to the laboratory in January
1978. Each animal was examined for size, sex, and
damage. Sixty undersize lobsters with no damage
or maximum of one appendage missing were
selected and marked with numbered squares of
Dymo Scotch Ikpe,^ fixed to the dorsal side of the
carapace with Repco Super Glue and placed in open
circulation seawater tanks. Aquaria were checked
daily for molts, and animals were fed to excess on
whole live mussels and fresh fish. If molting had
occurred, the exuvia was removed and the newly
molted animal left for a week to harden before
measuring and renumbering. In January 1979, each
animal was allowed to undergo a minimum of two
molts before the entire group (Group I, consisting
of 4 subgroups of 15 animals) was given exposures
of 0, 15, 30, or 60 min at a temperature of 34°-35°C.
Animals that died prior to exposure were not
replaced.
After exposure, undersize lobsters were returned
to their tanks and were checked daily for any molts
or deaths. Feeding and renumbering was continued
as for pre-exposure Every animal that survived was
allowed at least two molts before the experiment was
terminated.
A second group of undersize lobsters (Group II,
consisting of 5 groups of 12 animals), collected in
June 1978, were treated in the exact manner as
described for Group I with the exception that ex-
posures of 0, 15, 30, 60, or 120 min at 20°-21°C took
place 18 mo later, in December 1979.
^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
568
BROWN and CAPUTI: FACTORS AFFECTING GROWTH OF ROCK LOBSTER
Results
In the January 1979 exposure experiment (Group
I), all eight undersize animals exposed for 60 min
died before the second molt after exposure, while one
animal died from each of 0-, 15-, and 30-min exposure
categories leaving 7, 10, and 7 animals respectively.
An analysis of variance on growth increment at
the first molt after exposure showed that exposure
was significant {P < 0.01) after other factors (&g.,
sex, damage, initial size), which may have affected
growth, were taken into account. However, at the sec-
ond molt after exposure, the effect of exposure on
growth increment was not significant (P > 0.05). An
analysis of variance on the time taken (days) between
the last molt before exposure and first molt after
exposure (intern lolt period) resulted in exposure
being not significant. Exposure was also not signifi-
cant for the following intermolt period.
In the December 1979 exposure experiment
(Group II), one animal died in the 0-, 15-, 30-, and
120-min exposure categories and two died from the
60-min exposure before the second molt after ex-
posure In this experiment, exposure had a signifi-
cant effect on the growth increment for both the first
(P < 0.001) and the second (P < 0.01) molts after ex-
posure. An analysis on the intermolt period for the
first molt after exposure showed no significant ef-
fect due to exposure, but exposure was significant
(P < 0.05) for the following intermolt period, main-
ly due to the low number of days between molts for
animals in the 120-min exposure category.
TAGGING TRIALS
Materials and Methods
There are two main events in the commercial
fishery for P eygnus which follow molting by a large
proportion of the population. The first event is in
November-December when maturing 4-5 yr old pale-
shelled animals known locally as "whites" move off-
shore into deeper water, where the breeding stock
is generally situated. During the "whites" fishery,
about 40% of the total catch is taken (Morgan
1980b). The second event is in March-April when
postmolt, dark-shelled, sedentary animals called
"reds" are captured (George 1958; Morgan 1977). As
already mentioned in Brown and Caputi (1983), ac-
count had to be taken of these two periods when
planning tagging trials as the migratory "whites"
could be more mobile and in a physiologically dif-
ferent state than nonmigratory "reds" and hence
their growth could be affected differently by
handling practices (i.e., causing exposure, displace-
ment, and damage). With these possible differences
in mind, three tagging trials were conducted at Two
Rocks, Western Australia (lat. 31°29.7'S, long.
115°3rE), avoiding the period of the full moon, when
catches are at their lowest (Morgan 1974, 1977): 1)
migratory "whites" phase— 26 November to 10
December 1978; 2) nonmigratory "reds" phase— 19
February to 10 March 1979; and 3) migratory
"whites" phase— 16 November to 9 December 1979.
An area consisting of shallow limestone reefs (6-18
m depth) within 6 km of shore and stretching from
Two Rocks Marina to the mouth of Moore River was
fished with standard wire beehive pots without
escape gaps (Bowen 1971; Morgan and Barker 1974).
Pots were baited daily with a variety of fresh fish;
heads of Australian salmon, Arripis trutta; and
bullock hocks.
Tagging Trial A
An experimental area was established, consisting
of a grid on which pots were set and undersize
lobsters could be displaced distances of 0, 230, 460,
910, 1,370, and 1,830 m from a base Hne of ex-
perimental pots where they were captured (Brown
and Caputi 1983). Pots were pulled each morning
during the trial, weather permitting. Undersize (66
to <76 mm) lobsters were tagged with a numbered
western rock lobster tag (Chittleborough 1974b) and
their carapaces measured to the nearest 0.1 mm.
Also recorded was the animal's damage, sex, and the
depth and bottom type where it was caught and
released. Grid areas were generally fished only once
to avoid recapturing previously tagged animals.
Recaptures of tagged animals were made by com-
mercial fishermen who were paid a reward for the
tag and market value for the animal if it had molted
to legal size See Brown and Caputi (1983) for com-
plete details of experimental procedures. Number of
releases for this trial was about 1,500.
Tagging Trial B
Procedure for trial B was the same as trial A ex-
cept that the 1,370 m transect was not set and ex-
posure categories of 0, 30, 60, 120, and 180 min were
also examined. Exposed undersize lobster were
placed in plastic prawn baskets (lug baskets; com-
monly used by fishermen to sort their catch) and ex-
posed to air for the desired period before release at
one of the displacement transects. About 2,300 tag-
ged animals were released.
569
FISHERY BULLETIN; VOL. 83, NO. 4
Tagging Trial C
Similar procedures were followed as for trials A
and B, but only the 1,830 m and a new 3,660 m
transects were set and exposure categories of 0, 15,
30, 60 min were used. Because parasite infection was
observed on some animals (6.3% of releases), its
presence was recorded as it could affect growth. The
infection is a combination of a fungus {Fusarium sp.)
and a bacteria {Vibrio sp.), which causes black lesions
in the exoskeleton, usually in areas that have been
damaged (e.g., tail fans and appendages). Infections
were scored on an ordered scale of 0-6, with 0 in-
dicating no infection. About 2,900 tagged animals
were released.
Results
Figure 1 shows mean size (carapace) increment
related to month of recapture for each of three tag-
ging trials. In tagging trials A and C (November-
December releases), February was the first month
when there was evidence of molting in animals
recaptured (Fig. 1); therefore, subsequent analyses
on size increment only used recaptures from
February onwards. In tagging trial B (February-
March releases). May was the first month when there
was evidence of molting (Fig. 1), so only data from
this month onwards was used for the analyses.
The results of an analysis of variance (ANOVA) on
size increment for each of three tagging trials is
shown in Tkble 1. In this analysis recapture month,
sex, color, displacement, and exposure were treated
as factors while size at release, damage, and level of
parasite infection were treated as covariates. The
analysis enables the significance of these factors and
covariates to be determined after effects of other fac-
tors and covariates are taken into account.
In tagging trial A, after taking the effects of other
factors into account (eg., sex, recapture month, etc.),
the size increment per appendage missing was
smaller by 0.48 mm wdth standard error of 0.04. This
is also evident from Figure 2 which shows the rela-
tionship between mean size increment and numbers
of appendages missing for all recaptures from
February to June 1979. Size increment in tagging
trial C was also smaller by 0.48 mm per appendage
missing with standard error of 0.004 (see Figure 3),
while that for tagging trial B was 0.33 mm smaller
(standard error of 0.07).
From the ANOVA, size increments of displaced
compared with nondisplaced animals were smaller
by 0.32, 0.65, and 0.27 mm for tagging trials A, B,
and C respectively.
Exposure in tagging trial C, after other factors
were taken into account by the ANOVA, resulted in
increments smaller by 0.83, 1.34, and 2.30 mm for
15-, 30-, and 60-min exposure respectively, when com-
pared with the zero exposure category. This can also
be seen from Figure 3 which shows the mean size
increment for animals recaptured after February
1980 related to exposure and number of appendages
missing. While the effect of exposure on growth was
not significant for the February-March 1979 trial B,
size increments were smaller by 0.62 and 0.73 mm
for 30- and 60-min exposures respectively, compared
with unexposed animals.
Mean size increment of males was larger than
females by 0.95, 1.34, and 0.76 mm for the three tag-
ging trials. Although the size at release of all animals
was between 66 and 76 mm, there was still a highly
significant decrease in size increment due to size at
release of 0.25, 0.36, and 0.20 mm for every 1 mm
increase in size at release Difference in color, i.e,
dark-shelled vs. pale-shelled animals, was significant
in tagging trial A with pale-shelled animals having
a greater size increment by 0.65 mm, but this was
not evident in tagging trial C. In tagging trial C, level
of parasite infection of the animals was found to have
had a detrimental effect on growth.
DISCUSSION AND CONCLUSIONS
Exposure
Exposing undersize rock lobsters to the at-
mosphere was detrimental to their growth increment
at the first molt after exposure in both laboratory
and field tagging trials. In the December laboratory
experiment (Group II) the effect of exposure was still
significant at the second molt after exposure "Eg-
ging trial B (February-March 1979) resulted in ex-
posure not having a significant effect on growth
despite the presence of a negative trend between ex-
posure and size increment. This may have been due
to the fact that only 7 of the 110 animals recaptured
in May- June 1979 had been exposed; this is the
period when many of the undersize lobsters would
have undergone their first postexposure molt (Fig.
1). Since there is a closed season from 1 July to 14
November, no recaptures were made until the time
of the second postexposure molt in November-
December 1979, by which time the combined effects
of two molts may have masked the effect of the ex-
posure treatment. However, this was not the case in
tagging trial C (November-December 1979), which
was held at the start of the fishing season, where
the effect of exposure on the first molt which occurs
570
BROWN and CAPUTI: FACTORS AFFECTING GROWTH OF ROCK LOBSTER
20
19
18
17
16
15
M*
13
12
Ell
1—
1 10
UJ
cr
S9
LU
1/1 8
< -I
a. 7
<
<
<
^5
C. NOV- DEC 1979 RELEASES
o e
39 279 407
l_N Dj^
1978
M
M
_D_, J_
M
M
Ij
1979
1980
RECAPTURE MONTH
Figure 1— The mean size (carapace) increment by month of recapture and the sample size involved in calculating it shown next
to the points, for the three tagging trials at Two Rocks.
around February was clearly evident in animals
caught from February 1980 onwards (Fig. 3, Ikble 1).
Damage
Damage to undersize rock lobsters was clearly
shown to have a detrimental effect on growth (Ikble
1), which was directly proportional to the level of
damage (Figs. 2, 3).
Chittleborough (1975) found that growth incre-
ment of i? cygrnts was reduced under laboratory con-
ditions when four or more legs were removed and
repetitive loss of two or more limbs led to precocious
molting with reduced molt increments leading to an
overall reduction in growth. Davis and Dodrill (1980)
and Davis (1981) undertook research on the effect
of injuries Oimb loss) produced by amateur and pro-
fessional fishermen and natural causes (e.g.,
predators, molting accidents, etc) on the growth rate
of P. argus populations in the wild. They found that
571
FISHERY BULLETIN; VOL. 83, NO. 4
NUMBER OF MISSING APPENDAGES
Figure 2.— Two Rocks, November-December 1978. The relationship between the mean size increment and number of appendages
missing for recaptures from February to June 1979, with the sample size and standard error from the mean shown at each point.
Table 1.— The results of the analysis of variance on size increment
for the three tagging trials at Two Rocks with the level of significance
denoted by: NS, *, **, *** meaning not significant, P < 0.05, P <
0.01, and P < 0.001 respectively, and NA means not applicable.
Nov.-Dec.
Feb.-Mar.
Nov.-Dec.
Factor/covariate
1978
1979
1979
No. missing appendages
* * *
* * *
* * *
Displacement
*
*
Exposure
NA
NS
* * *
Recapture month
* * *
* * *
* * *
Sex
* * *
* * *
* * *
Size at release
* * *
* * *
* * *
Color
* *
NA
NS
Parasite infection
NA
NA
• * *
Sample size
687
335
636
the growth rate of injured animals was significant-
ly lower than that of uninjured animals, due to reduc-
tions in molt increment and an increase in intermolt
period. Their research did not demonstrate any pro-
portional relationship between the degree of injury
and the degree of molt increment depression as had
been shown for H. oregonensis and P. crassipes
(Kuris and Mager 1975) and also in this study on P.
cygnus. Davis (1981) stated that growth rate of P.
argus with minor injuries, five or fewer appendages
missing, was almost identical to the growth rate of
more seriously injured animals that were missing up
to nine legs and both antennae.
Displacement
The displacement of undersize rock lobster was
also found to significantly affect size increment in
each of the three tagging trials. This was probably
due to movement of animals from their home range
(Chittleborough 1974c) which could have interrupted
their normal feeding behavior and thus may have
contributed to a decrease in food intake and hence
growth.
Overall Effect
In general the handling of undersize rock lobsters
by fishermen which causes them to be exposed to
the atmosphere, damaged and displaced beyond their
home range, not only affects their survival (Brown
and Caputi 1983) but also affects growth of those
that survive As discussed in Davis (1981), this reduc-
tion in growth may result in:
1) The undersize lobsters staying below the legal size
for a longer period than necessary with some
being subject to natural mortality in this extra
period before entering the fishery.
2) Those animals which do enter the fishery would
do so at a reduced size, hence harvestable yield
would be reduced.
572
BROWN and CAPUTI: FACTORS AFFECTING GROWTH OF ROCK LOBSTER
0 MINUTE = 0 MINUTE EXPOSURE ETC
2 3 U b 6 1
NUMBER OF MISSING APPENDAGES
Figure 3— Two Rocks, November-December 1979. The mean size increment related to exposure categories and number of missing
appendages for animals recaptured from February 1980 onwards. Exposure and missing appendages categories with less than five
individuals have been combined and are plotted at the mean appendage level. The sample sizes are shown next to the points.
3) Size of these animals on reaching maturity would
also be reduced, which would cause a decrease
in fecundity directly proportional to their reduced
size (Morgan 1972). The time they would take to
reach maturity would probably not be affected
since age appears to determine maturity rather
than size (Chittleborough 1974d).
4) Affected animals would remain undersize for
longer, thereby increasing the possibility that they
could undergo multiple capture and handling.
Multiple handling would result in increased mor-
tality and further reduced growth.
These factors, when added to the estimate of
14.6% reduction in recapture rate (most likely due
to mortality) of the returned undersize lobsters dur-
ing the fishing season (Brown and Caputi 1983), con-
stitute a serious loss to the fishery. In addition, any
mortality and reduced growth which may occur as
a result of lifting the animals to the surface and
returning them to the sea would also need to be add-
ed to the above loss. This loss could not be quantified
as both experimentals and controls in the tagging
experiments experienced this.
As mentioned by Brown and Caputi (1983), use of
more effective escape gaps and an education pro-
gram to encourage fishermen to return their under-
size rock lobsters immediately to the sea while their
vessel remained in the immediate vicinity of where
the pot was pulled would help to overcome this
serious source of industry created wastage Both
these approaches are currently being examined wdth
a view to reducing the numbers of undersize lobsters
that are handled and the time they are kept on board
the vessels.
ACKNOWLEDGMENTS
The authors would like to thank J. Prince and J.
Jenke for technical assistance during this work; Ron
Duckrell, the skipper, and the crew of the Flinders
for assistance during the tagging trials; D. A. Han-
cock and N. Hall for critically reading the manu-
script and offering many helpful suggestions; and
573
FISHERY BULLETIN; VOL. 83, NO. 4
M. Isaacs for typing the manuscript. This research
was supported by a grant from the Australian
Department of Primary Industry's Fishing Industry
Research Trust Account.
LITERATURE CITED
AlTKEN, D. E.
1980. Moulting and growth. In J. S. Cobb and B. F. Phillips
(editors), The biology and management of lobsters, Vol. I, p.
91-163. Acad. Press, N.Y.
BowEN, B. K.
1963. Preliminary report on the effectiveness of escape gaps
in crayfish pots. West. Aust. Dep. Fish. Fauna Rep. 2, 9 p.
1971. Management of the western rock lobster (Panulirus
longipes cygnus George). Proa Indo-Pac Fish. Couna
14(II):139-153.
1980. Spiny lobster fishery management. In J. S. Cobb and
B. F. Phillips (editors). The biology and management of
lobsters. Vol. II, p. 243-264. Acad. Press, N.Y.
Brown, R. S., and N. Caputi.
1983. Factors affecting the recapture of undersize western
rock lobster Panulirus cygnus George returned by fishermen
to the sea. Fish. Res. 2:103-128.
Chittleborough, R. G.
1974a. Review of prospects for rearing rock lobsters. Aust.
Fish. 33(4):4-8.
1974b. Development of a tag for the western rock
lobster. CSIRO Div Fish. Oceanogr. Rep. 56, 19 p.
1974c Home range, homing and dominance in juvenile
western rock lobster. Aust. J. Mar. Freshw. Res. 25:227-234.
1974d. Western rock lobster reared to maturity. Aust. J. Mar.
Freshw. Res. 25:221-225.
1975. Environmental factors affecting growth and survival of
juvenile western rock lobsters Panulirus longipes (Milne-
Edwards). Aust. J. Mar. Freshw. Res. 26:177-196.
1976. Growth of juvenile Panuliriis longipes cygnus George
on coastal reefs compared with those reared under optimal
environmental conditions. Aust. J. Mar. Freshw. Res.
27:279-295.
Davis, G. E.
1981. Effects of injuries on spiny lobster, Panulirus argus,
and implications for fishery management. Fish. Bull., U.S.
78:979-984.
Davis, G. E., and J. W. Dodrill.
1980. Marine parks and sanctuaries for spiny lobster fisheries
management. Proc Gulf. Caribb. Fish. Inst. 32:194-207.
George, R. W.
1958. The biology of the Western Australian commercial cray-
fish Panulirus longipes. Ph.D. Thesis, Univ. Western
Australia, Nedlands, 124 p.
Hancock, D. A.
1981. Research for management of the rock lobster fishery
of Western Australia. Proc Gulf. Caribb. Fish. Inst. 33:
207-229.
KURIS, A. M., AND M. Mager.
1975. Effect of limb regeneration on size increase at molt of
the shore crabs Hemigrapsus oregonensis and Pachygrapsus
crassipes. J. Exp. Zool. 193:353-359.
Morgan, G. R.
1972. Fecundity in the western rock lobster, Panulirus
longipes cygnus (George) (Crustacea:Decapoda:Palinuridae).
Aust. J. Mar. Freshw. Res. 23:133-141.
1 974. Aspects of the population dynamics of the western rock
lobster Panulirus cygnus George II. Seasonal changes in the
catchability coefficient. Aust. J. Mar. Freshw. Res. 25:
249-259.
1977. Aspects of the population dynamics of the western rock
lobster and their role in management. Ph.D. Thesis, Univ.
Western Australia, Nedlands, 341 p.
1980a. Population dynamics and management of the western
rock lobster fishery. Mar. Policy 4:52-60.
1980b. Increases in fishing effort in a limited entry fishery
- the western rock lobster fishery 1963-76. J. Cons. Int. Ex-
plor. Mer 39:82-87.
Morgan, G. R., and E. H. Barker.
1974. The western rock lobster fishery 1972-1973. West.
Aust. Dep. Fish. Wildl. Rep. 15, 22 p.
Morgan, G. R., B. F. Phillips, and L. M. Joll.
1982. Stock and recruitment relationships in Panulirus
cygnus, the commercial rock (spiny) lobster of Western
Australia. Fish. Bull, U.S. 80:475-486.
Norton, P.
1981. The amateur fishery for the western rock lobster.
West. Aust. Dep. Fish. Wildl. Rep. 46, 108 p.
574
SEA SCALLOP FISHING IMPACT ON AMERICAN LOBSTERS IN
THE GULF OF ST LAWRENCE
G. S. Jamieson' and A. Campbell^
ABSTRACT
Damage to American lobsters, Homarus americanus, in Egmont Bay and off Miminegash, Price Edward
Island, is minimal from the drags of the seasonal sea scallop, Placopecten magellaniciis, fishery. During
May 1981, when commercial sea scallop fishing was occurring, American lobster abundance was low in
areas of profitable scallop exploitation. Sea bed substrate in these areas was generally smooth and most
lobsters were able to avoid the gear. In the areas with and without commercial scallop fishing, 1.3% and
11.7% of observed lobsters, respectively, were injured or retained by the drag. Lobster abundance in the
areas commercially exploited for scallops in May and June was significantly greater in July than in May,
but whether this was a result of a natural seasonal movement of lobsters or the cessation of scallop fishing
is unclear.
Sea scallop, Placopecten magellanicus, and American
lobster, Homarus americanus, populations are fully
exploited in Northumberland Strait, Gulf of St.
Lawrence (Wilder 1947, 1965; Robinson 1979;
Jamieson et al. 1981c; Campbell and Mohn 1983). In-
dividual fishermen frequently fish both species, com-
monly in the same general area, although the
fisheries are separated temporally (Jamieson et al.
1981c; Conan and Maynard 1983). Recently, localized
low abundance of these important, commercial
species has heightened long-held convictions by
fishermen of the negative impact of sea scallop
fishing on American lobster stocks. Fishermen's con-
cern became acute for the Egmont Bay area during
1980, coincident with the discovery and exploitation
of new nearshore scallop concentrations near West
Point, Prince Edward Island (Fig. 1). Decreased
scallop recruitment in recent years (Jamieson et al.
1981b, c) has resulted in a scarcity of scallops in
traditional fishing areas, causing increased ex-
ploration for commercially exploitable scallop
concentrations.
The magnitude of scallop gear-lobster interaction
is dependent on the spatial and seasonal distribu-
tions of scallops and lobsters and the impact of
scallop gear on commercial lobster abundance where
the distributions of both species overlap. Scallops are
widespread in Northumberland Strait (Caddy et al.
1977), but commercial concentrations are found only
'Department of Fisheries and Oceans, Fisheries Research
Branch, Halifax, Nova Scotia; present address: Pacific Biological
Station, Nanaimo, British Columbia V9R 5K6, Canada.
^Department of Fisheries and Oceans, Atlantic Biological Sta-
tion, St. Andrews, New Brunswick, EOG 2X0, Canada.
in limited areas. The precise locations of these areas
are undocumented, and since they vary with time,
they cannot be predicted with any accuracy. However,
commercial log data has shown the broad distribu-
tion of scallop concentrations in Northumberland
Strait during 1979-80 (Jamieson et al. 1981b, c).
The seasonal abundance and distribution of
commercial-sized lobsters is largely unknown, but
their general distribution overlaps that of scallops
(Stasko et al. 1977; Conan and Maynard 1983). There
have been few field studies conducted on lobsters in
this area: Ibmplemann (1933, 1934, 1935, 1936)
reported on lobsters and the fishery in Northumber-
land Strait; Wilder (1963) and Wilder and Murray
(1956) reported on movements and growth of tag-
ged lobsters liberated in Egmont Bay.
Scallop and Irish moss, Chondrus crispus, drags
can damage lobsters, although lobsters exposed on
open ground tended to avoid moving drags. Most
gear-induced damage has resulted from lobsters in
burrows being hit or crushed by rocks disturbed by
the drag (Scarratt 1973, 1975; Pringle and Jones
1980).
Investigations reported here document 1) the
scallop drag/lobster interactions off Miminegash,
Prince Edward Island, during August 1978 and in
Egmont Bay during May and July 1981; and 2) the
relative abundance and movement of lobsters trap-
ped and tagged in Egmont Bay prior to (June-July
1981) and during the lobster fishing season (10
August-10 October 1981). Lobster abundance may
change relatively rapidly because of their potential
high mobility. Therefore it is important to charac-
terize lobster microdistribution and assess the con-
Manuscript accepted January 1985.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
575-81^
FISHERY BULLETIN: VOL. 83, NO. 4
Sand E
Small Rocks ^M
Large Rocks
46°
35'
46°
30*
46
25*
FIGURE 1.— General substrate type as observed by divers in the areas surveyed in Egmont Bay, Northumberland Strait, Gulf of St. Lawrenca
Locations of stations (heavy lines) sampled for lobsters in Egmont Bay, Northumberland Strait: 1 = recently heavily fished scallop ground,
2 = recently lightly fished scallop ground, 3 = no recent scallop fishing (large rocks), 4 = no scallop fishing (deeper water).
sequences of scallop fishing on the degree of species
overlap. Scallop fishing may directly damage
lobsters, or because of the disturbance of the sea bed
by the drags, may cause lobsters to avoid or be at-
tracted to the overall area.
METHODS
Scallop Gear-Lobster Interactions
1978 Study
The interaction between three types of scallop gear
and lobsters was observed by divers between 15 and
30 August 1978. The study area was in 14 m of water
about 1 km from shore Oong. 46°52'30"W, lat.
64°14'00"N), and consisted of a sandy bottom with
occasional small rocks. The gear used was a two-
gang, toothed Gulf rock drag (60 cm buckets) (Fig.
2); a two-gang Digby rock drag (76 cm buckets, no
teeth) (MacPhail 1954); and a 152 cm Gulf sweep
chain drag. A Gulf sweep chain drag is a smaller,
lighter revision of an offshore scallop drag (Bourne
1964). A hood of 38 mm stretch mesh was placed over
the drags extending to a height of 81 m above the
sea bottom, and one of the buckets (half the chain
sweep drag) had a similar mesh hood on the outside
of the back of the drag (back cover). The bucket, or
portion of the drag, without a back cover had a mesh
liner. Two divers hung onto each drag during tows,
576
JAMIESON and CAMPBELL: SCALLOP FISHING IMPACT ON LOBSTERS
A. Dors a\ View
274 cm
A~
91 cm
cr
81 cm 3
n n n n n nnnr
Unlined Drag
60 cm
150
cm
V
Tow Bar ^^
4.
130
cm
r-i n ri p ri m
£-"
Teeth
L jned Drag
5 I cm
.y... .
Dumping
Ring
Spruce Log
J
,Drag Hood
Rubber Mat
B. Lateral View of Bucket 2
Rubber
M of
Spruce ^S^
Log
81 cm
\
25 cm
Figure 2.— Schematic drawings of a four-gang Gulf rocl^ drag: (A) hood and Hner arrangements used with buckets 2 and 3 in
1978 (buckets 1 and 4 were removed). In 1981, 4 unmodified buckets were used. (B) Lateral view of bucket 2 used in 1978.
577
FISHERY BULLETIN: VOL. 83, NO. 4
noting lobster behavior and the physical effect of the
drag on lobsters; carapace lengths (CL, back of eye
socket to posterior carapace margin) of fished
lobsters were measured. Tovv^ velocities, established
by engine rpm, were similar to commercial opera-
tions and tow duration was 5 min.
1981 Study
Dragging was conducted during 14-22 May and
27-31 July 1981. Four general areas (Fig. 3) were
surveyed in both periods. Scallops and lobsters were
known by fishermen to exist in areas A and A' but
scallop fishing had not occurred for several years;
five research tows were conducted in May and three
tows in July. Areas B and C were reported by
fishermen to be prime lobster ground where scallop
fishing had occurred recently or was in progress dur-
ing the study; 30 research tows were conducted in
May and 25 tows in July. Tbw locations were ran-
domized within an area and the number per area was
arbitrarily assigned according to the apparent
distribution of commercial effort in the scallop
fishery. Bottom water temperatures averaged 8.8°
and 18.4°C in May and July, respectively. A four-
gang Gulf rock drag (Fig. 2) with 51 cm buckets was
used throughout the study. Scallop rings had 69-75
mm and 80-84 mm inside and outside diameters,
respectively. Lead ropes 30 m long were attached to
each end of the 2.36 m club stick at the back of the
drag to define an area behind the drag to be surveyed
by divers. Before the drag was dropped, the lines
were let out while the vessel was steaming or drift-
ing to establish an unfished control area for survey
64° 20'
64 10
\ \ \
1
1 .'IVi.
.:,._JC^r^«T ■*!=
2^2Easn3
1^
ti yP
^^•^■<»ii<. A^^lS^i \ ..J.
\ \ -'' a1
\i / r %s-
o\
Egmont
B
ay
^^ lA-
V X!= ^
3/
"~~ N^
h-
/^
TTm .
■*
'~^
~'r\ /4
N
-«?
/ 2 \ /
N
">>
/ \ >
\
\
/
/A , /
L
0 y < tRock Pt.
1
-— I '. > N
Z' """"^^ r*
/ 1 < > /
/^ 57\ V
A f~ja a \ \-
-' '' ^; v.
1 35/ 62 'yi 8 j V-
1 f^^ \
V^ C ^<v/ \ji
1 — •
\ 31 46 71 / fV Abrams
1 i
.'-vj
\^^ ^/ \ o Village
\ 5i5 45^ V.
'N'.^ ' /
^*-^ 1 a^ k 0 1 2 km
,-N -V. (
/
\ - \
/
1 /^' :(^
1 \
)
/■ " \
\ tRed Hd.
y
( \
^ 1 ~
1
\. \
'""^
^ f
\ \
' ^"''■''^''^^i.i^^^
/
\ N
^^ ■' ' -^.iiii.ii^
( ~^
\ i
\
\
1 '^^^'^^^iiii.
\
\ V
N
s.
JK
X
\ 1
\
s
^--
\
\
1
1 N
46
3 5'
4 6°
30'
4 6°
2 5'
Figure 3.— Number of scallops fished/tow (average length = 97.5 m) by the gear in May in Egmont Bay, Northumberland
Strait, Gulf of St. Lawrence Identified areas are where both scallops and lobsters exist in commercial densities: A and
A' were areas where no scallop fishing had occurred for several years (= unfished control); B and C were areas where
scallop fishing had recently occurred or was in progress during the study. Substrate type is shown in Figure 1.
578
JAMIESON and CAMPBELL: SCALLOP FISHING IMPACT ON LOBSTERS
by the divers when the drag was finally lowered.
When the drag was on the bottom, divers swam
along the outside edge of each lead line with a 2 m
rod, noting all scallops and lobsters encountered in
the 2 m wide unfished "path" (120 m^). The divers
then positioned themselves on the drag and noted
the number of lobsters in the drag path during the
tow, which covered on average 975 m (SD = 221).
When the tow terminated, the divers searched the
drag path between the lead lines (70.8 m-) and col-
lected the scallops and lobsters encountered. Scallop
height (edge of hinge to distal edge of the valves)
and lobster carapace lengths were measured to the
nearest millimeter with a measuring board and ver-
nier calipers, respectively. Location (loran C
readings), bottom type (Fig. 1), water temperature,
and marine plant presence were noted. Tbw distance
and speed were calculated from loran C readings
(Jamieson 1982) and averaged 4.6 kn (SD = 1.9) in
May and 4.3 kn (SD = 1.7) in July. Average tow dura-
tion was 6.9 min.
Lobster Abundance and Distribution
Four study areas (Ikble 1; Fig. 1) were located by
loran C and were selected after bottom types were
characterized from scuba diving observations. The
areas were 1) recently heavily fished scallop ground,
2) recently lightly fished scallop ground, 3) ground
with large rocks with no recent scallop fishing, and
4) typical lobster ground in waters deeper than areas
1-3 with no scallop fishing. Fifty, three bow, single
kitchen and parlor design lobster traps with 121 mm
diameter entrance ring and 31-34 mm lath spaces
were set in each area. Each trap was baited with
salted gaspereau (or alewife), Alosa pseudoharengiis,
and/or Atlantic herring, Clupea harengus harengus.
The traps were set in groups, two traps per buoy,
within a 1 km radius of the center of the area (Tkble
1). The mean interval between trap hauls from 22
June to 30 July was 3 d (1-7 d range). Each trap was
reset as close as possible to the original site of each
trap set.
The sex and carapace length (CL in mm) of each
trapped lobster was recorded. Once a week, the ter-
minal quarter of a pleopod endopodite was removed
with scissors from each of 70-140 lobsters of various
size groups, and placed in a vial containing seawater.
The pleopod method described by Aiken (1973) was
used to determine the molt stage of each lobster.
The bottom and surface water temperatures were
recorded for each area and time fished. To observe
lobster movement and growth, a total of 2,002 lob-
sters (ca. 500 lobsters/area) were measured and tag-
ged (Tkble 1) with a sphyrion tag (Scarratt and Elson
1965) and returned to the water within 10 min and
0.5 km of the capture site During the 10 August-10
October fishing season, lobster samples were obtain-
ed at-sea from commercial lobster fishing boats at
a number of locations within and near areas 1-4.
One-way analysis of variance was used to compare
the mean number of lobsters per trap haul in each
area during a 1-wk sampling period and to compare
the mean distance moved for lobsters from the dif-
ferent study areas.
From tagged lobsters recaught during the study,
movement and direction statistics of tagged lobsters
were analyzed by methods Jones (1959) and Saila
Table 1.— Summary of Egmont Bay lobster tagging experiment, 22 June-30 July 1981.
Area 1
Area 2
Area 3
Area 4
Heavily fished
Lightly fished
Scallop ground
Lobster
Details
scallop ground
scallop ground
with rocks'
ground'
Location
Latitude (°N)
46°28'
46°27'
46°28'
46°23'
Longitude (°W)
64°10'
64013'
64° 12'
64°15'
Bottom type
mud, small rock
mud, small rock
mud, rocks
mud, rocks
(<10 cm)
(<10 cm)
(>10 cm)
(>10 cm)
Mean depth (m)
11
13
11
18
No. of traps
50
50
50
50
Trap soak-over
(days) (range)
2-5
1-7
2-5
1-5
No. of trap hauls
489
568
500
591
No. of lobsters
caught
2,507
1,967
2,568
2,330
Total tags released
500
501
500
501
Total tags returned^
182
162
234
162
% of total tags
released in area^
36.4
32.3
46.8
32.3
'No scallop fishing.
^Number of tags returned up to 30 October 1981 including tags witfiout recapture locations.
579
FISHERY BULLETIN: VOL. 83, NO. 4
and Flowers (1968) have reported, using a computer
program by Campbell et al. (1983).
RESULTS
Scallop Gear-Lobster Interactions
1978 Study
No scallops were present but lobsters were numer-
ous and were observed by divers to be frequently
foraging in the open. Average carapace length of 22
diver-collected lobsters was 61.3 mm (SD = 26.8).
While the microdistribution of substrate type was
patchy, tows were of sufficient duration to cover all
substrate types. Under the assumption of an average
uniform lobster density during tows, lobster catches
made by the Gulf sweep-chain drag over sand and
rock-sand were highest. Average catches in the lined
and unlined portion of the drag were 0.53 and 0.07
lobsters/m of drag width fished per min (m^^min^^),
respectively (Ikble 2).
No lobsters were retained by the unlined rock
drags, but since they were retained in the back cover
of the drag, lobsters were entering the drag and
passing through the rings. These lobsters did not
show any external evidence of damage. The hoods
Table 2.— Average number of lobsters caught
m~'min'' of drag width In the hoods and linings of the
scallop gear used in 1978. Each drag type was hauled
over both sand and sand-rock substrates off
Miminegash, Prince Edward Island. L = lined gear;
UL = unlined gear; H = hood; B = back cover.
Drag type
No.
tows
Lobster catch
UL
H
B
Gulf sweep chain 5 0.53 0.07 0.15 0.31
Gulf rock drag 5 0.11 0.00 0.06 0.11
Digby rock drag 6 0.02 0.00 0.07 0.04
of all three drag types contained lobsters, indicating
that lobsters can escape by swimming over the ad-
vancing drag.
1981 Study
RELATIVE SCALLOP AND LOBSTER ABUN-
DANCE.—Catch results and sightings per tow
(Jamieson et al. 1981a) indicated that for each study
area, considerable variation existed in abundance of
both scallops (Fig. 3) and lobsters (Fig. 4). Substrate
type was variable over the distance of a single tow,
and this appeared to be a major factor influencing
relative scallop and lobster abundance.
Scallop and lobster densities in the two areas (B
and C) fished for scallops varied significantly on
some dates (Tkble 3) from those densities in the non-
fished areas (A and A^); fished grounds had a greater
number of scallops, but fewer lobsters, than did the
nonfished ground. Between the two fished areas, the
only significant (P < 0.05) difference was in the
scallop drag catch in May, but study area C off Red
Head generally yielded more of both species than
did study area B off West Point (Figs. 3, 4).
There were no significant differences (P > 0.05)
in the densities of either scallop or lobster in the non-
fished area between the two sampling periods.
Lobster sightings per tow in both fished areas were
significantly greater (P < 0.05) in July than in May,
but the number of sightings averaged less than in
the unfished area. Although not always significant,
the general seasonal trend of lobster abundance, as
indicated by the control sampling procedures, in-
creased between May and July in all areas. Scallop
catch decreased significantly (P < 0.01) in the ground
off Red Head between May and July. On fished
ground, average scallop density decreased whereas
scallop density on the nonfished ground increased
during this time period.
Table 3. — Average scallop and lobster catch in a 4-gang Gulf rock drag in 1981, and the abundance per 1,000
m^ In each study area before the scallop drag was towed (control) and in the drag path behind the drag. Values
with asterisks are significantly different from the corresponding value in the nonfished scallop location. * =
P < 0.05; ** = P < 0.01; n = number of tows.
Month
Control density
Drag
Drag path
Location
n
Scallop
n
Lobster
n
No.
scallop
caught
n
No.
lobsters
observed
n
Scallop
n
Lobster
Nonfished
area
May
July
4
2
6.25
12.50
4
2
2.08
16.67
5
3
0.87
0.15
4
3
3.03
4.62
2
3
0.0
4.71
2
3
0.00
4.71
West Point
May
July
4
3
56.23
22.21
4
3
0.00
2.78*
11
7
7.59*
10.10
11
7
0.48
1.48*
8
5
24.70*
127.08
8
5
1.76
5.65
Red Head
May
July
9
9
99.03**
58.31
9
9
0.93
5.55
19
18
16.38**
8.34**
19
18
0.87
1.98*
12
10
68.25**
52.24
12
10
1.18
1.41
580
JAMIESON and CAMPBELL: SCALLOP FISHING IMPACT ON LOBSTERS
64° 20'
6 4 10"
Figure 4— Number of lobsters observed by divers in May during each tow in Egmont Bay, Northumberland Strait, Gulf
of St. Lawrence Substrate type is shown in Figure L Area designations are explained in Figure 3.
SCALLOP GEAR: LOBSTER INTERACTION.-
No relation was found between the two sample
periods and the number of lobsters injured or re-
tained during a tow (Ikble 4). The weighted percent-
age of lobsters injured or retained was 1L7 and L3,
for the nonfished and combined fished areas, respec-
tively. Injured lobsters were not found in the drag
path, although occasionally lobsters were observed
to retreat into burrows in front of a moving drag.
Whether they subsequently became damaged or
trapped in their burrows is unknown, but the absence
of damaged lobsters in the drag path suggests that
the frequency of lobster damage is low on commer-
cial scallop ground especially where there is a
general lack of large rocks and boulders. However,
14 of the 30 locations surveyed had occasional large
rocks.
Most lobsters encountered were too small (mean
CL = 72 mm) (Ikble 5) to be retained by the scallop
gear unless the steel rings making the drag were
partially blocked by debris. All lobsters <92 mm CL
can pass through a 70 mm inside diameter scallop
ring (Stasko 1975). Several lobsters were seen by the
divers entering the drag and passing through the
rings apparently unscathed. In 63 tows, 1 1 lobsters
were affected directly by the scallop gear: four were
retained by the drag (the ring openings were block-
Table 4.— Frequency by month and location of lobster reduction
and/or injury during dragging.
Nonfished
areas
Fished
areas
Details
Month
West Point
Red Head
No. lobsters
May
28
10
35
observed
July
32
24
82
No. lobsters
May
3
1
0
injured/retained
July
4
1
0
% injured/
May
11
10
0
retained
July
13
4
0
581
FISHERY BULLETIN: VOL. 83, NO. 4
Table 5. — Summary of lobster catches during closed fishing season (June-July 1981) and during the fishing season
(August-October 1981) in Egmont Bay. Shorts = prerecruits <63.5 mm CL; legals = recruits >63.5 mm CL.
No. of
No. of
Prerecruits
Recruits
No. per
% females
No. per
% females
Week
Time
lobsters
trap
% total
trap
of total
trap
of total
Mean
no.
period
Area
sampled
hauls
lobsters
haul
shorts
haul
legals
CL (mm)
1
22-26 June
2
2
104
0
0
0
0.02
0
81.0
4
2
96
50.0
0.01
0
0.01
100.0
72.0
2
29 June-
1
3
100
33.3
0.01
100.0
0.02
100.0
71.0
3 July
2
17
102
29.4
0.05
80.0
0.12
33.3
68.8
3
2
100
50.0
0.01
100.0
0.01
100.0
66.0
4
11
100
45.5
0.05
40.0
0.06
50.0
67.3
3
6-10 July
1
141
98
9.2
0.13
53.9
1.31
20.3
71.4
2
114
102
12.3
0.14
35.7
0.98
35.4
71.5
3
99
100
11.1
0.11
72.7
0.88
21.6
70.9
4
35
100
25.0
0.09
22.2
0.27
30.8
72.6
4
13-17 July
1
503
94
17.7
0.95
42.7
4.40
31.9
71.0
2
542
104
10.4
0.59
54.1
5.06
33.8
72.1
3
550
100
12.2
0.67
41.8
4.83
33.3
71.3
4
395
100
9.4
0.38
45.9
3.65
31.6
72.6
5
20-24 July
1
794
99
13.7
1.10
55.0
6.92
33.9
69.9
2
708
104
9.0
0.62
51.6
6.19
36.3
71.6
3
840
100
10.7
0.90
47.8
7.50
36.6
70.4
4
792
98
6.3
0.51
58.0
7.57
33.8
72.4
6
27-30 July
1
1,066
98
15.7
1.70
44.3
9.17
29.1
70.3
2
584
52
9.3
1.04
57.4
10.19
31.0
71.6
3
1,077
100
9.2
0.99
44.4
9.78
29.6
70.9
4
1,095
97
6.2
0.70
39.7
10.59
32.0
73.3
8
10-14 Aug.
D
1,582
488
24.5
0.79
44.9
2.40
33.1
71.9
9
17-21 Aug.
V)
155
125
47.7
0.59
46.2
0.65
(')
{')
10
24-28 Aug.
n
501
240
44.7
0.93
48.5
1.13
31.8
73.2
11
13 Aug.-
4 Sept.
V)
458
245
42.5
0.80
42.6
1.07
34.4
73.0
13
14-18 Sept.
n
496
237
51.6
1.08
50.8
0,99
44.2
71.5
15
28 Sept.-
2 Oct.
V)
129
74
7.7
1.18
53.4
0.57
n
(')
lAII fishing areas du
ing fishing
season.
2Size
and sex not recorded
ed with Laminaria longicruris), four passed under
the drag and were possibly injured, and three were
struck during the course of one tow (in May)
resulting in claw loss or a cracked carapace In the
latter instance, strong currents impeded the escape
of lobsters.
Scallop size frequencies were similar in May and
July in each of the two commercially fished areas
and all scallop age classes were exploited about
equally.
Lobster Abundance and Distribution
Abundance
The number of lobsters caught per unit of effort
(trap haul; CPUE) increased during the experimen-
tal fishing period in all areas (Ikble 5). During the
commercial fishing period, CPUE of prerecruits in-
creased but CPUE of legal-sized lobsters decreased
presumably as a result of fishing mortality. Number
of lobsters per trap haul was not significantly dif-
ferent between areas observed during the ex-
perimental period (Ikble 5). The use of CPUE is
unreliable in the quantitative estimation of lobster
abundance as many factors affect trapability, in-
cluding water temperature, lobster behavior, molting,
relative trap and lobster densities, and bait attrac-
tiveness (Elner 1980).
Lobster Movement
Of the 740 tagged lobsters recaptured (37%), 658
had recapture location data (Ikbles 1, 6). In areas
1, 2, and 3, the majority (65-78%) of tagged lobsters
were recaptured within 10 km of release, but in area
4, 50% were caught 11-18.5 km from release (Ikble
6). The mean distance moved was not significantly
different for tagged lobsters released in areas 1, 2,
or 3, but lobsters from area 4 moved a significantly
(P < 0.01) greater mean distance than those of the
other three areas.
Direction statistics (according to Saila and Flowers
1968) summarize the nature of lobster movement
582
JAMIESON and CAMPBELL: SCALLOP FISHING IMPACT ON LOBSTERS
Table 6. — Summary statistics of distance travelled and direction moved by tagged lobsters
released at four areas in Egmont Bay during June-July 1981, and recaptured up to 30 October
1981. (Direction statistics calculated according to Jones [1959] and Saila and Flowers [1968]
are 0 = mean vector angle from true north; V and V = directed movement along north-
south and east-west plane, respectively, negative values of V and V indicate net southerly
and westerly movement, respectively; R and Z = Rayleigh test statistics for randomness or
uniform distribution of points about a circle; * = significant at P < 0.01 indicates a non-uniform
distribution.) SD = Standard deviation.
Release
area
1
2
3
4
Heavily fished
Lightly fished
Scallop ground
Lobster
Details
scallop ground
scallop ground
with rocks!
ground'
% of total recaptures
moved 0-10 km
65.2
70.3
78.2
35.3
% of total recaptures
moved 11-18.5 km
28.1
16.2
19.8
49.7
% of total recaptures
moved >18.5 km
6.7
13.5
2.0
15.0
Total recaptures
164
148
207
139
Mean distance moved,
9.2
10.1
8.3
212.9
km (±1 SD)
(0.5)
(0.6)
(0.4)
(0.6)
Maximum distance
moved, km
25.0
45.0
38.9
49.7
0
247.3
289.3
310.5
344.4
V (km/d)
-0.055
0.026
0.062
0.213
V (km/d)
-0.132
-0.075
-0.073
-0.059
R
74.9
26.3
64.9
63.5
Z
34.2*
4.7*
20.4*
29.0*
'Ligtit or no scallop fishing.
2Value for mean distance travelled significantly different (P < 0.01 ); other values not significantly different
(P > 0.05).
(Tkble 6). The Rayleigh test statistic, Z, indicated a
non-uniform distribution of tag returns (P < 0.01)
for each area of release Results of the Rayleigh test
should be treated with caution (Batschalet 1965)
since there is some evidence of bimodality. In
general, the returns exhibited three main directions
of movement for lobsters: south-west for area 1,
north-west for areas 2 and 3, and north for area 4
(Tkble 6). V and V, the north-south and east-west
coefficients of directed movement, measure the mean
daily travel of the group. Lobsters from areas 1-3
showed little dispersion in a north-south direction
in contrast to lobsters from area 4, which moved the
greatest in a northward direction (0.213 km/d).
Lobsters from all areas generally moved west, but
lobsters from Area 1, the heavily fished scallop
ground, tended to disperse furthest west per day
(0.132 km/d). Dispersion to the west is perhaps large-
ly the result of the relative proximity of the release
areas to the western shore of Prince Edward Island,
which restricted lobster movement to the east.
Lobster Growth
Determinations of molt stage from pleopod ex-
aminations indicated that lobsters may have molted
as early as 6-12 July (Tkble 7). Trapability of lobsters
is affected by molt stage, with late molt stages (eg.,
D^q; Aiken 1973) being difficult to trap. The high
percentage of Dg to D^ animals (stages just before
molting) in mid-August indicated that considerable
molting was imminent, and this probably affected
CPUE at this time Many tagged lobsters (47.8%,
N = 46) recaptured during the period 24 August-26
September had molted.
DISCUSSION
The results of this study are probably area and
Table 7. — Percentage of pleopod stages of lobsters sampled from
Egmont Bay, July-September 1981. Pleopod stages 3.0-3.5 and
4.0-5.5 predict lobsters molting within 1.9-4.0 wk and 0.3-2.4 wk,
respectively, at 15°-19°C (Aiken 1973). Prediction of molting time
for pleopod stage 1.0-2.5 is unreliable but usually exceeds 4.0-10.3
wk.
% of lobsters
Pleopod stage
Period
1.0-2.5 3.0-3.5 4.0-5.5
Temper-
No. of ature
lobsters (°C)
6-10 July
97.1
1.5
1.4
69
15.5
13-17 July
98.2
0.9
0.9
113
16.0
20-24 July
96.5
3.5
0.0
142
16.5
27-30 July
89.9
6.6
3.5
117
19.0
10-14 Aug.
76.3
21.1
2.6
76
18.1
31 Aug.-4 Sept.
91.1
5.9
3.0
101
17.5
583
FISHERY BULLETIN: VOL. 83. NO. 4
time specific Nevertheless the extent of sea scallop
gear damage to American lobsters in Egmont Bay
was measured, and this permits estimation of the
damage to lobsters on similar substrate types in
other locations. In the nonfished area there was no
significant difference in the lobster abundance
between the May and July observations, whereas
there were significant differences in relative seasonal
lobster abundance in the fished areas. In western
Northumberland Strait at the time of this study,
scallop fishing occurred primarily between late April
and late June, with a minor amount of fishing
between mid-October and winter freeze-up
(Jamieson et al. 1981c). There was limited scallop
fishing during July. If lobsters were displaced by
scallop dragging during May and June, normal
seasonal lobster densities could be reestablished by
late July. It is unclear whether the greater density
of lobsters in the fished areas in July was due to nor-
mal seasonal migration onto these grounds or to the
absence of scallop fishing. Data from tagged lobsters
suggested that some immigration may have occurred
from the deeper water areas of the Strait, but it also
appeared that overall abundance on the scallop
grounds may have been reduced by scallop dragging
activity. Predators have been reported to be at-
tracted to the disturbed substrate in a drag's path
(Caddy 1973), but how this relates to lobsters is
unclear.
The trapability of lobsters is a function of many
variables (Elner 1980), making the quantification of
lobster abundance difficult in the four trap study
areas. There was a lower percentage of short lobsters
and a larger mean carapace length in Area 4 than
in the other areas (Tkble 5). When large lobsters were
trapped there were generally fewer small lobsters
in the traps (Tkble 5), but this may have resulted from
agonistic behavior (Cobb and Tkmm 1975) rather
than relative density. Water temperature increases
may also have affected behavior and possibly had
major modifying effects on lobster growth and/or
movement. McLeese and Wilder (1958) documented
an increase in lobster rate of movement with in-
creasing temperature, but what effect this had on
the average direction of movement during the study
period is unclear. The mean movement rate of
lobsters in our study (Tkble 7) was similar to that
reported by Saila and Flowers (1968) for mature
lobsters off Rhode Island. Saila and Flowers (1968)
showed that the coefficients of directed movement,
V and V, are sensitive to changes in movement pat-
terns at various life history stages, and hence are
a possible function of lobster maturity level and the
sex ratio used in their calculation. These potential
influences were not considered here because of
limited duration of the study and the relative close
proximity of release and recapture areas which were
probably not optimal to permit extensive data
analysis.
There probably was a directed movement of tag-
ged lobsters from area 4 (deeper water) into Egmont
Bay. This may have contributed to the increased
CPUE during July-October. Tfempleman (1936) found
there was some movement during the summer with
lobsters congregating in the relatively shallow in-
shore water areas of Northumberland Strait and that
some lobsters moved offshore in the fall. The
disproportionate sex ratio of legal-sized lobsters
observed in the present study suggested a
geographic distributional difference between the
sexes of lobsters after maturity during July-August.
Lobster trapability, and hence estimated abun-
dance, can be influenced by molt stage. Many legal-
sized lobsters appeared to have molted between
August and September, and while the data are in-
sufficient to support the fact that a molt may have
occurred prior to or during the experimental fishing
period (late June-July), other investigations have
presented evidence in the literature that lobsters in
this area do molt in late spring (Tfempleman 1934,
1936; Wilder 1963). If, in fact, two molts did occur
during the study period, this along with increased
water temperature increasing lobster movement
(McLeese and Wilder 1958) could partially explain
the rapid increase in CPUE during July. However,
no soft-shelled lobsters were observed during July,
while soft-shelled lobsters were quite frequently en-
countered in fishermen's traps during the August-
September fishing season.
The seasonal nature of the fisheries minimizes the
impact of scallop gear on lobsters because lobsters
are in low abundance on scallop ground at the time
of greatest scallop fishing activity. Commercial con-
centrations of scallops and lobsters also appear to
be largely separated spatially (Figs. 2, 3). What then
is the likely economic impact in Egmont Bay of
scallop fishing on lobsters, and how does this com-
pare to the value of the exploited scallop resource?
No reported commercial scallop fishing was reported
in 1980 off Red Head, but vessel logs recorded that
1,509.4 kg of adductor muscle meat were taken near
West Point (scallop log areas 77 and 78 combined,
Jamieson et al. 1981c). Average CPUE was about 2.4
kg/h • m "\ indicating that 629 h • m of effort was ex-
pended. In our study, a total of 8.2 h-m of research
effort was expended in May on the fished grounds
and 22 lobsters were observed behind the drag in
the drag path. Drag velocities over the bottom in
584
JAMIESON and CAMPBELL: SCALLOP FISHING IMPACT ON LOBSTERS
both commercial fishing operations and in our study
are assumed to be similar. If 2.6% of the lobsters
observed are retained or injured, with 50% of these
lobsters killed, then the total number of lobsters
estimated to be destroyed by commercial scallop
fishing in 1980 was 22 lobsters. If each lobster weigh-
ed 0.5 kg and was valued at $6.60 kg"\ then the
loss would be about $73. In comparison, at $8.27
kg"^ of scallop meat in May, 1980 (Jamieson et al.
1981c), the scallop landings from these two fished
areas had an estimated value of $12,483.
If lobster abundance was as high as that in the un-
fished area, i.a, 3.03 lobsters/1000 m^, then 139
lobsters, with a value of $460, would have been
destroyed. In both instances, this loss is negligible
in comparison to the values of the lobster and scallop
fisheries. These conclusions are in agreement with
the observations of Scarratt (1973) and Pringle and
Sharp (1980) in their assessments of the impact of
Irish moss raking on lobster populations.
ACKNOWLEDGMENTS
We thank M. Beattie, D. Duggan, S. Hamet, M.
Lundy, D. R. Maynard, and N. Witherspoon for
diving assistance; Captains E. Wedge and M. Ellis
of chartered vessels for their help and advice; D. J.
Scarratt and J. D. Pringle for their support and
manuscript review, and in particular, R. Chandler,
M. Etter, D. R. Maynard, and J. D. Pringle for coor-
dinating field studies and/or assistance in data
analyses.
LITERATURE CITED
Aiken, D. E.
1973. Proecdysis, setal development, and molt prediction in
the American lobster {Homarus americanus). J. Fish. Res.
Board Can. 30:1337-1344.
Batschalet, E.
1965. Statistical methods for analysis of problems in arrived
orientations and certain biological rhythms. Am. Inst. Biol.
Sci., 54 p.
Bourne, N.
1964. Scallops and the offshore fishery of the Maritimes.
Fish. Res. Board Can. Bull. 145, 60 p.
Caddy, J. Y.
1973. Underwater observations on tracks of dredges and
trawls and some effects of dredging on a scallop ground. J.
Fish. Res. Board Can. 30:173-180.
Caddy, J. F., T. Amaratunga, M. J. Dadswell, T. Edelstein, L.
E. LiNKLETTER, B. R. McMULLIN, A. B. StASKO, AND W. H.
van DePoll.
1977. 1975 Northumberland Stait project, Part I. Benthic
fauna, flora, demersal fish and sedimentary data. Can. Fish.
Mar. Serv., MS Rep. 1431, 46 p.
Campbell, A., S. E. Bellis, G. E. Fawkes, and C. Hastey.
1983. Computer programs for analysis of lobster (Homarus
americanus) movements from tag-recapture data. Can. Ms.
Rep. Fish. Aquat. Sci. 1705, 22 p.
Campbell, A., and R. K. Mohn.
1983. Definition of American lobster stocks for the Canadian
Maritimes by analysis of fishery-landing trends. TVans. Am.
Fish. Soc 112:744-759.
Cobb, J. S., and G. R. Tamm.
1975. Dominance status and molt order in lobsters (Homarus
americanus). Mar. Behav. Physiol. 3:119-124.
Conan, G. Y., and D. R. Maynard.
1983. Aerial survey of spatial distribution of effort in lobster
fishery of southern Gulf of St. Lawrence ICES Shellfish
Committee CM 1983/K 13, 14 p.
Elner, R. W.
1980. Lobster gear selectivity-A Canadian overview. In V. C.
Anthony and J. F. Caddy (editors). Proceedings of the
Canada-U.S. workshop on status of assessment science for
N. W. Atlantic lobster (Homarus americanus) stocks, St. An-
drews, N. B., Oct 24-26, 1978, p. 77-83. Can. Tfech. Rep. Fish.
Aquat. Sci. 932.
Jamieson, G. S.
1982. A system for the precise determination of tow distance
and tow path in offshore resource surveys. Can. Tfech. Rep.
Fish. Aquat. Sci. 1035, 34 p.
Jamieson, G. S., M. Etter, and R. A. Chandler.
1981a. The effect of scallop fishing on lobsters in the western
Northumberland Strait. CAFSAC Res. Doa 81/71, 19 p.
Jamieson, G. S., N. B. Witherspoon, and M. J. Lundy
1981b. Assessment of Northumberland Strait scallop stocks
- 1979. Can. Ttech. Rep. Fish. Aquat. Sci. 1013, 31 p.
1981a Assessment of Northumberland Strait scallop stocks
- 1980. Can. Tfech. Rep. Fish. Aquat. Sci. 1017, 44 p.
Jones, R.
1959. A method of analysis of some tagged haddock returns.
J. Cons. Perm. Int. Explor. Mer 25:58-72.
MacPhail, J. S.
1954. The inshore scallop fishery of the Maritime Provinces.
Fish. Res. Board Can., Atl. Biol. Stn. Circ, Gen. Ser. No. 22,
4 p.
McLeese, D. W., and D. G. Wilder.
■ 1958. The activity and catchability of the lobster (Homarus
americanus) in relation to temperature J. Fish. Res. Board
Can. 15:1345-1354.
Pringle, J. D., and D. J. Jones.
1980. The interaction of lobster, scallop, and Irish moss
fisheries off Borden, Prince Edward Island. Can. Tfech. Rep.
Fish. Aquat. Sci. 973, 10 p.
Pringle, J. D., and G. J. Sharp.
1980. Multispecies resource management of economically im-
portant marine plant communities of eastern Canada.
Helgol. wiss. Meeresunters. 33:711-720.
Robinson, D. G.
1979. Consideration of the lobster (Homarus americanus)
recruitment overfishing hypothesis; with special reference to
the Canso Causeway. In F D. McCracken (editor), Canso
Marine Environment Workshop Part 3 of 4 Parts Fishery
Impacts, p. 77-99. Can. Fish. Mar. Serv., Tfech. Rep. 834.
Saila, S. B., and j. M. Flowers.
1968. Movements and behavior of berried female lobsters
displaced from offshore areas to Narragansett Bay, Rhode
Island. J. Cons. Int. Explor. Mer 31:342-351.
Scarratt, D. J.
1968. 1973. The effect of raking Irish moss (Chondrus
crisjtus) on lobsters in Prince Edward Island. Helgol. wiss.
585
Meeresunters. 24:415-424.
1975. Observations on lobsters and scallops near Pictou, N.S.
Can. Fish. Mar. Serv., Ifech. Rep. 532, 6 p.
SCARRATT, D. J., AND P. F. ELSON.
1965. Preliminary trials of a tag for salmon and lobsters. J.
Fish. Res. Board Can. 22:421-423.
Stasko, H. B.
1975. Modified lobster traps for catching crabs and keeping
lobsters out. J. Fish. Res. Board Can. 32:2515-2520.
Stasko, A. B., T. Amaratunga, and J. F. Caddy.
1977. Northumberland Strait project, Part II. Commercial
shellfish data. Can. Fish. Mar. Serv., MS Rep. 1432, 29 p.
Temple MAN, W.
1933. Female lobsters handicapped in growth by spawning.
Biol. Board Can., Atl. Coast Stn. Prog. Rep. 6, p. 5-6.
1934. Spring, summer and fall lobster fishing in the southern
part of the Gulf of St. Lawrence Biol. Board Can. Bull.
XLIII, p. 13.
FISHERY BULLETIN: VOL. 83, NO. 4
1935. Lobster tagging in the Gulf of St. Lawrenca J. Biol.
Board Can. 1:269-278.
1936. Local differences in the life history of the lobster
(Homarus americanus) on the coast of the Maritime pro-
vinces of Canada. J. Biol. Board Can. 2:41-88.
Wilder, D. G.
1947. The lobster fishery of the southern Gulf of St. Lawrenca
Fish. Res. Board Can., Atl. Biol. Stn. Circ, Gen. Ser. No. 24,
16 p.
1963. Movements, growth and survival of marked and tagged
lobsters liberated in Egmont Bay, Prince Edward Island. J.
Fish. Res. Board Can. 20:305-318.
1965. Lobster conservation in Canada. Rapp. P.-v Reun.
Cons. int. Explor. Mer 156:21-29.
Wilder, D. G., and R. C. Murray.
1956. Movements and growth of lobsters in Egmont Bay, P.E.I.
Fish. Res. Board Can., Prog. Rep. Atl. Coast Stn. 64, p. 3-9.
586
1
AGE, GROWTH, AND DISTRIBUTION OF LARVAL SPOT,
LEIOSTOMUS XANTHURUS, OFF NORTH CAROLINA
Stanley M. Warlen and Alexander J. Chester^
ABSTRACT
Age and growth of the early life history stages of spot, Leiostomus xanthurus, were determined from
daily growth increments on otoliths of larval and early juvenile spot collected from Beaufort Inlet, NC,
to the continental shelf break during the fall and winter of 1978-79 and 1979-80. Spawning occurred on
the mid to outer continental shelf between early November and early March, but appeared to be concen-
trated from mid-December through January. Generally, the youngest larvae were found further offshore;
ages and lengths increased closer to shore Larvae entered the estuary at an average age of 59 days (range
40-74 days) and an average size of 13.6 mm (range 11.3-15.6 mm). Significantly younger and smaller lar-
vae immigrated at the beginning and end of the immigration period. Fish entered the estuary segregated
by age as indicated by the small within-sample variation in age A Gompertz growth equation was used
to express the relationship between age and standard length for 69 larvae collected in 1978-79 and 557
collected in 1979-80. Spot grew from about 1.6 mm SL at hatching to 17-19 mm SL at 90 days. There
were no significant differences in growth parameters between years; age-specific growth rates declined
from =5%/day at age 10 days to <l%/day at age 90 days.
The larvae of a number of commercially important
fishes that spawn on the outer continental shelf of
the southeastern United States are transported
shoreward to estuaries where development is com-
pleted (McHugh 1966; Chao and Musick 1977; Wein-
stein and Walters 1981; Warlen 1982). Although this
general pattern of oceanic spawning and estuarine
development has been known at least since publica-
tion of the work of Hildebrand and Cable (1930),
most recent studies have considered only the
estuarine phase (Chao and Musick 1977; Weinstein
and Walters 1981), and virtually no quantitative data
exist on age and size distribution or growth of lar-
vae between the time of spawning and estuarine
immigration.
Spot, Leiostomus xanthurus, spawn offshore and
are widely distributed in coastal waters from the
mid-Atlantic to Tfexas. Larvae have been reported
from North Carolina to Massachusetts (Berrien et
al. 1978), from the South Atlantic Bight (Fahay 1975;
Powles and Stender 1976), and from the Gulf of Mex-
ico (Fruge 1977; Govoni et al. 1983). Despite studies
on egg and larval development (Fruge and Truesdale
1978; Powell and Gordy 1980), growth of juveniles
(Weinstein and Walters 1981), and feeding ecology
'Southeast Fisheries Center Beaufort Laboratory, National
Marine Fisheries Service, NOAA, Beaufort, NC 28516-9722.
Manuscript accepted January 1985.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985
of larvae (Govoni et al. 1983) and juveniles (Chao and
Musick 1977), little is known of the early growth
history of spot. Our objectives were to 1) determine
the estimated age and size distribution of young spot
from the time of hatching in the ocean to recruit-
ment into the estuary, 2) estimate larval growth
rates, 3) estimate spawning times, and 4) determine
when young spot enter the estuary.
METHODS
Sources of Data
Larvae were collected off Beaufort, NC, during 11
2-d cruises of the RV John de Wolf II, from December
1978 to April 1979 (grid design, stations 1-10) and
from November 1979 to March 1980 (transect
design, stations 11-19) (Fig. 1). At all stations, ex-
cept Beaufort Inlet, samples were obtained from
oblique plankton hauls (Powles and Stender 1976)
collected with 60 cm diameter bongo nets (mesh sizes
333 or 505 /^m) rigged with flow meters. A surface
tow was made at Beaufort Inlet. Larvae were also
collected with a neuston net (Hettler 1979) about 1
mi inside the mouth of the Newport River at Pivers
Island (Fig. 1) seven times from mid-December 1979
to mid-April 1980. Samples were preserved in 95%
ethanol (final concentration =75%) within 5 min of
collection.
587
FISHERY BULLETIN: VOL. 83, NO. 4
76" 30'
76" 00*
Figure 1— Location of sampling sites for late-larval and early-juvenile spot in the mouth of the Newport
River estuary at Pivers Island and for larval spot in the ocean off Beaufort Inlet, NC. Circles are ■
tions sampled from December 1978 to April 1979 and triangles are those sampled October 1979 to
1980.
WARLEN and CHESTER: LARVAL SPOT OFF NORTH CAROLINA
Estimated Age and
Back-Calculated Length
We counted the number of growth increments on
otoHths (eg., Pannella 1971; Brothers et al. 1976) to
estimate age (in days) of each larva. Laboratory-
reared larval spot have been shown to deposit an
average of 1 ring/d on their otoliths (Peters et al.
1978; Warlen 1984^), but do not begin to do so until
5 d after hatching, a time coincident with yolk-sac
absorption and first feeding activity at 20°C (Peters
et al. 1978). Therefore, we added 5 to the number
of counted increments to estimate age. The spawn-
ing date of each larva was estimated by subtracting
age in days from date of capture
After we measured each larva in alcohol to the
nearest 0.1 mm standard length (SL), we teased the
largest pair of otoliths (sagittae) from the surround-
ing tissue, cleaned them in distilled water, and
mounted them on a glass microslide under a thin
layer of Flo-Texx^ mounting medium. They were ex-
amined with a compound microscope fitted with a
television camera. Growth increments were counted
from images of otoliths on a video monitor at
magnifications of at least 400 x. For selected larvae,
otolith radius and the growth increments along it
were measured to the nearest 0.1 yim with a filar
ocular micrometer. We then used Lee's (1920)
modification of the direct proportion formula to
back-calculate lengths and reconstruct the growth
of each fish. In addition to the assumption that
growth increments be daily, the reliability of back-
calculated lengths requires that grov^h of the otolith
must be linearly related to growth of the fish. We
found, for larvae 2.2-12.4 mm SL, that the relation
between body length and otolith radius was linear:
body length (mm) = 2.202 + 0.045 * otolith
radius (/.<m)
n = 32, r2 = 0.95. (1)
Weight-Length Relationships
Because larval fish are not weighed in many
ichthyoplankton field studies, a weight-length rela-
tionship is required to describe the growth of popula-
tions, assess production in terms of dry weight, and
^Warlen, S. M. 1984. Rates of increment formation in otoliths
of larval gulf menhaden, Brevoortia patronus and spot, Leiostomus
xanthurus. Unpubl. manuscr. Southeast Fisheries Center
Beaufort Laboratory, National Marine Fisheries Service, NOAA,
Beaufort, NC 28516-9722.
^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
estimate weight where only length is known. We
determined a dry weight-length relationship from
125 laboratory-reared larvae and early juveniles
(2.7-29.6 mm SL). Live fish were anesthetized in a
solution of MS-222 (tricane methanesulfonate),
removed from the solution, and measured to the
nearest 0.1 mm SL. Fish were then rinsed in distill-
ed water, placed on preweighed Nuclepore^ mem-
brane filters, freeze-dried, and weighed to the
nearest 1 ^g.
RESULTS
Spawning and Larval Movement
The temporal pattern of spawning found here,
though perhaps influenced by the particular dates
and stations sampled (Ikble 1), indicated that spot
is a late October-early March spawner (Fig. 2). The
majority (67%) of fish collected during the fall and
winter of 1979-80 were spawned during December
or January (Fig. 2).
The offshore larval distribution by estimated age
and length suggests that spawning occurred over the
outer continental shelf. Both mean age and length
varied inversely with distance from shore (Figs. 3,
4). Youngest (<25 d) and smallest (<4 mm) larvae
were found most often near or in the Gulf Stream,
80-100 km off Beaufort Inlet, paralleling the 183 m
depth contour (stations 5, 16, 17, 18). However, com-
parable ages and sizes also were found in the mid-
shelf area (stations 1, 14, 15) early in the spawning
season (December 1978; November and December
1979). Older (40-50 d) and larger (>8 mm) larvae
generally occurred closer to shore within about 40
km of Beaufort Inlet in <25 m of water (stations
10-13, 19), except during February and March 1980
when some larvae were caught 50 km offshore at
station 14. Spawning apparently is continuous
between late October and late February, since young
larvae occurred every month at the three offshore
stations (16-18). Most spawning off North Carolina
probably occurs between 75 and 95 km offshore, ex-
cept for some activity in the mid-shelf area early in
the spawning season. Our age-length data provided
no evidence that spot spawn near shore
Estuarine Immigration
Larvae entered the Newport River estuary over
a 4-mo period from about mid-December to mid-
April (Figs. 2, 5). None were caught prior to
December 1979 nor after 17 April 1980. Relative
abundance of larvae collected at Pivers Island dur-
589
FISHERY BULLETIN; VOL. 83, NO. 4
Table 1.— Number of larval spot per 100 m^ caught off North Carolina during the seasons
of 1978-79 and 1979-80. N.S. = No sample taken.
1978-79
cruise
Station number
No.
Date
1
2
3
4
5
6
7
8
9
10
1
6-7 Dec.
1.9
0
0
0
0
0
0
0
0
0
2
4-5 Jan.
5.0
0
N.S.
N.S.
5.6
0
0
19.3
0
0
3
31 Jan.-I Feb.
N.S.
N.S.
N.S.
N.S.
N.S.
N.S.
N.S.
N.S.
0
0
4
7-8 Mar.
1.8
6.4
N.S.
N.S.
N.S.
0
0
1.7
2.7
0
5
26-27 IVIar.
0
0
N.S.
N.S.
N.S.
0
0
0
0
13.3
6
23-24 Apr.
1979-80
0
N.S.
0
0
0
0
0
0
0
0
cruise
Stat
ion number
No.
Date
Inleti
11
12
13
14
15
16
17
18
7
15-16 Nov.
N.S.
0
0
0
N.S.
43.1
3.3
N.S.
N.S.
8
3-4 Dec.
N.S.
0
0
3.1
1.1
0
4.0
1.1
45.0
9
15-16 Jan.
N.S.
2.4
0.4
0.7
108.6
8.8
4.1
N.S.
N.S.
10
11-13 Feb.
N.S.
0
0
4.1
31.5
17.9
0.6
0.3
2.3
11
19-20 Mar.
65.6
0
0
0.7
4.2
11.4
0.4
0.6
0
^Same as station 19.
ing the winter periods of 1967-70 showed major im-
migration peaks in February and March (unpublished
data from R. M. Lewis, Beaufort Laboratory; Thayer
et al. 1974). The duration of estuarine immigration
generally reflected the duration of the spawning
season (Fig. 2).
Statistically significant monthly variations
(ANOVA, P < 0.05) in both age and length of larvae
entering the New^port River estuary were observed
from December to April (Fig. 5). Mean age at entry
increased linearly from December to March and then
decreased in April. Thus, larvae spawned at the
beginning or end of the season spent relatively less
time in the offshore environment than did larvae
spawned in the middle of the season. Length follow-
ed a similar trend, except during January and early
February when it remained about constant, in-
dicating a declining rate of growth. As determined
from seven samples collected at Pivers Island (Fig.
5) and one at Beaufort Inlet (19 March 1980), spot
entering the estuary averaged 59 d-old (range 40-80).
In general, larvae entering the estuary together
had similar spawning dates. As a rule, 50% of the
fish in any Pivers Island sample had been spawned
within a period of 5 d and all had been spawned
within a period of 14 d (Fig. 2). The one exception
was the last sample from Pivers Island in which
several larvae were more than a month older than
the majority of fish. We infer from the generally
small variation in age of fish within a sample that
a continuum of cohorts moved past Pivers Island
enroute to the upstream parts of the estuary and
that early juveniles entered the lower estuary
segregated by age.
Growth Estimates
Average growth of larvae was described by the
Laird version (Laird et al. 1965) of the Gompertz
growth equation (Zweifel and Lasker 1976) fitted to
estimated age and size at time of capture data for
1978-79 and 1979-80 (Fig. 6). Variance about the
estimated growth curve was assumed to represent
genetic differences in growth potential and the ef-
fects of differing environmental conditions over the
year (Pennington 1979). To stabilize the variance of
length over the observed age interval, we used the
log-transformed version of the Gompertz growth
equation:
In [L.J = In [L,.,] +
'(0)
'W
(0)J
a
[1 - e-"']
(2)
where L,„ = length at time t,
length at i = 0,
specific growth rate at ^ = 0,
rate of exponential decay of the
specific growth rata
'(0
^(0) =
The time origin {t = 0) was selected as hatching time
(day 0) and values for L q,, A,q,, and a were obtain-
ed by nonlinear regression. Age accounted for 96%
of the variation in length for one year class (1978-79)
and 91% of the variance in length for the other
(1979-80) in the log-transformed models. We
estimated that spot grew from about 1.6 mm SL at
hatching to 17-19 mm at 90 d. The predicted size at
hatching agrees well with laboratory observations
of Powell and Gordy (1980). Population growth
590
VVARLEN and CHESTER: LARVAL SPOT OFF NORTH CAROLINA
Q.
<
X
o
<
2
20
10
30
20
10
I-
<
o
UJ
oc
^ oc
o <
3
>-
$ 20
3
OC
m
u. 10
(21)
-cm
PI
(21)
—cm —
INLET
(12)
HXD 1
PI
H h
(48)
I — n
C-11
30
20
10
30
OC
g 20
g 10
"30
S 20
CO
>
O 10
(7)
I — CEM
PI
(
(225)
113-
(9)
KXH
PI
(9)
\-cn — I
PI
C-10
(84)
-cm — I
C-9
(9)
i-nzH
PI
U (9)
I TIH
PI
(32)
-CD— I
C-8
(71)
-a-
C-7
10 20
I NOVEMBER
T
I
I
10 20
DECEMBER
"W
I
I
I
I
10 20
JANUARY
30.
10 20
FEBRUARY
J L
10
I MARCH
SPAWNING DATE
Figure 2.— Schematic plots of the spawning times of larval spot caught in the ocean (cruises 7-11 of RV John
de Wolf 11) and late-larvae/early-juvenile spot caught in the Newport River estuary at Pivers Island, NC. In
each distribution, the vertical line is the median value and 50% of the data points fall within the block. Lines
beyond the boxes represent the range of data points.
curves were not significantly different between years
[Hotelling's T~ test of A . a, and L- Bernard
(0)'
'(0)'
(1981) as modified by Hoenig and Hanumara (1983)].
Age-specific growth rates for both years decHned
from =5%/d at age 10 d to <l%/d at age 90 d.
lb determine differences in growth rates for two
groups of larvae of different ages but from the same
cohort, we back-calculated lengths at 5-d intervals
up to 25 d for 10 larvae caught at stations 15 and
16 on 15-16 January 1980 and for 10 larvae caught
at Beaufort Inlet on 19 March 1980 (Ikble 2).
Although the estimated mean spawning date for
591
FISHERY BULLETIN: VOL. 83. NO. 4
76** 30*
76** 00*
Figure 3.— Contour plots of the mean ages of larval spot averaged by station for all samples collected
by the RV John de Wolf II, December 1978-April 1979 and November 1979-March 1980, and for early
juveniles collected at Pivers Island, NC, October 1979-April 1980. Numerals in parentheses are the
numbers of fish aged.
592
WARLEN and CHESTER: LARVAL SPOT OFF NORTH CAROLINA
76" 30*
76- 00*
Figure 4— Contour plots of the mean standard length of larval spot averaged by station for all samples
collected by the RV John de Wolf II, December 1978-April 1979 and November 1979-March 1980, and for
early juveniles collected at Pivers Island, NC, October 1979-April 1980. Numerals in parentheses are the
number of fish collected and measured.
593
FISHERY BULLETIN: VOL. 83, NO. 4
90
80
70
CO
>«
(d
•o
^^
UJ
O
<
60
50
40
30
T
I
A- length
• = age
I
I
I
f i
i
I
I
I
I
I
I
I
1
I
(9) (9) (9) (9) (7) (12)
(21)
16
15
14
13
12
E
E
>,^
I
I-
O
z
UJ
_l
o
tr
<
Q
Z
<
co
11
DEC
JAN
FEB
MAR
APR
10
IMMIGRATION TIME
Figure 5.— Age (mean + 1 standard error) and standard length (mean ± 1 standard error) of late-larval spot entering
the Newport River estuary in North Carolina, December 1979-April 1980. The numbers offish measured and aged
at each sampling date are in parentheses.
both groups was identical (22 December 1979), the
variance about the mean was greater for Inlet-
caught fish. Consequently, back-calculated lengths
also were more variable for Inlet-caught fish {F-test,
P < 0.05), but on the average they appeared to be
larger at every age (^test corrected for unequal
variance, P < 0.05).
Significant differences were found for the weight-
length relation (Fig. 7) of laboratory-reared larvae
<6 mm and those >6 mm (ANCOVA, P < 0.001). We
selected 6 mm as the dividing point because basic
changes in body form had been observed to occur
at around 6 mm (Powell and Gordy 1980). The length
exponent for spot <6 mm SL (4.201) was close to
the mean value (4.152) reported by Laurence (1979)
for larvae of seven marine fishes, while larvae > 6
mm (3.282) approached isometric growth (Ricker
1975).
594
WARLEN and CHESTER: LARVAL SPOT OFF NORTH CAROLINA
20
15-
10
S 5
\-
(D
Z
UJ
-I
o
<
a
z
<
I-
co
1978-1979
15
10
• ••
L(,)=1.686e2«39(l-e-00211'
n= 69
1979-1980
L. . = 1 .609e
n=557
2.624 l-e
-0.0255t
10 20 30 40
50
60
70
80 90
100
AGE (days)
Figure 6— Growth of larval and early-juvenile spot collected from oceanic and estuarine waters of North Carolina in the fall-winter, 1978-79
and 1979-80. The Laird-Gompertz growth model was used to describe the data. Estimates of the parameters were obtained by fitting
the log-transformed version of the model to the data. "T" is the point of maximum absolute growth (inflection point) in the growth curve
595
FISHERY BULLETIN: VOL. 83, NO. 4
Table 2.— Mean back-calculated standard length of 10 spot from
each of two collections of the same cohort (average spawning
date 22 December 1979) taken about 2 mo apart in 1980.
15-16 January
19 March
Age
(d)
Stations 15-16i
Station 19 (Beaufort Inlet)^
SL (mm) SD
N
SL (mm) SD N
5
3.1
0.13
10
3.5
0.39
10
10
3.7
0.15
10
4.4
0.49
10
15
4.6
0.32
10
5.1
0.62
10
20
5.1
0.34
7
6.0
0.67
10
25
6.0
0.35
2
7.0
0.80
10
^Larval mean age, 23 d; mean size, 5.7 mm
^Larval mean age, 83 d; mean size, 15.0 mm
DISCUSSION
Although spot is a winter spawner, it spawns in
relatively warm water. Very young larval spot (<15
d) occurred only in water above 19.3°C, an observa-
tion corroborated by experimental evidence in-
dicating that spot spawn only between 17.5° and
25°C (Hettler and Powell 1981). In late fall and early
winter off North Carolina, such warm temperatures
are found only on the outer continental shelf near
the Gulf Stream. Newly ripe adults probably
emigrate in the fall of the year from the cooling
waters of bays and sounds in Virginia (Hildebrand
and Schroeder 1928), North Carolina (Roelofs 1951),
and South Carolina (Dawson 1958) to spawn in such
warm waters. Hildebrand and Schroeder (1928) and
Dawson (1958) also suggested that spot spawn along
the outer continental shelf.
Warm coastal waters in the fall and the influence
of warm Gulf Stream waters later in the season may
provide a suitable spawning temperature regime
over a long period. The extended (4.5 mo) spawning
season of spot is typical of the general pattern for
Atlantic coast sciaenids (Powles 1981). The spawn-
ing season of spot in North Carolina in 1979-80 was
similar to that found by Hildebrand and Cable (1930)
in North Carohna and by Dawson (1958) in South
Carolina. Because most of the larvae caught off
North Carolina were spawned in December and
January, we conclude that these are the months of
peak spawning. This conclusion is supported by the
observation that peak estuarine immigration occurs
in February and March (unpublished data from R.
M. Lewis, Beaufort Laboratory; Thayer et al. 1974)
for fish we estimate to have been about 2 mo-old.
Hildebrand and Cable (1930) and Lewis and Judy
(1983) also inferred, from length-frequency informa-
tion, that peak spawning occurs in December and
January.
The trend of decreasing larval age and size (Figs.
2, 3) with distance from shore supports the idea that
spot spend virtually their entire larval period in the
ocean. Berrien et al. (1978) and Lewis and Judy
(1983) also noted an inverse trend of size with
distance from shore in the same area to 79 km off-
shore A similar trend may exist in the Gulf of Mex-
ico where Fruge (1977) found small larval spot to
be most abundant 60-80 km off the Louisiana coast.
By the time larvae have been transported to shore
and enter estuarine nursery areas, they have reach-
ed the late larval or early juvenile stage.
Although the mechanism is unclear by which lar-
val spot from 74 to 93 km offshore arrive at the
estuary in about 60 d, their initial onshore movement
is probably a passive transport by water currents in
Onslow Bay. A consistent counterclockwise eddy
(Stefansson et al. 1971) and a strong indication of
bottom drift in a northerly direction on the outer
and mid-continental shelf and directly to the coast
inshore during January-April (Bumpus 1973) could
aid in the transport of larvae. Nelson et al. (1977)
considered that zonal Ekman transport was a signifi-
cant mechanism for movement of larval Atlantic
menhaden, Brevoortia tyrannus, from offshore
spawning grounds to inshore nursery grounds in the
same study area at about the same season of year.
Data from recent years, however, does not lend sup-
port for this hypothesis (Schaaf^). A recent analysis
by Yoder (1983) suggested that mean Ekman
transport does not favor onshore flow in surface
waters during winter off the southeastern United
States. Rather, cross-shelf transport of larval fishes
may depend on highly variable, short-term meteo-
rological events which reverse the mean surface flow.
Variations in transport rates of larvae in the ocean
as well as spawning at variable distances from shore
may be responsible for the seasonal differences in
age and length at immigration (Fig. 5). In addition,
factors affecting growth, such as temperature and
the distribution of food organisms, interact with the
physical factors of transport to produce the temporal
pattern of age and length observed in a given
year.
Young spot undergo several environmentally
related changes in growth during their larval and
juvenile stages. Growth in length of larval spot is
rapid (initially approaching 7%/d) and coincides with
the winter peak of plankton productivity in the
relatively warm water of the outer continental shelf
(Tbrner et al. 1979; TUrner 1981; Yoder et al. 1981;
^W. E. Schaaf, Southeast Fisheries Center Beaufort Laboratory,
National Marine Fisheries Service, NOAA, Beaufort, NC
28516-9722, pers. commun. January 1984.
596
WARLEN and CHESTER: LARVAL SPOT OFF NORTH CAROLINA
100,000
>6 mm fish
Weight =1.4516 Length
- n=93, r2«0.986
10,000
3
S2
lij
>
CO
a
1,000
3.282
100
10
^ 6 mm fish
Weight= 0.2230 LengtH*-^^''
n=32, r2=0.982
J I I I
4 6 810
J I I I
100
BODY LENGTH (mm)
Figure 7— Relationships between dry weight and standard length of spot for length classes <6 mm and >6
mm. Fish were from laboratory spawned and reared stocks.
Yoder et al. 1983). By the time larvae enter the cooler
(often <10°C) coastal and estuarine waters, growth
rate has slowed considerably (<1.5%/d). The asymp-
tote of 22.2 mm SL (Fig. 6, 1979-80 data) estimated
by our growth model corresponds closely to the size
of juvenile spot collected early in their estuarine
residency (Weinstein and Walters 1981). Increase in
length of newly immigrated spot is relatively slow
(=0.5%/d from December to March, estimated from
figure 3 of Weinstein and Walters 1981), and it is
597
FISHERY BULLETIN: VOL. 83, NO. 4
not until after the usual peak in plankton abundance
(Thayer et al. 1974) and increases in water temper-
ature that growth rates accelerate and persist at a
high level through the summer (=1.0%/d from April
to August, estimated from figure 3 of Weinstein and
Walters 1981).
Within the same cohort, older fish had statistically
larger back-calculated sizes at each age than did
younger fish (Tkble 2). One explanation is that size-
selective mortality (eg., predation, Bailey 1984)
favors survival of faster growing larvae and that the
apparent growth rate depends on the size (and age)
of larvae on which it is calculated. Alternatively, the
two groups may have been spawned in different loca-
tions and experienced different environmental con-
ditions that could affect growth.
ACKNOWLEDGMENTS
We thank Mary Boyd for preparing and reading
the otoliths and John Merriner, William Nicholson,
and William Schaaf for their critical reviews of
earlier drafts of this manuscript. We also thank the
many participants on the 1 1 cruises of the RV John
de Wolf II. This research was supported by a
cooperative agreement between the National Marine
Fisheries Service, NOAA, and the U.S. Department
of Energy.
LITERATURE CITED
Bailey, K. M.
1984. Comparison of laboratory rates of predation on five
species of marine fish larvae by three planktonic inverte-
brates: effects of larval size on vulnerability. Mar. Biol.
(Berl.) 79:303-309.
Bernard, D. R.
1981. Multivariate analysis as a means of comparing growth
in fish. Can. J. Fish. Aquat. Sci. 38:233-236.
Berrien, P. L., M. P. Fahay, A. W. Kendall, Jr., and W. G. Smith.
1 978. Ichthyoplankton from the RV Dolphin survey of con-
tinental shelf waters between Martha's Vineyard, Massa-
chusetts and Cape Lookout, North Carolina, 1965-66. U.S.
Dep. Commer., NOAA, Northeast Fish. Cent., Sandy Hook
Lab., Tfech. Ser. Rep. 15, 152 p.
Brothers, E. B., C. P. Mathews, and R. Lasker.
1976. Daily growth increments in otoliths from larval and
adult fishes. Fish. Bull., U.S. 74:1-8.
Bumpus, D. F.
1973. A description of the circulation on the continental shelf
of the east coast of the United States. Prog. Oceanogr.
6:111-157.
Chao, L. N., and J. A. MusiCK.
1977. Life history, feeding habits, and functional morphology
of juvenile sciaenid fishes in the York River estuary, Virginia.
Fish. Bull., U.S. 75:657-702.
Dawson, C. E.
1958. A study of the biology and life history of the spot,
Leiostomus xanthurtis Lacepede, with special reference to
South Carolina. Contrib. Bears Bluff Lab. 28:1-48.
Fahay, M. P.
1975. An annotated list of larval and juvenile fishes captured
with surface-towed meter net in the south Atlantic Bight dur-
ing four RV Dolphin cruises between May 1967 and February
1968. U.S. Dep. Commer., NOAA Tfech. Rep. NMFS
SSRF-685, 39 p.
Fruge, D. J.
1977. Larval development and distribution of Micropogon un-
dulatus and Leiostomus xanthums and larval distribution of
Mugil cephalv£ and Bregmaceros atlanticus off the south-
eastern Louisiana coast. M.S. Thesis, Louisiana State Univ.,
Baton Rouge, 75 p.
Fruge, D. J., and F M. Truesdale.
1978. Comparative lar\'al development of Micropogon un-
dulatvs and Leiostomics xanthurus (Pisces: Sciaenidae) from
the northern Gulf of Mexico. Copeia 1978:643-648.
GovoNi, J. J., D. E. Hoss, and A. J. Chester.
1983. Comparative feeding of three species of larval fishes in
the northern Gulf of Mexico: Brevoortia patronus,
Leiostomics xanthurus, and Micropogonias undulatiis. Mar.
Ecol. Prog. Ser. 13:189-199.
Hettler, W. F.
1979. Modified neuston net for collecting live larval and
juvenile fish. Prog. Fish-Cult. 41:32-33.
Hettler, W. F, and A. B. Powell.
1981. Egg and larval fish production at the NMFS Beaufort
Laboratory, Beaufort, N.C., USA. Rapp. P.-v Reun. Cons. int.
Explor. Mer 178:501-503.
Hildebrand, S. F., and L. E. Cable.
1930. Development and life history of fourteen teleostean
fishes at Beaufort, N.C. Bull. U.S. Bur. Fish. 46:383-488.
Hilldebrand, S. F., and W. C. Schroeder.
1928. Fishes of Chesapeake Bay Bull. U.S. Bur. Fish.
43:1-366.
HoENiG, N. A., and R. C. Hanumara.
1983. Statistical considerations in fitting seasonal growth
models for fishes. Cons. Int. Explor. Mer, C. M. 1983/D:25,
25 p.
Laird, A. K., S. A. Tyler, and A. D. Barton.
1965. Dynamics of normal growth. Growth 29:233-248.
Laurence, G. C.
1979. Larval length-weight relations for seven species of
northwest Atlantic fishes reared in the laboratory. Fish.
Bull., U.S. 76:890-895.
Lee, R. M.
1920. A review of the methods of age and growth determina-
tion of fishes by means of scales. Fish. Invest., Minist. Agric
Fish. Food (G.B.) Ser. II, 4(2):l-32.
Lewis, R. M., and M. H. Judy.
1983. The occurrence of spot, Leiostomus xanthurus. and
Atlantic croaker, Micropogonias undulatus, larvae in Onslow
Bay and Newport River estuary, North Carolina Fish. Bull.,
U.S. 81:405-412.
McHUGH, J. L.
1966. Management of estuarine fisheries. In R. F. Smith, A.
H. Swartz, and W. H. Massman (editors), A symposium on
estuarine fisheries, p. 133-154. Am. Fish. Soc, Spec Publ. 3.
Nelson, W. R., M. C. Ingham, and W. E. Schaaf.
1977. Larval transport and year-class strength of Atlantic
menhaden, Brevoortia tyrannus. Fish. Bull., U.S. 75:23-41.
Pannella, G.
1971. Fish otoliths: Daily growth layers and periodical pat-
terns. Science (Wash., D.C.) 173:1124-1127.
Pennington, M. R.
1979. Fitting a growth curve to field data. In J. K. Ord, G.
P. Patil, and C. Ikillie (editors). Statistical distributions in
598
WARLEN and CHESTER: LARVAL SPOT OFF NORTH CAROLINA
ecological work, p. 419-428. Int. Co-op. Publ. House,
Fairland, MD.
Peters, D. S., J. C. DeVane, Jr., M. T. Boyd, L. C. Clements, and
A. B. Powell.
1978. Preliminary observations on feeding, growth and energy
budget of larval spot (Leiostomits xanthwrus). In Annual
Report of the NMFS, Beaufort Laboratory, Beaufort, N.C.,
to the U.S. Department of Energy, p. 377-397.
Powell, A. B., and H. R. Gordy.
1980. Egg and larval development of the spot, Leiostomvs xan-
thurus (Sciaenidae). Fish. Bull., U.S. 78:701-714.
Powles, H.
1981. Eggs and larvae of North American sciaenid fishes. In
H. Clepper (editor), Marine recreational fisheries 6, p.
99-109. Sport Fish. Inst., Wash., D.C.
Powles, H., and B. W. Stender.
1976. Observations on composition, seasonality and distribu-
tion of ichthyoplankton from MARMAP cruises in the South
Atlantic Bight in 1973. S.C. Mar. Resour. Cent., Tfech. Rep.
Ser. 11, 47 p.
RiCKER. W. E.
1975. Computation and interpretation of biological statistics
of fish populations. Bull. Fish. Res. Board Can. 191, 382 p.
ROELOFS, E. W.
1951. The edible finfishes of North Carolina. In H. F. Ikylor
(editor). Survey of the marine fisheries of North Carolina,
p. 109-139. Univ. N.C. Press. Chapel Hill.
StefXnsson, U., L. p. Atkinson, and D. F. Bumpus.
1971. Hydrographic properties and circulation of the North
Carolina shelf and slope waters. Deep-Sea Res. 18:383-420.
Thayer, G. W., D. E. Hoss, M. A. Kjelson, W. F. Hettler, Jr.,
AND M. W. Lacroix.
1974. Biomass of zooplankton in the Newport River estuary
and the influence of postlarval fishes. Chesapeake Sci.
15:9-16.
TllRNER, R. E.
1981. Plankton productivity and the distribution of fishes on
the southeastern U.S. continental shelf. Science (Wash., DC.)
214:353-354.
TliRNER, R. E., S. W Woo, and H. R. Jitts.
1979. Estuarine influences on a continental shelf plankton
community. Science (Wash., D.C.) 206:218-220.
Warlen, S. M.
[1982]. Age and growth of larvae and spawning time of Atlan-
tic croaker in North Carolina. Proc Annu. Conf. Southeast.
Assoc Fish Wildl. Agencies 34:204-214.
Weinstein, M. p., and M. P. Walters.
1981. Growth, survival and production in young-of-year
populations of Leiostomits xanthwrus Lacepede residing in
tidal creeks. Estuaries 4:185-197.
Yoder, J. A.
1983. Statistical analysis of the distribution of fish eggs and
larvae on the southeastern U.S. continental shelf wath com-
ments on oceanographic processes that may affect larval sur-
vival. Estuarine Coastal Shelf Sci. 17:637-650.
Yoder, J. A., L. P. Atkinson, J. 0. Blanton, D. R. Deibel, D W
Menzel, and G. a. Paffenhofer.
1981. Plankton productivity and the distribution of fishes on
the southeastern U.S. Continental Shelf. Science (Wash.,
D.C.) 214:352-353.
YoKER, J. A., L. P. Atkinson, S. S. Bishop, E. E. Hofmann, and
T N. Lee.
1983. Effect of upwelling on phytoplankton productivity of
the outer southeastern United States continental shelf.
Continental Shelf Res. 1:385-404.
ZWEIFEL, J. R., and R. LASKER.
1976. Prehatch and posthatch growrth of fishes— a general
model. Fish. Bull., U.S. 74:609-621.
599
DIET OF PACIFIC COD, GADUS MACROCEPHALUS, AND
PREDATION ON THE NORTHERN PINK SHRIMP,
PANDALUS BOREALIS, IN PAVLOF BAY, ALASKA
W. D. Albers and p. J. Anderson'
ABSTRACT
Analysis of 455 Pacific cod, Gadus macrocephalus, stomachs collected in 1980 and 1981 from Pavlof Bay,
in the western Gulf of Alaska, showed considerable predation on northern pink shimp, Pandalus borealis.
The most frequently occurring prey items were pink shrimp, P. borealis, 63%; euphausids, 41%; walleye
pollock, Theragra chalcogramma, 27%; and capelin, Mallotus villosus, 26%. Pandalid shrimp and snow
(Tknner) crab occurred more frequently with increasing cod size (30-69 cm fork length). Euphausids
decreased in frequency of occurrence with increasing cod size Pink shrimp length distributions from cod
stomachs and trawl samples were similar. Estimated consumption of pink shrimp by cod in Pavlof Bay
ranged from 142 to 857 t over a 112-day period from late May through mid-September 1981. Cod preda-
tion may be one reason for the failure of the pink shrimp stock to rebuild in Pavlof Bay following closure
of the commercial fishery in 1979. Cod predation may also play a role in keeping other reduced pink shrimp
stocks in the western Gulf of Alaska from rebuilding to former levels.
)
Pacific cod, Gadus macrocephalus, predation on
northern pink shrimp, Pandalus borealis, in Pavlof
Bay (Fig. 1) was studied to determine if it is a fac-
tor in keeping the pink shrimp stock from rebuilding
thera National Marine Fisheries Service (NMFS)
and Alaska Department of Fish and Game (ADF&G)
survey data from the late 1970's indicate that when
pink shrimp populations in regions of western Alaska
began to decrease, cod abundance started to in-
crease Pink shrimp has been reported to be an im-
portant food item in the diet of Pacific cod in the
Gulf of Alaska (Jewett 1978; Hunter 1979). Preda-
tion of pink shrimp by cod may have substantial in-
fluence on shrimp stock abundance
Pavlof Bay was chosen as the study area because
it supported a commercial fishery for pandalid
shrimp in the 1970's and is suspected to contain a
geographically isolated stock of pink shrimp (Ander-
son 1981). From 1972 through 1979, 13,641 1 of pink
shrimp were commercially harvested from Pavlof
Bay (calculated from ADF&G commercial catch data
and NMFS survey data). Survey data from Pavlof
Bay indicate that in 1977 and 1978 when pink shrimp
abundance began decreasing, cod abundance began
increasing (Fig. 2). Following the 1979 season the
bay was closed to commercial shrimping due to
depressed shrimp abundance levels which remain-
ed low through 1983.
This report presents data which suggest that
Pacific cod predation is a factor in keeping shrimp
stocks from rebuilding. The summer diet of cod, prey
size selectivity, and an estimate of pink shrimp
biomass consumed by cod in Pavlof Bay during a
112-d period from late May through mid-September
1981 are discussed.
MATERIALS AND METHODS
Pacific cod were collected from 31 tows during
three trawl surveys. The first collection was done by
NMFS on 25-26 August 1980, the second by ADF&G
on 23-25 May 1981, and the third by NMFS on 10-11
September 1981. The collecting was done during
daylight hours over a period of about 14 h a day. All
three surveys used a high-opening shrimp trawl with
an 18.6 m headrope and footrope described by
Wathne (1977). Mesh size of the trawl is 32 mm and
path-width is about 10 m. Each tow was about 1.8
km in length. Randomly selected sampling locations
were restricted to depths >55 m since previous
surveys showed that neither shrimp nor cod were
found in abundance in shallow water. Both shrimp
and cod are uniformly distributed at depths >55 m
in Pavlof Bay.
When possible, five stomachs per 5 cm interval of
fork length (FL) were removed from every trawl
catch and preserved in 10% Formalin^. In the
'Northwest and Alaska Fisheries Center, National Marine
Fisheries Service, NOAA, 2725 Montlake Blvd. E., Seattle, WA
98112.
^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Manuscript accepted January 1985.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
601
FISHERY BULLETIN: VOL. 83, NO. 4
Figure 1.— Location of the study area of pink shrimp and Pacific cod (55 m isobath indicated by dotted/dash-line).
laboratory, prey items were sorted to the lowest
possible taxon. Frequency of occurrence (number of
stomachs containing the food item), number of each
prey item, volume by water displacement (nearest
0.1 mL), and wet weight (nearest gram) were record-
ed. From these measurements, percentages by fre-
quency of occurrence, number, and volume were
calculated from non-empty stomachs only.
Size composition was recorded for prey species of
commercial importance including pink shrimp
(carapace length, CL); humpy shrimp, Pandalus
goniuriLs, CL; snow (Tknner) crab, Chionoecetes bair-
di, carapace width (CW); and walleye pollock,
Theragra chalcogramma, fork length (FL). Addi-
tionally, size composition was recorded for samples
of pink shrimp (CL), humpy shrimp (CL), Pacific cod
(FL), and walleye pollock (FL) caught in each tow.
lb determine if Pacific cod were feeding on
selected sizes of pink shrimp, the Kolmogorov-
Smirnov test (Sokal and Rohlf 1969) was used to test
602
ALBERS and ANDERSON: DIET OF PACIFIC COD
for a significant difference between pink shrimp
length distributions measured from Pacific cod
stomachs and those measured from the trawl. Pink
shrimp lengths tested were ^16.5 mm CL. Ander-
son (1981) reported that shrimp <16.5 mm CL are
not fully vulnerable to trawl capture
Population biomass estimates for pink shrimp and
Pacific cod were calculated using the area swept
technique (Alverson and Pereyra 1969).
An estimate of pink shrimp biomass consumed by
Pacific cod in Pavlof Bay during the 112-d period be-
tween the late May and mid-September 1981 surveys
was determined through methods described by Minet
and Perodou (1978). Undigested weights (W) of pink
shrimp were determined from carapace lengths
using the weight-length relationship W = 0.000802
(CL)-'^^^ (calculated from Pavlof Bay pink shrimp
length-weight data). The mean weight of pink shrimp
per stomach for each 5 cm length group of Pacific
cod was calculated from stomachs where at least
80% of the pink shrimp were measurable (Ikble 1).
A stomach which contained <80% measurable pink
shrimp was deemed not suitable for determining the
weight of undigested shrimp consumed. These data
were then weighted using 768 cod lengths measured
during the three surveys. The mean weight of pink
shrimp in the stomach of an average-sized cod was
then estimated for each survey (Tkble 1).
The average rates of elimination (r) of food from
Pacific cod stomachs collected during the May and
September 1981 surveys were calculated from Jones'
(1974) equation for food elimination rates from
Atlantic gadoids including Atlantic cod, Gadus
morhua. Jones found that the rates of elimination
for the three species of gadoids studied were effec-
tively the same, adjusting for fish and meal size, and
temperature Since Pacific cod are very similar to
Atlantic cod, we used Jones' equation in the absence
of more relevant information:
r (g/h) =
j^QO.035 {To - Tc) J^O.46 QJ^li
175
where Tc = 6°C; temperature of the experiment
(Jones 1974).
To = 5°C (May), 7°C (September); observed
temperature in Pavlof Bay from expen-
dable bathythermograph data.
X = 98.9 g (May), 109.0 g (September); the
average weight of food found in one
stomach. The average weight of food
was estimated for each 5 cm length
group of Pacific cod and then weighted
using 502 cod lengths measured dur-
ing the May and September surveys.
Stomachs containing at least 60% of
the greatest weight of food encounter-
ed for each cod length group were used
to determine X.
Q = 0.12; the average rate of elimination of
1 g of food from the stomach of a 40
cm gadoid (Jones 1974).
L = 52.7 cm (May), 53.0 cm (September);
the average length of Pacific cod calcu-
lated from 236 fish measured in May
and 266 fish measured in September.
E
C
a
o
o
c
o
T)
c
D
M
<
0
0
Qj
800
600 —
400 —
r— 600
200 —
400
— 200
o
0
Q.
>
cr
c
Q.
Q
D
O
0
:r
<Q
N.
0
3
1872 1874
' I ' 1 ' T '
1876 1878 1880 1882
YEAR
Figure 2.— Abundance of pink shrimp and Pacific cod from NMFS summer trawl survey data
collected in Pavlof Bay, 1972-82.
603
FISHERY BULLETIN; VOL. 83, NO. 4
RESULTS
Cod Diet
:c CD °-
O) 05 t
00
E
Q.
«
CO
■D
c
CO
>>
to
o
oo
(0
3
<
u
a
E
o
a>
c
o
Q.
E
jsi:
0)
to
gi
T3
c
3
c
10
E
c
g
w
(0
O
I
00
l3
00
0)
E
B
a.
(X>
(0
3
o>
3
<
CD
= o^
.5>1o E
O) 0} c
» T3
£1 O
E "
C3)J
CD
en
l|i
.s't; E
ffi 0) ;=
£> O
E "
0> u) t
CD '<B S,'^ ^
X 5:2' -SB
p p ■'t CD 05 "^
tb c\i CO irj ■^ cjj
^ ■"t CD -^ 1^
CO CM O OJ
00
e3>
o o -^ CO p r^
cvi CO o T^ cO cO
CO
CO
, CO 'T -"t CM 1- CvJ
I 1- CO I- 00 CM
CD
CO
c^
CJCMCMCOOOOJ'* CO
h^ooaiiri^cvjcvj oi
cvioo'd-cDr^oir) lo
00 CD •>- 00 T- 1^
O)
CM
5|a
^ 00 Q.
.5>to E
0) CD C
CD *:g'-SS
Q> 3 C
2-5^
COpcOCMppoO 05
cocJjcJ>^^r^Kc^ \p
■.- 1- CM 1- IT) in 1^.
CMcn'S-oocO'^co CO
'S- C3> CO 1- CO
CM
■«t in CD CM CD in 1-
co
CO
CM
O CM ^ O •■- CM CM
t^ CM CO r^
1- in ■*
o
CM
CJ)
in
d) -o
JO o
E "
2 cj t
ft"
CM in 00 1^ ■>- in
O CD CO CO h^ 00 CM
CO
(O
CM
CM CM CJl h- CO CD ■.-
T- -"U" CO in
CD
CO
CvJ
I O) C3
^0>^0>^CT>^0
coco'S-'^inincoco
ciincbincbmoin
cocO'^'tinincDcD
Of 455 Pacific cod stomachs examined, 435 con-
tained food. Data obtained from cod stomachs col-
lected in August 1980, May 1981, and September
1981 are presented in Ikble 2. Combining these data,
the most frequently occurring prey items were pink
shrimp (63%), euphausids (41%), walleye pollock
(27%), and capelin, Mallottis villosus, (26%). Crusta-
ceans, mostly shrimp, crab, and euphausids, were
present in 93% of the stomachs containing food and
comprised 45% of the volume Ifeleosts, mostly wall-
eye pollock and capelin, were present in 60% of the
stomachs containing food and comprised 54% of the
volume Gastropods, bivalves, sipunculids, and asci-
dians together comprised 1% of the volume
Crustaceans made up the greatest part of the diet
in the May sample and teleosts comprised the
greatest part of the diet in the August and
September samples (Ikble 2). Shrimp, mostly pink
shrimp, made up 67% of the volume in May com-
pared with 28%, combining August and September
data. Crabs, mainly snow crab, comprised 10% of the
volume in May compared with 3% in August-
September. Teleosts, primarily walleye pollock and
capelin, made up 4% of the volume in May and 65%
in August-September.
Data on the 10 most frequently occurring food
items was categorized by 10 cm length (FL) groups
of Pacific cod in a size range of 30 through 69 cm
(Tkble 3). Hurtubia's (1973) trophic diversity method
was used to assure that enough stomach samples had
been analyzed to give representative values for each
length group. Pink shrimp occurred most frequent-
ly in all but one length group (30-39 cm) and was
the dominant food item by volume in all length
groups. Pink shrimp and snow crab increased both
in frequency of occurrence and volume with in-
creasing cod size Conversely, euphausids were the
most frequently encountered food item in the 30-39
cm length group, but their frequency of occurrence
and volume decreased with increasing cod size No
trends were evident for the occurrence of teleosts.
Although data from the three surveys were combined
for Tkble 3, the above trends were evident in each
of the surveys.
The size ranges and mean sizes of pink shrimp and
humpy shrimp consumed by Pacific cod were similar
in general to those found in the trawl (Tkble 4). Size
range and mean size of walleye pollock consumed by
cod were considerably smaller than those fish cap-
tured by the trawl.
604
ALBERS and ANDERSON: DIET OF PACIFIC COD
Table 2.— Percent frequency ot occurrence (F), percent by number (N). and percent by volume {V) of food items in
Pacific cod stomachs for August 1980 and May and September 1981. Food categories followed by (total) is tfie sum
of the food items that fall within that category for percent number and percent volume. Percent frequency of occur-
rence is the number of stomachs containing the food category or item divided by the total number of stomachs con-
taining food.
August 1980
May 1981
September 1981
(n = 202)
(n = 63)
(n = 170)
Food items
F
N
V
F
N
V
F
N
V
Crustacea (total)
93.1
92.2
29.4
100.0
99.5
95.0
91.2
57.6
37.6
Amphipoda
—
—
—
—
—
—
1.8
0.3
<0.1
Euphausiacea
53.5
77.0
6.1
81.0
87.3
17.8
12.4
3.3
0.1
Decapoda
Natantia (total)
71.3
15.0
23.0
76.2
10.4
67.1
80.6
46.1
32.2
Pandalidae
—
—
—
3.2
0.1
0.1
1.8
0.2
<0.1
Pandalus borealis
56.9
9.3
18.5
65.1
7.6
59.7
70.6
34.9
29.9
Pandalopsis dispar
—
—
—
17.5
0.5
1.0
1.2
0.1
<0.1
Pandalus goniurus
20.3
1.7
2.3
25.4
0.4
1.7
4.1
0.9
0.5
Pandalus hypsinotus
0.5
<0.1
0.1
4.8
0.1
1.1
1.2
0.1
0.3
Crangonidae
—
—
—
—
—
—
4.1
0.8
0.2
Crangon sp.
3.0
0.2
0.1
7.9
0.1
0.2
2.9
0.5
<0.1
Crangon communis
2.5
0.2
0.1
12.7
0.2
0.3
18.2
2.9
0.5
Crangon dalli
—
—
—
—
—
—
3.5
0.5
0.1
Argis sp.
—
—
—
4.8
0.1
0.3
1.2
0.1
<0.1
Argis dentata
—
—
—
4.8
0.1
0.3
1.8
0.2
<0.1
Argis far
—
—
—
—
—
—
4.7
0.7
0.2
Hippolytidae
0.5
<0.1
<0.1
6.3
0.1
0.1
—
—
—
Eualus sp.
0.5
<0.1
<0.1
—
—
—
—
—
—
Eualus macilenta
—
—
—
11.1
0.3
0.2
5.3
0.8
<0.1
Eualus suckleyi
0.5
<0.1
<0.1
1.6
0.1
0.2
2.9
0.4
0.1
Unidentified Natantia
26.7
3.6
1.9
30.2
0.7
1.9
20.0
3.0
0.4
Reptantia (total)
3.5
0.2
0.3
39.7
1.8
10.1
31.2
7.9
5.3
Lithodidae
Paralithodes camtschatica
0.5
<0.1
<0.1
—
—
—
—
—
—
Majidae
Chionoecetes bairdi
1.5
0.1
0.2
41.2
1.8
10.0
25.3
6.2
4.7
Paguridae
2.0
0.1
0.1
—
—
—
0.6
0.1
<0.1
Pagurus aleuticus
—
—
—
—
—
—
0.6
0.1
0.2
Pinnotheridae
Pinnixa sp.
—
—
—
1.6
<0.1
0.1
8.2
1.5
0.4
Osteichthyes (total)
59.4
8.1
68.8
15.9
0.4
3.7
77.1
38.2
60.6
Ammodytes hexapterus
1.5
0.1
0.1
1.6
<0.1
<0.1
—
—
—
Gadus macrocephalus
—
—
—
—
—
—
1.2
0.1
1.8
Hippoglossoides elassodon
0.5
<0.1
1.3
—
—
—
4.7
0.7
4.1
Icelus sp.
—
—
—
—
—
—
0.6
0.1
0.3
Lumpenella longirostris
—
—
—
1.6
<0.1
0.1
—
—
—
Lumpenus sp.
—
—
—
1.6
<0.1
0.1
10.0
1.8
1.3
Lumpenus fabricii
—
—
—
—
—
—
0.6
0.1
<0.1
Lumpenus maculatus
0.5
<0.1
<0.1
—
—
—
—
—
—
Lumpenus sagitta
—
—
—
1.6
<0.1
0.1
—
—
—
Lycodes sp.
—
—
—
—
—
—
0.6
0.1
0.6
Lycodes brevipes
—
—
—
—
—
—
1.2
0.1
0.9
Mallotus villosus
28.7
4.6
32.7
4.8
0.1
1.4
29.4
8.9
20.5
Theragra chalcogramma
13.4
.7
24.8
1.6
<0.1
1.2
51.8
17.0
21.9
Trichodon trichodon
—
—
—
—
—
—
5.9
0.7
4.3
Zaprora silenus
—
—
—
—
—
—
0.6
0.1
0.7
Unidentified Osteichthyes
30.7
2.7
9.9
14.3
0.3
0.8
37.1
8.5
4.2
Bivalvia (total)
1.0
0.1
0.1
4.8
0.1
0.1
14.7
3.1
0.1
Clinocardium sp.
0.5
<0.1
<0.1
3.2
<0.1
<0.1
1.8
0.2
<0.1
Macoma sp.
—
—
—
—
—
—
0.6
0.1
<0.1
Yoldia sp.
—
—
—
3.2
<0.1
<0.1
12.4
2.6
<0.1
Unidentified Bivalvia
0.5
<0.1
<0.1
1.6
<0.1
<0.1
1.8
0.2
<0.1
Gastropoda (total)
1.0
0.1
0.1
3.2
0.1
0.1
0.6
0.1
<0.1
Naticidae
1.5
0.1
0.1
1.6
<0.1
<0.1
—
—
—
Neptunidae
—
—
1.6
<0.1
<0.1
0.6
0.1
<0.1
Trochidae
Margarities sp.
—
—
—
1.6
<0.1
<0.1
—
—
—
Unidentified Gastropoda
—
—
—
1.6
<0.1
<0.1
—
—
—
Ascidiacea
0.5
<0.1
0.2
—
—
—
—
—
—
Sipuncula (Phylum)
0.1
<0.1
0.1
1.6
<0.1
0.1
2.4
0.4
0.6
Plant
2.0
0.1
1.4
3.2
<0.1
0.9
4.7
0.6
1.0
Pebbles
2.5
—
0.1
19.0
—
0.4
18.8
—
0.4
605
FISHERY BULLETIN; VOL. 83, NO. 4
Table 3,— The 10 most frequently occurring food items are categorized by 10 cm length (FL) groups of Pacific cod
from 30 to 69 cm. Data is presented by percent frequency of occurrence (F), percent by number (A/), and percent
by volume (V).
30-39 cm
40-49 cm
50-59 cm
60-69 cm
{n
= 20)
(n
= 216)
(n
= 173)
(n
= 23)
Food items
F
N
V
F
N
V
F
N
V
F
N
V
Euphausiacea
78.8
51.3
7.5
54.7
58.3
9.0
48.1
54.8
8.9
27.3
32.7
3.0
Pandalus borealis
36.4
15.1
31.9
61.0
19.0
30.6
69.9
17.7
36.4
81.8
29.7
47.6
Pandalus goniurus
3.0
0.5
0.9
13.8
0.7
1.2
20.2
1.3
1.2
22.8
0.6
0.9
Crangon sp.
5.6
2.4
<0.1
3.5
0.2
0.1
4.0
0.3
0.1
9.0
0.3
0,2
Crangon communis
—
—
—
10.1
0.9
0.4
12.9
1.2
0.3
18.2
1.4
0,5
Eualus macilenta
11.1
0.3
0.3
5.2
0.3
0.1
6.7
0.4
0.1
—
—
—
Chionoecetes bairdi
—
—
—
11.5
1.4
2.5
26.7
3.0
5.1
59.1
5.3
9.0
Lumpenus sp.
—
—
—
4.3
0.9
0.8
3.5
0.5
0.4
4.5
0.2
0.3
Mallotus villosus
14.1
8.7
28.3
19.6
3.5
18.3
24.4
4.7
17.5
22.8
4.7
9.3
Theragra chalcogramma
16.7
9.5
8.5
20.5
4.4
15.2
22,7
6.3
16.7
13.7
6.3
3.9
All sizes of cod examined were feeding on both
small and large pink shrimp. Pink shrimp length (CL)
distributions measured from cod stomachs and from
trawl samples began to overlap at about 12 mm (Fig.
3). Piesults from the Kolmogorov-Smirnov test com-
paring pink shrimp length distributions >16.5 mm
CL from cod stomachs and trawl samples showed
no significant difference {P > 0.10) in August 1980
and May 1981. There was a significant difference {P
= 0.009) in the September 1981 sample. No signifi-
cant difference between length distributions in-
dicates that cod were not feeding on selective sizes
of pink shrimp. A significant difference indicates
that cod consumed a greater proportion of smaller
shrimp than was captured by the trawl.
stomach were 24.4 g for May and 11.2 g for
September 1981 (Tkble 1). Per day, the average
amount of pink shrimp consumed by one cod was 8.1
g and 3.7 g for May and September, respectively.
The estimated weight of an average length cod
was 1,689.5 g for the May survey and 1,720.1 g for
the September survey (W = 0.00000593L3168.
Owen and Blackburn 1983). Cod biomass estimates
were 1,621 t for May and 591 t September,
respectively.
Based on the above parameters, estimates of pink
shrimp biomass consumed were calculated using the
May and September data (Ikble 5). With May data.
Pacific cod consumed an estimated 875 t of pink
shrimp over the 112-d period, whereas the
Table 4.-
-Size range and mean size of prey and trawl caught animals. Size data were not collected for snow
crab in the trawl. CL = carapace length; FL = fork length; CW = carapace width.
Number r
neasured
Trawl
Size
range
Mean
size
Prey
Prey
Trawl
Prey
Trawl
Pink shrimp 1,143
Humpy shrimp 102
Walleye pollock 236
Snow crab 69
7,823
202
2,100
6.5-26.0 mm (CL)
8.0-17.5 mm (CL)
6.0-25.0 cm (FL)
6.0-42.0 mm (CW)
10.0-26.0 mm (CL)
10.5-18.5 mm (CL)
6.0-63.0 cm (FL)
16.2 mm
13.5 mm
10.3 cm
22.2 mm
18.0 mm
13.9 mm
22.8 cm
Estimate of Pink Shrimp
Biomass Consumed
The extent of the Pacific cod predation on pink
shrimp in Pavlof Bay was examined by estimating
total biomass consumed during a 112-d period from
late May through mid-September 1981. Analysis
using Jones' (1974) equation indicated that for both
1981 surveys the average amount of food found in
a cod stomach was digested in about 3 d. The average
weights of undigested pink shrimp found in a cod
Table 5. — Calculation of the total pink shrimp biomass consumed
by Pacific cod during a 112-d period from late May through mid-
September 1981. Two estimates are presented using the May and
September data.
May 1981
Sept. 1981
Mean weight of pink shrimp
consumed daily by one cod (g)
8.1
3.7
112-d consumption by one cod (g)
907.2
414.4
Weight of an average length cod (g)
1,689.5
1,720.1
Proportion of pink shrimp eaten
relative to cod weight
0.54
0.24
Cod biomass estimate (t)
1,621
591
Pink shrimp biomass consumed (t)
875
142
606
ALBERS and ANDERSON: DIET OF PACIFIC COD
September information suggests that cod consum-
ed an estimated 142 t of pink shrimp over the same
period.
DISCUSSION
Cod Diet
Pink shrimp was the dominant food item identified
by frequency of occurrence (63%) and percent
volume (31%). In the Gulf of Alaska near Kodiak
Island, Jewett (1978) reported pink shrimp occur-
ring in 4% of the Pacific cod examined, and Hunter
(1979) found pink shrimp occurring in 24% of the
cod, representing 16% of the diet by weight. Hunter
also identified pink shrimp as the dominant food
item in his study. However, our study exhibited a
higher percent frequency of occurrence for that
species. Unlike our study, Jewett and Hunter's
studies included examinations of cod from offshore
areas, which were not regions of high pink shrimp
density (Gaffney 19773).
The prey size ranges of walleye pollock and snow
crab in our study were similar to those found by
Hunter (1979). In our study, the maximum length
of walleye pollock consumed by cod was 25 cm FL,
although the majority were between 6 and 20 cm.
Hunter (1979) reported that cod around Kodiak
Island were feeding on groundfish (including wall-
eye pollock) between 2 and 24 cm. The snow crab
consumed by cod in Pavlof Bay ranged from 5 to 45
mm CW, which is similar to the size range of snow
crab (1-40 mm) found in cod stomachs by Hunter
(1979). Jewett (1978) reported a greater size range
of snow crab occurring in cod stomachs (from 1.8
to 70 mm), yet 78% were between 7 and 23 mm. The
maximum size of cod examined by Jewett was 92 cm
TL (total length) compared with 69 cm FL in our
study, and this difference probably accounts for his
observation of larger snow crab.
We believe that cod were not feeding on selected
sizes of shrimp. The size ranges and mean sizes of
pink shrimp and humpy shrimp consumed by cod
were similar to those found in the trawl (Tkble 4).
However, cod did consume small (<10.0 mm CL) pink
shrimp that were not captured by the trawl. We
believe this is due to trawl bias toward larger shrimp.
No significant difference was found between pink
shrimp length distributions from cod stomachs and
trawl samples in two of the three surveys, indicating
that cod were not feeding on selected sizes of shrimp.
There was a significant difference (P = 0.009) for
the September 1981 survey. In this sample either cod
selected slightly for smaller shrimp or the trawl
caught slightly larger shrimp.
Estimate of Pink Shrimp
Biomass Consumed
The estimated pink shrimp biomass in Pavlof Bay
decreased by 1,501 1 between the May and Septem-
ber surveys in 1981. During this period we estimated
that Pacific cod consumed between 142 and 875 t
of pink shrimp. Since Pavlof Bay is believed to con-
tain a geographically isolated stock of pink shrimp
(Anderson 1981) and because the bay was closed to
shrimp fishing in 1981, cod predation is responsible
for at least part of the biomass decline
The estimate of pink shrimp biomass consumed
over the 112-d period using the May survey data was
733 t more than was estimated using September
data. Two of the parameters used to calculate con-
sumption estimates were responsible for this dif-
ference In May the mean weight of pink shrimp con-
sumed daily by one cod was about double the amount
in September. Pink shrimp were more abundant and
made up a larger percentage of the diet in May than
in September. Additionally, cod biomass was
estimated to be almost three times higher in May
than it was in September causing the consumption
estimate to be higher in May (Tkble 5).
We belive that consumption of pink shrimp by cod
probably lies toward the high end of the calculated
range (142-875 t). Biomass estimates were probably
conservative for pink shrimp and Pacific cod. Bio-
mass was calculated on the assumption that all cod
and shrimp were on bottom and all those in the path
of the trawl were caught. This is not true for cod
or shrimp. For example, Edwards (1968) reported
that up to 49% of the gadoids in the path of a trawl
avoid capture. Also, an estimate of the catchability
of shrimp with the high-opening shrimp trawl was
about 56% (Alaska Department of Fish and Game
1982'*). If the cod biomass estimate was conservative,
the consumption of pink shrimp by cod would be
higher than calculated. Further, if the pink shrimp
biomass estimate was conservative, the calculated
^Gaffney, F. G. 1977. Kodiak pandalid shrimp research. Com-
mercial Fisheries Research and Development Act, Project No.
5-36-R. Unpubi. manuscr., 76 p. National Marine Fisheries Ser-
vice, NOAA, Wash., DC 20235.
■•Westward Region Shellfish Staff, Alaska Department of Fish
and Game 1982. Westward Region Shrimp Fishery Management
Plan. Unpubi. manuscr., 70 p. Alaska Department of Fish and
Game, Kasheruaroff, Mission Road, P.O. Box 686, Kodiak, AK
99615.
607
FISHERY BULLETIN: VOL. 83, NO. 4
15
AUGUST 1980
P
e
r
c
e
n
t
F
r
e
q
u
e
n
c
y
10 —
oJ_L
10
^S Cod n=287
^^ Trawl n=2685
15 20
Carapace Length(mm)
25
30
15—1
MAY 1881
^S Cod n=406
^ Trawl n=2586
r
c
e
n
t
F
r
e
q
u
e
n
c
y
10
5 —
15 20
CarapacQ Length(mm)
25
30
608
ALBERS and ANDERSON: DIET OF PACIFIC COD
t5-i
P
e
r
c
e
n
t
F
r
e
q
u
e
n
c
y
ID-
S-
SEPTEMBER 198
^ Cod
n=440
^ Trawl
n=2552
^
10
15 20
Carapace Length(mm)
25
30
Figure 3— Size distribution of pink shrimp from trawl samples and Pacific cod stomachs for August 1980 and May and September
1981.
biomass decline of pink shrimp between May and
September 1981 would also be greater.
Pacific cod are probably feeding on pink shrimp
in Pavlof Bay the entire year although the largest
concentrations of cod are likely to occur from spring
through fall. Trawl survey data from Pavlof Bay in-
dicate that cod biomass decreased from 93 t in
September 1978 to 20 t in February 1979 and then
increased to 371 t in May 1979. Pacific cod are
migratory; they move to shallow areas (<90 m) in
spring to feed and return to deeper areas (165-247
m) offshore in fall or winter to spawn (Moiseev 1953).
The majority of Pavlof Bay is <90 m deep which is
not preferred winter habitat.
Although we believe that Pacific cod predation has
an effect on the present reduced population of pink
shrimp, predation probably was not the primary
reason for the initial decline of pink shrimp in Pavlof
Bay that began in 1977. At that time Pacific cod
abundance was just beginning to increase (Fig. 2).
Fishing removed about 3,819 t (calculated from
ADF&G commercial catch data and NMFS survey
data) of pink shrimp between the 1977 and 1978
surveys, which was 30% of the estimated available
biomass in 1977. This harvest and the dying out of
the strong 1971 year class (Anderson 1981) were
probably responsible for most of that initial decrease
Cod predation did become a factor, however, once
the pink shrimp resource was reduced. This impact
on pink shrimp appears substantial despite the
reduction of cod in Pavlof Bay (Fig. 2).
ADF&G (footnote 4) has reported diminishing pink
shrimp stocks in other areas of the western Gulf of
Alaska. Some areas that once contained high con-
centrations of pink shrimp experienced reductions
in abundance at the same time as Pavlof Bay. In most
areas, no increase in pink shrimp abundance was
observed through 1982, though many areas were
closed to fishing. Like Pavlof Bay, these other areas
experienced an increase in Pacific cod abundance
about the same time as pink shrimp populations were
declining. Cod predation may play a role in keeping
these reduced pink shrimp stocks from rebuilding
to former levels.
ACKNOWLEDGMENTS
Thanks to Pete Jackson and Dave Jackson, Alaska
609
Department of Fish and Game, for collecting the
May 1981 stomach samples.
LITERATURE CITED
Alverson, D. L., and W. T. Pereyra.
1969. Demersal fish explorations in the northeastern Pacific
Ocean - an evaluation of exploratory fishing methods and
analytical approaches to stock size and yield forecasts. J.
Fish. Res. Board Can. 26:1985-2001.
Anderson, P. J.
1981. A technique for estimating growth and total mortality
for a population of pink shrimp Pandaliis borealis from the
western Gulf of Alaska. In T. Frady (editor), Proceedings
of the International Pandalid Shrimp Symposium, February
13-15, 1979, Kodiak, Alaska, p. 331-342. Univ. Alaska, Fair-
banks, AK, Sea Grant Program, Sea Grant Rep. 81-3.
Edwards, R. L.
1968. Fishery resources of the North Atlantic area, hi D. W.
Gilbert (editor), The future of the fishing industry of the
United States, p. 52-60. Univ Wash. Publ. Fish., New Sen 4.
Hunter, M. A.
1979. Food resource partitioning among demersal fishes in
the vicinity of Kodiak Island, Alaska. M.S. Thesis, Univ.
Washington, Seattle, 120 p.
HURTUBIA, J.
1973. TVophic diversity measurement in sympatric predatory
species. Ecology 54:885-890.
FISHERY BULLETIN: VOL. 83, NO. 4
Jewett, S. C.
1978. Summer food of the Pacific cod, Gadus macrocephalics,
near Kodiak Island, Alaska. Fish. Bull., U.S. 76:700-706.
Jones, R.
1974. The rate of elimination of food from the stomachs of
haddock, Melanogrammus aeglejinus, cod Gadvs morhua and
whiting Merlangivs merlangiis. J. Cons. Int. Explor. Mer
35:225-243.
MiNET, J. P., AND J. B. PERODOU.
1978. Predation of cod, Gadus morhua, on capelin, Mallotus
villosus, off eastern Newfoundland and in the Gulf of St.
Lawrence Int. Comm. Northwest Atl. Fish. Res. Bull. 13:
11-20.
MOISEEV, P. A.
1953. Treska i kambaly dalnevostochnykh morei (Cod and
flounders of far-eastern seas). [In Russ.] Izv. Tikhookean.
Nauchno-Issled Inst. Rybn. Khoz. Okeanogr. 40:1-287.
[Engl, transl. by Fish. Res. Board Can., Transl. Ser. No. 119,
576 p.]
Owen, D. L., and J. E. Blackburn.
1983. Bottomfish catch and trawl data from an otter trawl
survey in northern Shelikof Strait, Chignik area, and Chiniak
gully, Alaska, July and August 1981. Alaska Dep. Fish
Game, Ifech. Data Rep. 82, 68 p.
SOKAL, R. R., and F. J. ROHLF.
1969. Biometry, the principles and practice of statistics in
biological research. W H. Freeman and Company, San Fran-
cisco, 776 p.
Wathne, F.
1977. Performance of trawls used in resource assessment.
Mar. Fish. Rev 39(6): 16-23.
610
VERTICAL DISTRIBUTION OF ICHTHYOPLANKTON OFF
THE OREGON COAST IN SPRING AND SUMMER MONTHS
George W. Boehlert,' Dena M. Gadomski,^ and Bruce C. Mundy^
ABSTRACT
Day and night discrete-depth tows were taken off the Oregon coast in spring and summer months to
assess the vertical distribution of ichthyoplankton in nearshore waters. Over 1,000 larvae representing
33 taxa of both coastal and offshore ichthyoplankton assemblages were taken; Psettichthys melanostictus
was the most abundant coastal species and Lyopsetta exilis the most abundant offshore species. Larvae
were generally most abundant at 10-30 m, near the seasonal thermocline in both day and night collec-
tions. Larval abundance in July was much higher than in April-May collections. Limited evidence for diel
vertical migration suggests that Psettichthys melanostictiis moves to surface waters at night and Gadus
macrocephalus moves to deeper water at night. No trends of changes in depth distribution were observed
with increasing size
Knowledge of the vertical distributions of larval
fishes is crucial to full understanding of their biology
and to understanding the results of ichthyoplankton
surveys (Ahlstrom 1959; Kendall and Naplin 1981).
The interaction between vertical distributions and
physical processes can have important effects on
onshore-offshore distributions of planktonic
organisms in upwelling regions such as the coastal
northeastern Pacific (Peterson et al. 1979; Parrish
etal. 1981; Wroblewski 1982; Rothlisberg et al. 1983).
Near-surface distribution, for example, may result
in shoreward transport in slicks associated with in-
ternal waves (Shanks 1983). In the coastal region off
Oregon, the only information on larval fish vertical
distribution is a comparison between abundances of
Paro'phrys vetultcs and Isopsetta isolepis larvae from
neuston and oblique bongo net tows (Laroche and
Richardson 1979) and one 24-h study with stratified
samples taken by bongo nets without opening-closing
devices (Richardson and Pearcy 1977). With the ex-
ceptions of the classic study by Ahlstrom (1959) and
recent studies by Brewer et al. (1981) and Schlotter-
beck and Connally (1982), little else is known about
the vertical distribution of larval fishes in north-
eastern Pacific coastal waters. In this paper, we pre-
sent information on vertical distributions of larval
fishes off Oregon.
'College of Oceanography and Marine Science Center, Oregon
State University, Newport, OR; present address: Southwest
Fisheries Center Honolulu Laboratory, National Marine Fisheries
Service, NOAA, P.O. Box 3830, Honolulu, HI 96812.
^College of Oceanography and Marine Science Center, Oregon
State University, Newport, OR; present address; Section of Fishes,
Los Angeles County Museum of Natural History, 900 Exposition
Boulevard, Los Angeles, CA 90007.
METHODS
Six series of samples were collected in 1982, four
during daylight (30 April, 14 May, 2 and 13 July) and
two during night (2 and 6-7 July). The first two series
(30 April, 14 May) were taken at station NHIO, 10
nmi (18.5 km) off Newport, OR, on the Newport
hydroline (lat. 44°40'N; Fig. 1). All others were col-
lected at NHS (9.2 km offshore). Each sample series
consisted of a variable number of tows at discrete
depth strata from the surface to within about 4 m
of the bottom (Tkble 1).
Tows were stepped oblique in five intervals of 3
min each, resulting in a total sampling time of 15
min in each 5 or 10 m depth stratum. The sampler
was an opening-closing lUcker trawl (Clarke 1969)
with three nets and a double-release mechanism
operated by messengers. The nets were 0.505 mm
mesh (Nitex^) with a 1 m^ mouth; all tows were at
a wire angle of 45° at approximate tow speeds from
0.9 to 1.1 m/s. At this angle, effective mouth area
of the net is 0.71 m^. An uncontaminated, discrete
depth sample was collected in the second net by
lowering the trawl with the first net open, opening
the second net for the desired sampling time, and
retrieving the trawl with the third net open. Water
volumes filtered were estimated with General
Oceanics flowmeters mounted in the center of each
net. Volumes of water filtered usually ranged be-
tween 250 and 450 m^/sampla Temperature and
salinity data were collected throughout the water col-
umn on each cruise using Niskin bottles to collect
^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Manuscript accepted January 1985.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
611-9l|
FISHERY BULLETIN: VOL. 83, NO. 4
124'
I I'
W
440
45'N
440
30'
440
45' N
44
30
. N
124
II '
• W
Figure L— Locations of the sampling conducted during the present study. NH5 and NHIO indicate
the stations used.
Table 1.— Number of tows per depth stratum with total volumes filtered. (Asterisk indicates that for subsequent
analysis the NHIO day sample In the two deepest categories were combined with the 50-60 m stratum.) Sample
times were as follows: Day— 4/30, 1018-1547; 5/14, 0808-1600; 7/2, 0608-0907; 7/13, 0554-1048; night— 7/2,
0016-0514, 7/6-7/7, 2330-0410.
Day
Night
NHIO
NHS
Total volume
filtered
NH5
Depth
filtered
7/6-
filtered
(m)
4/30
5/14
(m3)
7/2
7/13
(m3)
7/2
7/7
(m3)
0-5
2
2
1,682.7
2
2
1,392.6
2
2
1 ,574.8
5-10
2
2
1,783.7
2
2
1,451.2
2
2
1,575.7
10-20
2
2
1,595.7
2
862.9
2
2
1,292.9
20-30
2
2
1 ,796.7
2
929.3
2
2
1,237.6
30-40
1
2
1,415.8
2
920.5
1
2
1,184.0
40-50
1
2
1,488.1
2
920.9
1
2
1,034.8
50-60
1
2
1,891.2
2
671.3
1
1
808.3
60-70*
1
1
930.0
—
—
—
—
—
—
70-80*
—
1
704.8
—
—
—
—
—
—
612
BOEHLERT ET AL.: VERTICAL DISTRIBUTION OF ICHTHYOPLANKTON
water samples at 5 to 10 m intervals or using a self-
contained Applied Microsystems CTD-12. The
salinities of water bottle samples were determined
in the laboratory using a Guideline 8400 autosali-
nometer. The CTD salinities from 13 July were not
used because of suspected machine malfunction. The
CTD temperatures from 13 July agreed with sur-
face bucket temperatures and were used in our study.
Plankton samples were preserved at sea in 10%
buffered Formalin. Samples were sorted for fish lar-
vae in the laboratory using a dissecting microscope.
Larvae were identified to the lowest possible taxon,
measured (standard length), and stored in 5% buf-
fered Formalin.
Larval abundances were calculated as number per
1,000 m'* for each tow. The six sampling series were
combined into three data sets, spring daytime
samples (30 April and 14 May, NHIO), summer day-
time (2 and 13 July, NHS), and summer nighttime
(2 and 6-7 July NHS). In April and May the salinity
profiles closely paralleled each other, with lower
salinity at the surface, 30.S-31.0"/„o, than in deeper
water, where salinities gradually increased to about
33-34°/oo (Fig. 2a). Water temperatures above 50 m
April 30
3iO
33J
34.0
0
5
10
20-
30-
■C 40-
o.
SO-
SO
70-
April 30
May 14
Salinity (%o)
"~1 1 1 1 1 1 1 1
7.0 e.O 9.0 10.0 1 1.0 12.0 13.0 14.0 15.0
Temperature ('O
Q.
O
0-
5-
10-
20'
30-
40-
50-
60-
70-
July 13
'\ 7 July 2
30^
I
31/)
T
-r
31.5 32.0 32.5
Salinity (%o)
I
33.0
— I
3i5
—I
34.0
o^
5
10
20
30
^ 40
Q.
50-
60
70-
~1 1 1 1 1 1 1 1
7.0 8.0 9.0 10.0 II.O I2X) liO 14.0 liO
Temperature CO
Figure 2.— Salinity and temperature profiles during the collections, a. Salinity profiles during the spring collections, b. Spring temperature
profiles, c Summer salinity profiles, d. Summer temperature profiles.
613
FISHERY BULLETIN: VOL. 83, NO. 4
in April and May were about 9°-ll°C (Fig. 2b). No
thermocline was present. Thus, hydrographic
regimes support grouping April and May samples
together. Temperature and salinity profiles in April
and May were typical for the winter Oregon
hydrographic regime prior to the onset of late spring-
early summer upwelling (Huyer 1977).
In July the salinity and temperature profiles dif-
fered from those in April and May (Figs. 2c, d).
Salinities were more uniform in summer than spring
throughout the water column, ranging from 32.07oo
at the surface to 33.4"/u„ below about 20 m (Fig. 2c).
The temperature gradient in July was greater than
in April and May due to warmer surface waters (Fig.
2d). Surface temperatures ranged from 12.8° to
14.6°C, decreasing with depth to about 8.2°-9.6°C at
40 m. A thermocline was present at about 10-20 m.
Temperature and salinity profiles in July were typical
of the summer Oregon hydrographic regime (Huyer
1977). Surface temperatures suggest that samples
were not taken during active upwelling.
RESULTS
In this study, a total volume of 29,145.5 m^ was
filtered and 1,007 larvae, representing 33 taxa, were
enumerated from 75 discrete depth tows. Larvae
were most abundant in summer, with an abundance
peak 10-30 m deep during daytime and 20-30 m deep
during nighttime (Fig. 3). In spring, larvae were
distributed relatively uniformly throughout the
water column below 5 m with small abundance peaks
at 10-20 and 40-50 m. During daytime in both spring
and summer, larvae were least abundant at the sur-
face (0-5 m), although abundance at the surface in-
creased at night. The depth distribution at night also
differed in having a secondary abundance peak near
the bottom (50-60 m) and greater overall larval abun-
dance than during the day.
The larval fish species were categorized as coastal
(most abundance 2-28 km from the coast, see Tkbles
2, 3, and 4), or offshore (most abundant 37-111 km
from the coast, see Ikbles 5, 6, and 7), according to
larval assemblages described by Richardson and
Pearcy (1977). Most larvae in this study were of the
coastal assemblage because samples were collected
at NH5 and NHIO (9.2 and 18.5 km from the coast,
respectively). The spawning seasons of the dominant
species off Oregon are discussed in Mundy (1984);
most of the fall-winter spawning species were not
represented in this study. Since many species were
not abundant enough to demonstrate trends, only
the dominant species will be discussed below.
Coastal Assemblage
Gadus macrocephalus, Microgadus proximtis,
Isopsetta isolepis, and Psettichthys melanostictiis lar-
vae were abundant in all three sampling periods
(Tkbles 2, 3, 4, Fig. 4). Gadus macrocephalus larvae
were most abundant during the day at 20-30 m in
both spring and summer, but were very abundant
in the deepest stratum (below 50 m) in night samples
(Fig. 4). Microgadus proximvs larvae do not show
as clear a trend, but were most abundant in deeper
water during summer, particularly at nighttime In
spring they were distributed throughout the water
column. Isopsetta isolepis and P. melanostictus were
also most abundant in nighttime samples. More /.
isolepis larvae were found at 10-20 m in spring,
whereas in summer they were collected throughout
the water column, with abundance peaks near the
bottom. Psettichthys melanostictus larvae were more
abundant in summer than spring samples. During
daytime in summer, P. melanostictus were most
abundant below 10 m, whereas at nighttime,
although found throughtout the water column, they
were most abundant in waters shallower than 10 m
(Fig. 4).
Seasonal abundance changes were observed for
0 -I
5
10
20
-^ 30
E
a.
O 40
50
4.4
4>--.,
3.3,3
• .4 Day, Spring
• • Day, Summer
•— — • Nig hi, Summer
H
I — I — I — I — I — I — I — I — I —
0 10 20 30 40 50 60 70 80 90
Mean Abundance (No./IOOOm^)
Figure 3.— Overall larval abundance (larvae per 1,000 m^) for all
collections. Numbers adjacent to data points indicate the number
of samples taken.
614
BOEHLERT ET AL.: VERTICAL DISTRIBUTION OF ICHTHYOPLANKTON
Table 2.— Mean abundances (number per 1,000 m^) for coastal larval species from spring (day only)
samples.
Depth (m)
Species 0-5 5-10 10-20 20-30 30-40 40-50 >50 Mean
Clupeidae
Clupea harengus — — 1.76 2.36 1.25 0.75 — 0.87
Osmeridae
Undetermined spp. — 1.85 5.02 1.22 1.51 1.16 0.23 1.57
Gadidae
Gadus macrocephalus 1.14 0.53 5.69 7.59 2.91 — 0.89 2.68
Microgadus proximus 1.13 2.04 3.87 2.97 0.73 2.95 0.45 2.02
Cottidae
Artedius fenestralis — — _____ _
Artedius harringtonl — — — — _ 0.75 0.41 0.17
Artedius meanyi — — — — — — 0.44 0.06
Clinocottus embryum — — — — — — — —
Cottus asper — 0.53 _____ o.08
Radulinus asprellus — — — — — _ 2.60 0.37
Agonidae
Odontopyxis trispinosa — — — — — _ 0.23 0.03
Cyclopteridae spp. 1 _ _ _ o.74 2.29 3.64 0.45 1.02
Undetermined spp. — — — 0.47 _ _ — 0.07
Bathymasteridae
Ronquilus jordani — 0.59 — — — — — 0.08
Ptilichthyidae
Ptilichthys goodei — — 0.94 — — — — 0.13
Bothidae
Citharichthys stigmaeus _ _ _ _ o.73 — 0.87 0.23
Pleuronectidae
Isopsetta isolepis 0.49 1.79 7.78 2.86 — 1.29 0.66 2.12
Lepidopsetta bilineata — 0.59 0.94 _ _ _ _ o.22
Parophrys vetulus — 0.59 1.76 — — — 0.45 0.40
Psettichthys melanostictus 1.48 5.46 5.58 — 0.73 — 0.44 1.96
Table 3. — Mean abundances (number per 1,000 m^) for coastal larval species from summer day samples.
Depth (m)
Species 0-5 5-10 10-20 20-30 30-40 40-50 >50 Mean
Clupeidae
Clupea harengus — — _____ _
Osmeridae
Undetermined spp. — — _ _ _ _ 3 59 0.53
Gadidae
Gadus macrocephalus — — 1.38 12.01 1.08 1.09 — 2.22
Microgadus proximus — — 2.01 1.01 — 3.28 3.49 1.40
Cottidae
Artedius fenestralis — — 1.00 1.15 — — — 0.31
Artedius harringtonl — 0.68 4.54 3.30 2.18 2.19 3.39 2.33
Artedius meanyi — — 3.38 2.02 1.10 — — 0.93
Clinocottus embryum — — — — — — — —
Cottus asper — 0.53 _____ 0.O8
Radulinus asprellus _______ _
Agonidae
Odontopyxis trispinosa — — — 1.01 — — — 0.14
Cyclopteridae spp. 1 — — — 2.22 2.16 — — 0.63
Undetermined spp. — — 2.16 4.18 1,08 2.18 6.05 2.24
Bathymasteridae
Ronquilus jordani 0.63 0.70 2.01 1.01— — — 0.62
Ptilichthyidae
Ptilichthys goodei — — — — — — — —
Bothidae
Citharichthys stigmaeus — — 1.00 — — — — 0.14
Pleuronectidae
Isopsetta isolepis — — 2.07 1 .01 2.20 — 4.82 1 .44
Lepidopsetta bilineata — ______ _
Parophrys vetulus — — — — — — — _
Psettichthys melanostictus 0.98 2.03 22.98 7.48 3.24 3.26 11.18 7.31
615
FISHERY BULLETIN: VOL. 83, NO. 4
Table 4.— Mean abundances (number per 1,000 m^) for coastal larval species from summer night
samples.
Species
Clupeidae
Clupea harengus
Osmeridae
Undetermined spp.
Gadidae
Gadus macrocephalus
MIcrogadus proximus
Cottidae
Artedius fenestralis
Artedius harringtoni
Artedius meanyi
Clinocottus embryum
Cottus asper
Radulinus asprellus
Agonidae
Odontopyxis trispinosa
Cyclopteridae spp. 1
Undetermined spp.
Bathymasteridae
Ronquilus jordani
Ptilichthyidae
Ptilichthys goodei
Botfiidae
Citharichthys stigmaeus
Pleuronectidae
Isopsetta isolepis
Lepidopsetta bilineata
Parophrys vetulus
Psettichthys melanostictus
Depth (m)
0-5 5-10 10-20 20-30 30-40 40-50 >50
Mean
— 4.42 15.15 4.56 — 0.75 1.12 3.71
— — — 0.82 3.16 8.11 22.98 5.01
0.66 0.61 — 4.66 1.95 3.29 6.91 2.58
3.20 — 0.78 1.57 — 0.75 2.60 1.27
1.35 4.41 5.44 11.30 0.73 1.27 1.40 3.70
0.66 4.48 0.71 4.12 0.74 1.01 3.62 2.19
0.66 — — ____ 0.09
— — — — — — 2.50 0.36
— — 0,77 0.79 — — — 0.22
— — — 3.96 0.73 — 4.74 1.35
— — 0.71 1.70 — 1.27 — 0.53
— — — 0.74 0.74 — — 0.21
— 2.57 1.63 6.50 2.64 10.90 1.12 3.62
0.66 — 0.71 — _ _ _ 0.20
24.63 31.37 13.65 18.86 7.78 6.07 6.91 15.61
to -P
20 -I
50 -
40 -1
SO '
Spring- Ooy
Summer - Doy Summer- Night
60
0
S
10
f 30
a.
e 40
O
50 -
60
Godm
moerocepholm
20
I >
10 20
p Pselllchlhvi
melano3ticlu>
I I
20 40
20 40
0
S -
10
20 -
30 -
40
50 -
60
I Lyopselto
eiilis
I 1
20 40 20 40 20
Abundonce (No./IOOOm^)
40
Figure 4.— Vertical abundance patterns of the three most abun-
dant taxa {Gadus niacrocephaltus, Psettichthys melanostictus,
and Lyopsetta exilis) during the three sampling periods.
616
Artedius and cyclopterid species. Artedius
fenestralis, A. harringtoni, and A. meanyi were
taken almost exclusively in the summer sampling
period. All species were most abundant in nighttime
samples. During the day, A. harringtoni larvae were
distributed relatively uniformly throughout the
water column from about 10 to 60 m, whereas at
night most larvae were taken from the 5-30 m depth
strata. Most cyclopterid larvae collected in spring
were the larval type referred to as Cyclopteridae spp.
1 by Richardson and Pearcy (1977). Other cyclopterid
species were more abundant in summer. Most
cyclopterid larvae were collected below 20 m during
both night and day, and in summer were abundant
at the deepest sampling depths.
Osmerid larvae of undetermined species had a
unique distribution pattern. They were abundant
during spring, rare during summer daytime samples,
and most abundant during summer nighttime
samples. During both spring and summer, larvae
were most abundant at the 10-20 m depth stratum.
Offshore Assemblage
Spring to summer differences in abundance pat-
terns were more distinct for offshore larval species
as compared with coastal species (Tkbles 5, 6, 7).
BOEHLERT ET AL.: VERTICAL DISTRIBUTION OF ICHTHYOPLANKTON
Table 5.— Mean abundances (number per 1,000 m^) for offshore larval species from spring (day only)
samples.
Depth (m)
Species
0-5 5-10 10-20 20-30 30-40 40-50 >50
Mean
Offshore
Engraulidae
Engraulis mordax
Bathylagidae
Bathylagus ochotensis
Bathylagus pacificus
Myctophidae
Protomyctophum crockeri
Protomyctophum thompsoni
Stenobrachius leucopsarus
Bythitldae
Brosmophycis marginata
Scorpaenidae
Sebastes spp.
Bothidae
Citharichthys sordidus
Pleuronectidae
Glyptocephalus zachirus
Lyopsetta exilis
Coastal-Offshore
Pleuronectidae
Hippoglossoides elassodon
— — 0.56 — 0.78 7.28 0.87 1.36
— — — — — — 0.22 0.03
— — — — — 0.75 — 0.11
— — — — — 1.74 1.19 0.42
0.49 6.79 2.76 0.47 — — — 1.50
— 2.73 1.06 1.49 — — — 0.75
— — 1.06 — — —
— — — — 11.27 14.9
1.49 — —
8.56
0.15
4.96
0.21
Table 6.— Mean abundances (number per 1,000 m^) for offshore larval species from summer day
samples.
Depth (m)
Species
0-5 5-10 10-20 20-30 30-40 40-50 >50 Mean
Offshore
Engraulidae
Engraulis mordax
Bathylagidae
Bathylagus ochotensis
Bathylagus pacificus
Myctophidae
Protomyctophum crockeri
Protomyctophum thompsoni
Stenobrachius leucopsarus
Bythitidae
Brosmophycis marginata
Scorpaenidae
Sebastes spp.
Bothidae
Citharichthys sordidus
Pleuronectidae
Glyptocephalus zachirus
Lyopsetta exilis
Coastal-Offshore
Pleuronectidae
Hippoglossoides elassodon
0.98 2.13 — — — — — 0.44
1.49 0.73 _____ 0.32
— 0.65 3.03 1.08 1.10 — — 0.84
— 0.73 _____ 0.10
— 2.11 19.55 4.52 _ _ _ 3.74
— — 10.03 11.53 4.38 2.13 — 4.01
1.10 —
0.16
Only Sebastes and Lyopsetta exilis larvae were abun-
dant in all three sampling periods. Sebastes larvae
were most abundant in nighttime samples, when
they were mainly collected in shallow water (0-20 m).
In both spring and summer daytime samples they
were also in relatively shallow waters (5-40 m),
although they were not abundant at the shallowest
stratum (0-5 m). During day, L. exilis larvae were
distributed in deeper water, particularly in spring,
when all larvae were collected below 30 m (Fig. 3).
At night, most L. exilis were shallower, between 5
and 30 m.
Two species, Bathylagus ochotensis and Steno-
brachius leucopsarus, were collected only in spring
samples. These two species were predominantly col-
lected at different depths with B. ochotensis found
617
FISHERY BULLETIN: VOL. 83, NO. 4
Table
7.-
-Mean abundances
(number
per 1,000 m^)
samples
for offshore larval
spec
les from
summer
night
Species
Depth (m)
0-5 5-10
10-20 20-30 30-40
40-50
>50
Mean
Offshore
Engraulidae
Engraulis mordax
Bathylagidae
Bathylagus ochotensis
Bathylagus pacificus
Myctophidae
Protomyctophum crockeri
Protomyctophum thompsoni
Stenobrachius leucopsarus
Bythitidae
Brosmophycis marginata
Scorpaenidae
Sebastes spp.
Bothidae
Citharichthys sordidus
Pleuronectidae
Glyptocephalus zachirus
Lyopsetta exilis
Coastal-Offshore
Pleuronectidae
Hippoglossoides elassodon
4.09 3.76
1.12
3.86 0.68 2.38 0.82 — — 1.12 1.27
— — 0.78 — 0.74 1.27 10.27 1.87
0.66 0.68 0.77 0.91 _ — _ 0.43
— 8.28 15.05 32.99 — 3.53 1.12 8.71
— — 0.71 —
— 1.12 0.26
in deeper water (40-50 m) and S. leucopsarus in
shallow water (5-20 m).
Two species of larval flatfishes and Engraulis mor-
dax were collected only in summer samples. Glypto-
cephalus zachirus were most abundant during day
at 5-30 m, and Citharichthys sordidus at night below
50 m. Engraulis mordax larvae were collected only
above 10 m. Engraulis mordax were most abundant
at night when more than half were in very shallow
waters, <5 m. During the day, more E. mordax were
found at 5-10 m than at 0-5 m.
A relationship between larval size and depth was
not evident for any species. Because of the low abun-
dances of larvae, however, this relationship could not
be adequately considered for most species. A change
in larval size with season was demonstrated for the
most abundant species (Tkble 8), with mean larval
standard lengths of all species greater in summer
than in spring samples. There were no obvious dif-
ferences between the size of larvae caught in day and
night summer samples.
DISCUSSION
Peak abundances of all taxa combined occurred at
10-30 m on all sample dates (Fig. 3) and character-
ized several individual taxa during the day, including
Clupea harengus, Osmeridae, Gadus macrocephalus,
Sebastes spp., and Parophrys vetulus, as well as
Lyopsetta exilis and Psettichthys mslanostictus in the
summer. The 10-30 m depth range bracketed the
lower boundary of the seasonal thermocline in July,
although no thermocline was present in April-May
(Fig. 2). This trend for the peak abundance of fish
larvae to be centered near the thermocline is similar
to that found in other regions (Ahlstrom 1959; MOler
et al. 1963; Kendall and Naplin 1981).
The trend for most larvae to be found in midwater
was similar to that described by Brewer et al. (1981)
for their deepest stations off southern California. We
did not find large concentrations of larvae near the
bottom as they did, except at night, when gadids, cot-
tids, cyclopterids, and pleuronectids were abundant.
Our sampling gear was ineffective just above the bot-
tom as compared with the roller-equipped gear used
by Brewer et al. (1981).
Richardson and Pearcy (1977) found larvae to be
most abundant at 0-10 m and least abundant at
51-100 m during late May off Oregon. We found lar-
vae to be most abundant at 10-30 m. This difference
may be due to differences in hydrography and sta-
tion locations. Their station was 18 km offshore,
closer to the shelf break where the depth of water
was over 150 m deep. The faunal composition in each
study was also different. Richardson and Pearcy
(1977) captured more specimens of several surface-
associated taxa than we did, including large Clupea
harengus, Stenobrachius leucopsarus, Ronquilus jor-
dani, and Ammodytes hexapterus. We captured
higher densities of deeper dwelling taxa, including
gadids and cottids. Several taxa taken in both studies
had different distributions in each, including Sebastes
618
BOEHLERT ET AL: VERTICAL DISTRIBUTION OF ICHTHYOPLANKTON
Table 8. — Ranges and mean standard lengths (mm) for dominant fish larvae. N = number of larvae; Min. =
minimum; Max. = maximum.
Spring: Day
Summer: Day
Summer: Night
Species
N
Min.
Mean
Max.
N
Min.
Mean
Max.
N
Min.
Mean
Max.
Coastal
Clupea harengus
10
7
8.2
9
0
—
—
—
0
—
—
—
Osmerid
17
3
7.1
17
3
29
33.1
38
35
23
31.8
40
Gadus macrocephalus
29
8
10.8
20
17
9
13.6
17
28
9
13.3
19
Microgadus proximus
22
6
10.9
19
9
11
21.3
36
18
6
18.4
33
Artedius fenestralis
0
—
—
—
2
11
12.0
13
8
10
11.6
13
Artedius harringtoni
2
6
6.5
7
15
5
8.2
13
33
5
8.6
14
Artedius meanyl
1
—
4.9
—
6
7
9.9
16
19
7
9.4
18
Radulinus asprellus
10
6
7.6
9
0
—
—
—
0
—
—
—
Liparid type 1
12
4
5.7
6
4
3
3.1
3
2
3
3.5
4
Liparid unknown
1
—
10.2
—
14
5
16.7
25
10
15
20.4
23
Ronquilus jordani
1
—
6.6
—
5
22
27.1
33
5
24
24.1
25
Isopsetta isolepis
22
4
8.9
21
9
10
20.0
23
28
7
16.1
23
Psettichthys
melanostictus
—
3
7.0
22
41
9
20.0
27
150
8
20.8
28
Offshore
Engraulis mordax
0
—
—
—
4
12
13.5
15
12
7
13.1
16
Bathylagus ochotensis
16
5
8.1
19
0
—
—
—
0
—
—
—
Stenobrachius
leucopsarus
19
3
5.2
9
0
—
—
—
0
—
—
—
Sebastes spp.
8
4
4.7
6
6
4
14.6
18
12
12
16.0
18
Citharichthys sordidus
0
—
—
—
1
—
20.5
—
11
17
37.8
40
Glyptocephalus zachirus
2
13
25
37
22
14
29.9
39
4
22
34.5
50
Lyopsetta exilis
71
4
8.4
15
27
11
13.2
16
79
7
12.2
20
spp., Cyclopteridae spp. 1, and Isopsetta isolepis.
These differences indicate the need for more exten-
sive sampling before the variability of vertical
distributions off Oregon can be understood, par-
ticularly as they relate to hydrographic condi-
tions.
We found Engraulis mordax larvae entirely at 0-10
m. Brewer et al. (1981) found greater concentrations
of Engraulis below 10 m, while Ahlstrom (1959)
found Engraulis to be concentrated in the upper 23
m with some specimens occurring to 105 m. Off
Oregon, Engraulis larvae are found concentrated at
0-20 m (Richardson 1973), in association with the
Columbia River plume, a lens of warm, low salinity
water usually 20-40 m deep (Richardson 1980). Our
limited data suggest that Engraulis mordax larvae
occur at depths that would place them within the
plume, rather than beneath it or at its boundary. The
vertical distribution suggests restriction to the
warmest part of the water column (Fig. 2d); north-
ern anchovies rarely spawn in waters with surface
temperatures below 14°C (Lasker et al. 1981).
The seasonal differences in species composition be-
tween the April-May and July samples were those
that would be expected in samples from winter and
summer hydrographic regimes, except that Artedius
fenestralis and A. meanyi have been taken in April
and May of other years (Mundy 1984). The presence
of Clupea harengus, Radulinus asprellus, myctophid,
and bathylagid larvae only in April-May, during a
winter hydrographic regime, is expected from
previous studies (Richardson and Pearcy 1977;
Mundy 1984).
Studies of day/night differences in the distribution
of fish larvae are confounded by daytime avoidance
of nets by larvae (Ahlstrom 1959). Daytime avoidance
of nets is suggested in our study by the greater
numbers of larvae taken during the night than day
at all but two depth strata. The lack of length dif-
ferences between larvae caught in day and night,
however, and the fact that no taxa were taken only
in night samples during July suggests that diurnal
net avoidance was not related to taxon or size The
same comparisons with 70 cm bongo net samples
(Richardson and Pearcy 1977) suggest that diurnal
avoidance by large larvae was greater for bongo nets
than for the Tlicker trawl.
Evidence for vertical migration exists for several
species in this study (Tkbles 3, 4, 6, 7). Psettichthys
melanostictus abundance in surface waters (0-10 m)
increased greatly at night (Fig. 4). Engraulis mor-
dax were most abundant at 5-10 m than 0-5 m dur-
ing the day, but more evenly distributed at night.
This could be due either to vertical migration or net
avoidance in the shallowest stratum during the day.
Ahlstrom (1959), however, presented evidence for
negative phototaxis by anchovy larvae, and Hunter
and Sanchez (1976) demonstrated nighttime migra-
tion to the surface in larvae larger than 10 mm SL.
Thus larvae migrate upwards at night, but are con-
619
strained to shallower water in the day as compared
with the southern subpopulation.
The clearest case of vertical migration was that
of Gadus macrocephalus (Ihbles 3, 4), which was
most abundant at 20-30 m in the day and deeper than
50 m at night. The migration of this species was
primarily responsible for the increased total abun-
dance of larvae near the bottom at night (Fig. 3). This
pattern of movement is similar to that observed for
larval Ammodytes personatics by Yamashita et al.
(1985), who suggested that this reverse vertical
migration allowed feeding in daytime and avoidance
of migrating predators at night. This nocturnal de-
scent, not previously reported for Gadus larvae,
should be confirmed with further sampling. Gadus
morhua larvae 3.8-4.9 mm long move from deeper
water in the day to 0-2 m at night, and descend in
the water column with growth (Hardy 1978). Lar-
vae of another gadid, Melanogrammus aeglefinu^,
are most common in the thermocline and their depth
of greatest abundance fluctuates as the thermocline
depth changes with rotary tidal currents, causing oc-
casional descent in the water column at night (Miller
et al. 1963).
Offshore taxa in Oregon coastal waters should oc-
cur in greatest numbers during onshore surface
water transport during winter and early spring. This
was true in our study for the mesopelagic Myc-
tophidae and Bathylagidae, but not for other offshore
assemblage taxa (Tkbles 5, 6, 7). Almost all of the
bathylagid and myctophid larvae except Steno-
brachiv^ leucopsaru^ were found below 30 m.
Ahlstrom's (1959) work confirms these general
distributions; he found most larvae of the genera
taken in this study (Electrona = Protomyctophum;
Laynpanyctus = Stenobrachiu^) at depths >56 m,
beneath the thermocline, except Stenobrackius. He
found Stenobrachius to have the shallowest distribu-
tion of all myctophid larvae in his study (0-41 m).
Richardson and Pearcy (1977) also found Steno-
brachius larvae to be in shallow waters (0-50 m) with
many at 0-10 m during the day. The distribution of
larval mesopelagic fishes, or other offshore taxa, can-
not be related to the depth of onshore transport
because virtually nothing is known about the depth
of winter onshore transport off Oregon (Peterson et
al. 1979; Huyer*). Both deep and surface dwelling
larvae of mesopelagic fishes collected in our study
appear to be transported onshore, however, sug-
gesting that transport occurs over a broad depth
range off Oregon.
*A. Huyer, Associate Professor, Oregon State University, Cor-
vallis, OR 97331, pars, commun. 29 September 1983.
FISHERY BULLETIN: VOL. 83, NO. 4
ACKNOWLEDGMENTS
This research was supported by NOAA Office of
Sea Grant, Department of Commerce, under Grant
No. NA81-D-00086. We thank M. Yoklavich, J.
Shenker, and the crew of the RV Sacajawea for
assistance in sampling. We also thank W. G. Pearcy
and H. G. Moser for reviewing the manuscript.
LITERATURE CITED
Ahlstrom, E. H.
1959. Vertical distribution of pelagic fish eggs and larvae off
California and Baja California. U.S. Fish Wildl. Serv., Fish.
Bull. 60:107-146.
Brewer, G. D., R. J. Lavenberg, and G. E. McGowan.
1981. Abundance and vertical distribution of fish eggs and
larvae in the southern California bight: June and October
1978. Rapp. R-v. Reun. Cons. int. Explor. Mer 178:165-167.
Clarke, M. R.
1969. A new midwater trawl for sampling discrete depth
horizons. J. Mar. Biol. Assoc U.K. 49:945-960.
Hardy, J. D., Jr.
1978. Family Gadidae: Gadus morhua Linnaeus, Atlantic cod.
In Development of fishes of the Mid-Atlantic Bight, an atlas
of egg, larval -i- juvenOe stages. Vol. II, p. 236-259. U.S. Dep.
Inter., Fish Wildl. Serv.
Hunter, J. R., and C. Sanchez.
1976. Diel changes in swim bladder inflation of the larvae of
the northern anchovy, Engraulis mordax. Fish. Bull., U.S.
74:847-855.
Huyer, A.
1977. Seasonal variation in temperature, salinity, and densi-
ty over the continental shelf off Oregon. Limnol. Oceanogr.
22:442-453.
Kendall, A. W., Jr., and N. A. Naplin.
1981. Diel-depth distribution of summer ichthyoplankton in
the Middle Atlantic Bight. Fish. Bull., U.S. 79:705-726.
Laroche, J. L., AND S. L. Richardson.
1979. Winter-spring abundance of larval English sole,
Parophrys vetulus, between the Columbia River and Cape
Blanco, Oregon during 1972-1975 with notes on occurrences
of three other pleuronectids. Estuarine Coastal Mar. Sci.
8:455-476.
Lasker, R., J. PelXez, and R. M. Laurs.
1981. The use of satellite infrared imagery for describing
ocean processes in relation to spawning of the northern an-
chovy Engraulis mordax. Remote Sens. Environ. 11:439-
453.
Miller, D., J. B. Colton, Jr., and R. R. Marak.
1963. A study of the vertical distribution of larval haddock.
J. Cons. Perm. Int. Explor. Mer 28:37-49.
Mundy, B. C.
1984. Yearly variation in the abundance and distribution of
fish larvae in the coastal upwelling zone off Yaquina Head,
Oregon from June 1969 to August 1972. MS Thesis, Oregon
State Univ., Corvallis, 158 p.
Parrish, R. H., C. S. Nelson, and A. Bakun.
1981. Transport mechanisms and reproductive success of
fishes in the California current. Biol. Oceanogr. 1:175-
203.
Peterson, W. T., C. B. Miller, and A. Hutchinson.
1979. Zonation and maintenance of copepod populations in the
Oregon upwelling zone Deep-Sea Res. 26A:467-494.
620
BOEHLERT ET AL.: VERTICAL DISTRIBUTION OF ICHTHYOPLANKTON
Richardson, S. L.
1973. Abundance and distribution of larval fishes in waters
off Oregon, May-October 1969, with special emphasis on the
northern anchovy, Engraulis mordax. Fish. Bull., U.S. 71:
697-711.
1980. Spawning biomass and early life of northern anchovy,
Engraulis mordax, in the northern subpopulation off Oregon
and Washington. Fish. Bull., U.S. 78:855-876.
Richardson, S. L., and W. G. Pearcy.
1977. Coastal and oceanic fish larvae in an area of upwelling
off Yaquina Bay, Oregon. Fish. Bull., U.S. 75:125-145.
ROTHLISBERG, P. C, J. A. CHURCH, AND A. M. G. FORBES.
1983. Modelling the advection of vertically migrating shrimp
larvaa J. Mar. Res. 41:511-538.
SCHLOTTERBECK, R. E., AND D. W. CONNALLY.
1982. Vertical stratification of three nearshore southern
California larval fishes Engraulis mordax, Genyonemus
lineatus, and Seriphus politus. Fish. Bull., U.S. 80:895-
902.
Shanks, A. L.
1983. Surface slicks associated with tidally forced internal
waves may transport pelagic larvae of benthic invertebrates
and fishes shoreward. Mar. Ecol. Prog. Ser. 13:311-315.
Wroblewski, J. S.
1982. Interaction of currents and vertical migration in main-
taining Calanus marshallae in the Oregon upwelling zone—
a simulation. Deep-Sea Res. 29A:665-686.
Yamashita, Y., D. Kitagawa, and T. Aoyama.
1985. Diel vertical migration and feeding rhythm of the lar-
vae of the Japanese sand-eel, Ammodytes personatus. Bull.
Jpn. Sot Sci. Fish. 51:1-5.
621
DOLPHIN HABITATS IN THE EASTERN TROPICAL PACIFIC
David W. K. Au and Wayne L. Perryman^
ABSTRACT
Research-ship surveys by the Southwest Fisheries Center provided information on the distributions of
spotted, spinner, striped, and common dolphins in the eastern tropical Pacific The main surveys were
conducted from January to March during 1976, 1977, 1979, and 1980. Two ships were used per survey,
and together they overlapped most areas in the eastern Pacific where dolphins and yellowfin tuna are
jointly fished by purse seiners.
The spatial distribution of sightings and of sighting rate of these species show a complementarity to
their patterns, although there is a broad overlap. Spotted and spinner dolphins occurred primarily in tropical
waters north of the Equator, but also in the seasonal tropical waters south of the Galapagos Islands. These
dolphins were relatively infrequent along the Equator, off Costa Rica, and northern South America. Com-
mon and striped dolphins tended to be more frequent in these same areas of less frequent spotted and
spinner dolphins.
The differences in habitats of these two species pairs can be described in oceanographic terms. Spotted
and spinner dolphins are primarily in Tropical Surface Water, centered off southern Mexico and extending
westward along lat. 10°N, where thermocline "ridging" and relatively small annual variations in surface
temperature are features. Common and striped dolphins appear to perfer equatorial and subtropical waters
with relatively large seasonal changes in surface temperature and thermocline depth and with seasonal
upwelling.
The species composition of various areas in the eastern tropical Pacific supports the contention of two
major communities. South of where spotted and spinner dolphin schools predominate (along with Risso's,
bottlenose, and rough-toothed dolphins), striped and common dolphins and also pilot whales become in-
creasingly important. Observations along the Equator also suggest a fauna different from that of the
Tropical Surface Water that is most characterized by spotted and spinner dolphins.
A trophic basis to these faunal differences is suggested by the interactions with fish and birds. Assum-
ing the birds indicate co-occurring tuna, only the spotted and spinner dolphins are commonly found with
fish. The distribution of these dolphins as they co-occur with bird flocks and tuna indicates that this inter-
specific association is confined primarily to the TVopical Surface Water and is a characteristic feature
of its epipelagic community.
The eastern tropical Pacific Ocean supports produc-
tive tuna fisheries as well as an abundant and diverse
cetacean fauna. Ibna fishermen there take advan-
tage of the fact that tuna and dolphins frequently
swim together. In the "porpoise-tuna" fishery for
yellowfin tuna, Thunnus albacares, spotted and spin-
ner dolphins, Stenella attenuata and S. longirostris,
are temporarily caught by purse seiners in order to
take the associated tuna. Striped and common
dolphins, S. coeruleoalba and Delphinus delphis, are
caught to a lesser extent for the same reason. These
dolphins suffer incidental mortality in the fishery
and, because of the resulting concern, the Southwest
Fisheries Center has been studying their populations
to better advise on their management (Smith 1983).
Learning about their habitats is one aspect of these
studies. .<■
'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, 8604 La Jolla Shores Drive, La
Jolla, CA 92038.
Perrin (1975a), using the information collected
mainly aboard tuna seiners, first showed that the
geographic distributions of spotted, spinner, and
striped dolphins in the eastern Pacific are extensive,
stretching westward from the American coasts past
long. 145°W at about lat. 10°N and also dipping
south and southwest of the Galapagos Islands. Evans
(1975) showed that the common dolphin occurs off-
shore of Central America to about long. 112°W and
also along the Equator, westward past the Galapagos
Islands. Recent summaries of available information
(Au et al. 19792; gcott 1981; Perrin et al. 1983) have
shown that the distributions of these dolphins are
even more extensive than originally perceived. In-
deed the species have been reported from localities
across the entire Pacific (Alverson 1981).
Manuscript accepted January 1985.
FISHERY BULLETIN: VOL. 83. NO. 4, 1985.
2Au, D. W. K., W. L. Perryman, and W. F Perrin. 1979. Dolphin
distribution and the relationship to environmental features in the
eastern tropical Pacific Admin. Rep. LJ-79-43, 59 p. Southwest
Fisheries Center La Jolla Laboratory, National Marine Fisheries
Service, NOAA, P.O. Box 271, La Jolla, CA 92038.
623
FISHERY BULLETIN: VOL. 83, NO. 4
The purpose of this paper is to describe the
January-March distributions of schools of spotted,
spinner, striped, and common dolphins as determin-
ed from research ship surveys. Being independent
and distinct from data collected by observers aboard
tuna seiners, these survey data enable a separate
evaluation of habitats and ecological relationships.
The distributions derived will be discussed in terms
of habitat features and interspecific associations in-
cluding those of other cetaceans, yellovvrfin tima, and
certain seabirds. We propose that tv^o major ceta-
cean communities can be recognized, centered
broadly about the tropical and about the equatorial-
subtropical surface water provinces (Fig. 1).
METHODS
The Southwest Fisheries Center conducted or par-
ticipated in 17 research cruises studying cetaceans
between 1976 and 1981. Eight major cruises were
carried out between January and March of 1976,
1977, 1979, and 1980, with the NOAA ships David
Starr Jordan and Tovmsend Cromwell. During these
surveys, schools of all cetacean species encountered
(at least 23 species in the areas of interest) were ap-
proached to allow close observation. The combined
cruise tracks of these January-March surveys form-
ed an extensive coverage of the eastern tropical
Pacific and included areas not frequently searched
by fishing vessels (Fig. 2). The latter are the
equatorial waters and areas both south of lat. 8°N
and west of long. 110°W. The cruise tracks during
any particular year were chosen to investigate cer-
tain aspects of dolphin distribution, ag., the inten-
sive surveys during 1979 off southern Mexico and
central America constituted a joint aircraft-ship
survey of the nearshore habitat. The remaining other
nine cruises were either for special studies or of ships
of opportunity. In the latter case, the ships did not
usually divert course to inspect cetacean schools that
were sighted.
Cetacean observations from a research ship were
conducted by scanning the waters ahead and to the
sides of the ship through 20 x 120 mm USN MK-3
Figure L— Surface water masses and boundaries of the tropical ocean in the eastern Pacific, based on Wyrtki's (1964a, 1967) analysis
to long. 140°W. Boundaries are a function of the 24°C surface isotherm and the TC/IO m thermocline gradient. Notice that in October
the southern boundary to the eastern tropical ocean lies mostly north of the Equator, while in March this boundary lies far to the south
so that southern subtropical waters become tropical.
624
AU and PERRYMAN: DOLPHIN HABITATS
or 25 X 150 mm Fuji binoculars, mounted both port
and starboard either on or above the flying bridge
The sighting distance to the horizon was about 7.0
and 5.5 nmi for the David Starr Jordan and Town-
send Cromwell respectively. Both ships cruised at
about 10 kn (18.5 km/h). The cetacean search-day
generally started at 0600 and ended 1800, with two
teams, or watches, alternating. In 1976 and 1977 the
watches were each 2 or 3 h long, depending on the
ship. In 1979 and 1980 they were all standardized
to 3 h. There were two experienced persons on each
watch, who alternated each hour between the port
and starboard binoculars. A third person sometimes
helped in record keeping, obtaining supplementary
data, and temporarily relieving the other watch
members. The peripheral data collected included
bathythermograms, surface temperature and salin-
ity, weather observations, sighting condition
measurements, sighting effort, and observations on
fish and birds.
When a cetacean school was sighted, its angle
relative to the ship's heading was measured and its
distance from the ship estimated. The ship then ap-
proached the school for closer observation. School
size was estimated and the species identified.
The reader is cautioned that the distributions to
be described are based upon relatively few sightings
of schools (Tkble 1) and that they pertain to the
January-March season specifically. Though the pat-
tern of sampling was widespread, the actual area
surveyed was a very small fraction of the huge area
Table 1.— Summary of school sizes for spotted, spin-
ner, striped, and common doipfiins from the January-
March research cruises of 1976, 1977, 1979, and 1980.
Arithmetic
Geom(
X
3tric
Species
n
X
s
S1
Spotted2
157
148.52
300.93
65.55
3.56
Spotted and
spinner
79
357.42
444.50
211.67
2.93
Spinner^
44
228.39
291.54
107.05
3.88
Striped
187
60.84
69.78
40.74
2.56
Common
98
261.16
484.64
108.47
3.72
Totai^
565
'Standard deviation factor for the geometric mean.
zjotal spotted dolphin schools is 157 + 79 = 236.
^Total spinner dolphin schools is 44 + 79 = 123.
"Additionally, there were 838 school sightings of unidentified
and other species of dolphins (Delphinidae) and 543 school
sightings of whales (Balaenopteridae, Ziphiidae, and
Physeteridae).
170
30'
70"
30"
Hawaiian Islands
JANUARY-MARCH R/V CRUISE TRACKS
FOR 1976, 1977, 1979, 1980
Christinas Island *
30'
170
J
Figure 2.— Cruise tracks of the January-March cruises by RV David Starr Jordan and RV Townsend Cromwell. These cruises took place
in 1976, 1977, 1979, and 1980.
625
FISHERY BULLETIN: VOL. 83, NO. 4
of the eastern Pacific The patterns of species
distribution we describe will not always be obvious.
Nevertheless there is evidence from other distribu-
tion studies, using data collected from the fishery,
that these patterns are real (Perrin et al. 1983).
The results described in this paper are based upon
our personal experiences at sea where the procedure
of investigating all cetacean schools and continuously
monitoring the physical and biotic environment
enabled the development of an ecological under-
standing of these dolphins. Continuity in these
studies was provided by the fact that on each ship
there was at least one experienced observer who par-
ticipated during all cruise years. We present our
results as an independent, research-ship based,
assessment of species distributions and habitat
areas.
RESULTS
Distribution and Relative Abundance
of Dolphin Schools
Plots of the sighting localities of schools of spot-
ted, spinner, striped, and common dolphins, obtain-
ed during the January-March research cruises, show
the geographical distributions of these species dur-
ing the northern winter season. Table 1 summarizes
the numbers and sizes of the schools which were
identified and studied. Geographic locations referred
to in the text can be found in Figure 1.
Spotted and spinner dolphins are often in mixed
schools (33.5% of spotted dolphins schools also con-
tained spinner dolphins. Table 1), and so the sight-
ings of spotted or of mixed spotted plus spinner
dolphin schools are shown together (Fig. 3). Most of
the mixed schools were encountered off southern
Mexico, where the eastern form of spinner dolphin
(Perrin 1975a, b; Perrin et al. 1977) usually accom-
panied spotted dolphins (cf. Figs. 3, 4). Mixed schools
were uncommon along the Equator, as was the spot-
ted dolphin itself, especially west of long. 110°W.
Large schools (>300 individuals) of spotted dolphin
were widely scattered, but tended to be more com-
mon off southern Mexico. Westward extensions of
distribution appeared to occur as three main lobes:
about lat. 10°n, between lat. 0° and 5°N, and be-
tween lat. 2°S and 5°S.
170°
30°
140°
— r
130°
— r-
120°
— r
70°
30°
Hawaiian Islands
\
O o°
Christmas Island *
o o
>4 . i^
A.
Marquasas Islands
O SPOTTED DOLPHIN
• SPOTTED a SPINNER DOLPHIN
o •
o °0°
Figure 3.— Distribution of spotted and spotted plus spinner dolphin schools seen during the January-March research cruises. Larger circles
indicate schools of >300 animals.
626
AU and FERRYMAN: DOLPHIN HABITATS
The spinner dolphin appears to be distributed like
the spotted dolphin, with westerly extending lobes
of distribution in similar latitudes (Fig. 4). Schools
were infrequent along the Equator, more so than
were those of spotted dolphin. The eastern spinner
was encountered frequently off southern Mexico,
where its main population center appeared to be
relatively localized. However, eastern spinner
dolphins were seen as far offshore as long. 126°W
near lat. 10°N and also nearly to the Equator within
a broad, 600 nmi coastal belt off Central America.
The whitebelly form of spinner dolphin (Perrin
1975a, b; Perrin et al. 1977) occurred in a broad
range north and south of the Equator and at the
southern and western portions of the total spinner
dolphin range Large schools (>300) were seen most-
ly off southern Mexico (eastern spinner) and south
of the Equator (whitebelly spinner).
Striped and common dolphins seem to have a
distribution pattern qualitatively different from that
of spotted and spinner dolphins (Fig. 5). A distinct
distributional lobe, consisting primarily of common
dolphins, occurred off Baja California, with exten-
sions around the Revilla Gigedo Islands (ca. lat.
19°N, long. 111°W). Between lat. 5° and 12°N, off
Central America, there was a second lobe made up
of both species. This lobe attenuated to the west
along lat. 10°N, but appeared to re-intensify past
long. 130°W. Only striped dolphins were seen in the
intermediate interval between long. 100°W and
130°W along this lobe A third lobe appeared to
originate off Peru. It merged somewhat with the
outer portions of the Central American lobe, and
then extended westward along the Equator.
Equatorial waters were frequented by both species
out to about long. 100°W, beyond which striped
dolphins apparently predominate. The striped
dolphin is the more widespread of the two species;
however, its school sizes are small (Tkble 1). Large
schools (>300) of the common dolphin occurred
within each of the three main centers of its
distribution.
The above sighting data were adjusted to show the
distributions of relative abundance of schools by cor-
recting for searching effort. Effort is calculated as
miles searched = time searched x ship speed.
Relative abundance of schools was expressed as
schools per 100 nmi searched (approximately the
170°
30°
ISO*
— T"
120»
— r
90-
80"
70°
30"
Hawaiian Itlandt
Christmas Island *
Marquasa* Islands
I I
• EASTERN SPINNER
O WHITEBELLY SPINNER
O CD O
Figure 4.— Distribution of spinner doipliin schools, eastern and whitebelly forms, seen during the January-March research cruises. Larger
circles indicate schools >300 animals.
627
FISHERY BULLETIN: VOL. 83, NO. 4
170°
30°
Hawaiian Islands
Christmas Island *
o ^o-^o'
10' -
Marqussas Islands
Figure 5.— Distribution of striped and common dolphin schools seen during the January-March research cruises. Larger circles indicate
schools >300 animals.
distance searched during 1 d). Data for days during
which the Beaufort wind force was equal to 4 (11-16
kn) for more than 50% of the time, or averaged more
than 4, were not used. Only schools sighted at
distances not more than 3 perpendicular nmi from
the ship's track and not more than 5 radial nmi dis-
tant were considered, to reduce the effects due to
distance on sightability. The latter criterion was not
applied to the 1976 cruises, because the radial
distances then were frequently overestimated. An
areal smoothing procedure that consisted of
calculating the average number of schools per 100
mi searched within sequential, overlapping 5°
squares was employed. Sequential squares were off-
set 2.5° in latitude and longitude, so that each was
wholly overlapped by 25% of the area of each of four
adjacent squares. A day's sighting rate was assign-
ed to a particular square if more than 50% of the
search effort occurred therein, and the value was
plotted at the center point of that square If the
search effort fell equally in two squares, the day's
results were assigned to both squares. These moving,
areal means of sightings per 100 nmi searched were
plotted and contoured. Contouring (and interpola-
tion) constituted a second level of areal smoothing.
The maps so generated describe the distribution
of relative abundance of species schools as surveyed
during January to March. These relative abundance
data were combined for spotted and spinner dolphins
and for striped and common dolphins, both because
these species pairs had similar distributions and
because pooling gave desirable sample sizes.
The combined spotted and spinner dolphin map
(Fig. 6) shows some patterns already noted from the
school distribution. These schools appeared relatively
more abundant off southern Mexico (mostly spotted
and eastern spinner dolphins) and again along an
east-west band just north of the Equator, especially
west of long. 105°W. Another band of greater abun-
dance occurred south of the Equator. Spotted and
spinner dolphins appeared less abundant just west
of Costa Rica, off the coast of northern South
America, and along the Equator. A weak lobe of
higher relative abundance extended west of long.
120°W broadly about lat. 10°N.
Striped and common dolphins show a relative
abundance pattern in which areas of higher density
tend to be complementary to that of spotted and
628
AU and FERRYMAN: DOLPHIN HABITATS
MO'
30'
150'
— T"
70'
30'
Hawaiian lalandt
SPOTTED AND SPINNER DOLPHIN
SCHOOLS PER 100 MILES SEARCHED
RESEARCH CRUISES JAN.-MAR.
1976. 1977, 1979, 1980
30"
I
O.S
Chrittmaa Island *
i
Figure 6— Distribution of relative abundance of spotted and spinner dolphins, inferred from data of the January-March research cruises.
Hawaiian and Marquesan sightings are not considered.
spinner dolphins (Fig. 7). Conspicuous lobes extend-
ed from off Baja California and also broadly from
the coasts of Central America and northern South
America out to and along the Equator. Within the
latter lobe, centers of higher relative abundance oc-
curred west of Nicaragua and Costa Rica and west
of the Galapagos Islands, all areas where reduced
abundance of spotted and spinner dolphins occurred.
The Galapagos area and the lobe off Baja Califor-
nia were dominated by the common dolphin (cf. Fig.
5).
Dolphins of Tropical Water and
Upwelling-Modified Water Habitats
The areas of greater frequency of spotted and spin-
ner dolphins during January-March are the typical
tropical waters of the eastern tropical Pacific. These
waters are underlain by a sharp thermocline,
generally >2°C/10 m, at depths usually much <50
m. The surface temperatures are >25°C, and the
salinities <34''/oo. Such tropical waters are defined
by Wyrtki (1966, 1967) as Tropical Surface Water
(see Fig. 1). In particular the warm "Inner Tropical"
Waters (Wyrtki 1964a) lying primarily north of the
Equator comprise the major habitat of spotted and
spinner dolphins (Fig. 6). The waters south of the
Equator, where the relative abundance of these
dolphins is also higher, are seasonally tropical, and
are therefore called southern Subtropical Surface
Water (Wyrtki 1966, 1967). These waters, occurring
approximately south of lat. 2.5° S, have surface
salinities >357oo, and during January-March
(southern summer), warm to more than 26°C over
a shallow, sharp thermocline Since spotted and spin-
ner dolphins occur there frequently, at least during
January-March, it appears that spotted and spinner
dolphins prefer all waters whose characteristics are,
or become, tropical in the eastern Pacific However
the primary habitat appears to be the "Inner"
Tropical Waters north of the Equator.
In contrast striped and common dolphins appear
to prefer waters with more variable conditions dur-
ing January-March. Their most important habitat ap-
pears to be broadly centered about equatorial waters
(Fig. 7). This band of distribution extends into the
central Pacific along the Equator. In the east it
broadens widely to include Tropical Water off Cen-
629
FISHERY BULLETIN: VOL. 83. NO. 4
tral America and Subtropical Water off Peru. The
equatorial distribution is in Equatorial Surface
Water (Wyrtki 1966, 1967), a transitional water mass
straddling the Equator and characterized by
salinities between 34 and 35"/oo, upwelling, and a
relatively weak thermoclina These waters are
markedly cooled from June to December (southern
winter-spring) by increased upwelling and by advec-
tion from the Peru Current. In the Subtropical Water
habitats of striped and common dolphins, both off
Peru and Baja California, there are also large
seasonal changes in temperature structure and ef-
fects from upwelling. Finally the Tropical Water
habitat in the Central American Bight is notably
variable (below).
The waters we call the "Central American Bight"
(roughly, the near coastal waters from Guatemala
to Ecuador) constitute the most important area of
overlap for spotted, spinner, striped, and common
dolphins, but this overlap is not balanced among the
species. These waters are tropical, but they are the
most variable within the Tropical Surface Water pro-
vince The Equatorial Countercurrent, flowing
eastward between lat. 4°N and 10°N, terminates and
turns there, creating a complex circulation. The an-
nual north-south migration in these latitudes of the
Intertropical Convergence Zone, where north and
south trade winds meet, bring southerly winds, rain,
reduced salinity, and an intensified Countercurrent
during the second half of the year (Bennett 1966;
Wyrtki 1967, 1974; Forsebergh 1969). Later during
the northern winter (January-March), northeaster-
ly winds blow across Central America from the
Atlantic, producing coastal upwelling, wind stir-
ring, and more complex temperature patterns. The
Costa Rica Dome, a localized, offshore upwelling
at about lat. 8°N, long. 90°W (Wyrtki 1964b),
also may be seasonally intensified (Hofmann et al.
1981).
These variable Central American Bight waters ap-
pear to have more abundant schools of striped and
common dolphins than of spotted and spinner
dolphins (cf. Figs. 3-7). It seems that all areas with
greater concentration of striped and common
dolphins have highly variable oceanographic features
that are "upwelling-modified".
In spite of the rather strong overlap in distribu-
tion among the four dolphin species in the Central
America Bight, the biogeographic distinction, in-
cluding the relationships to environment, between
170'
30"
160*
— r-
1«0'
— r
130*
— I—
70'
30'
20-
Chriatmat Island *
COMMON AND STRIPED DOLPHIN
SCHOOLS PER 100 MILES SEARCHED
RESEARCH CRUISES JAN. -MAR.
1976, 1977, 1979, 1980
/
Figure 7.— Distribution of relative abundance of striped and common dolphins, inferred from data of the January-March research cruises.
630
AU and FERRYMAN: DOLPHIN HABITATS
the spotted and spinner dolphins of the Tropical
Water and the striped and common dolphins of the
Upwelling-Modified Water may be quite apparent.
This was the case during the intensive winter surveys
of 1979 in the Central American Bight, shown in
Figure 8. Superimposed in the figure are contours
of the 20°C isotherm depth (essentially the ther-
mocline depth) which were obtained from expendable
bathythermograph probes dropped at 30-60 mi in-
tervals (55.6-111.1 km). Notice that spotted and spin-
ner dolphins were encountered mainly off southern
Mexico, where the deeper 20°C isotherms indicated
the occurrence of a large surface lens of warm water.
The warmest surface waters in the eastern tropical
Pacific normally occur in this area; the thermocline
gradient is weaker, and the annual variation in sur-
face temperature is relatively small (Wyrtki 1964a).
In the more variable tropical waters of the Central
American Bight, where the thermocline had shoal-
ed or ridged to <60 m, both these species were seen
too. However, striped and common dolphin schools
predominated, especially near the shallower iso-
therms that mark the location of the Costa Rica
Dome Finally the equatorial distribution of primar-
ily striped and common dolphins was evident. The
sampling suggested that Subtropical Waters south
of the Galapagos Islands were probably also impor-
tant to these latter two species. A 1977 aerial survey
of cetaceans in these waters off Central America
(SWFC 1977'^) obtained results similar to those just
described.
Though there appear to be large-scale geographic
differences in the habitats of spotted and spinner
dolphins and of striped and common dolphins, there
was no evidence of negative association among these
species. The frequency of days in the Central
American Bight, both in 1979 and 1980, with dif-
ferent combinations of these species encountered,
are summarized in Tkble 2. There was no evidence,
using chi-square contingency tests for association
among spotted and/or spinner dolphins and striped
or common dolphins, that the species were not oc-
curring independently on any particular day.
Our contention that spotted and spinner dolphins
and striped and common dolphins differentially in-
habit waters of different oceanographic characteris-
^Southwest Fisheries Center (SWFC). 1977. Aerial survey trip
report January - June 1977. Admin. Rep. No. LJ-78-01, 73 p.
Soutliwest Fisheries Center La Jolla Laboratory, National Marine
Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA 92038.
120
30°
110"
100°
90°
80°
20<
10°
o SPOTTED OB SPINNER DOLPHIN
• STRIPED OR COMMON DOLPHIN
— DEPTH OF 20° C ISOTHERM (M)
10°
120°
70°
-130°
20'
- 10°
SOUTH
AMERICA
10'
110°
100°
90°
80°
70°
Figure 8.— Distribution of dolphin schools by species type in the Central American Bight, with
reference to the depth of the 20°C isotherm. Data are from the January-March cruises of 1979.
631
FISHERY BULLETIN: VOL. 83, No. 4
Table 2.— Number of days according to combinations of four species of dolphins that were encountered
in the Central American Bight.
Spotted and/or
spinner
Striped
Common
With
With
With
With
None of
Year
Area'
Alone
striped
common
striped
+ common
Alone
common
Alone
these spp.
1979
N
17
2
0
0
1
1
1
6
S
6
7
0
4
6
1
6
8
1980
N
9
2
0
0
0
0
0
0
S
5
5
1
4
6
3
3
7
'Northern (N) and southern (S) areas are partitioned to illustrate species differences by area; the dividing line is perpen-
dicular to the coast at lat. 16°N.
tics is supported by physical environmental measure-
ments. The data indicated a species differential with
respect to waters with temperature >25°C and
salinities <34.5''/oo, and waters of <25°C and
>34.5%o. The former is primarily Tropical Surface
Water and the latter primarily Equatorial-
Subtropical Surface Water. Of 217 spotted and/or
spinner dolphin schools encountered during the
January-March cruises, and having associated
temperature and salinity measurements, 80.6% were
in this TVopical Surface Water, while only 19.4% were
in the Equatorial- Subtropical Surface Water. In com-
parison 53.7% of 229 similarly observed schools of
striped and/or common dolphins were in the Ti"opical
Surface Water and 46.3% were in the Equatorial-
Subtropical Water. The differential in percentages
by species pair reflects the more uniform "Inner
Tropical" Surface Water habitat of spotted and spin-
ner dolphins and the importance to striped and com-
mon dolphins of both the variable Tropical Water off
Central America and the variable waters along the
Equator, west of Peru, and southwest of Baja
California.
Because the school sighting data are represented
by many combinations of temperature and salinity
from various areas, it is useful to summarize these
results in terms of an integrated measure of temper-
ature and salinity, i.e, sigma-^, a measure of water
density (see Sverdrup et al. 1942). Table 3 lists the
numbers and percentages of spotted and spinner and
of striped and common dolphins according to their
occurrence at different intervals of sigma-^. The
percentages of striped and common dolphin schools
were higher than that of spotted and spinner dolphin
schools for sigma-t ^22.5 (primarily Equatorial-
Subtropical Water). The opposite was true for sigma-
t <22.5 (primarily Tropical Water). The difference
in percentage distribution by species pair is signifi-
cant (P < 0.01, Kolmogorov-Smirnov test).
Seasonal Features of Habitats
It is not clear how dolphin populations are affected
by seasonal changes in the environment, although
the available data suggest what may happen. The far
offshore habitat of spotted and spinner dolphins, be-
tween long. 120°W and 140°W at about lat. 10°N,
is an important "porpoise-tuna" fishing area during
Table 3. — Percent distribution of dolphin schools^ according to surface water density
(sigma-f).
sigma-f
Spotted
Spinner^
Total
o/o
Striped
Common
Total
%
+ 18.5-19.0
2
2
0.9
+ 19.0-19.5
2
1
3
1.4
5
5
2.2
+ 19.5-20.0
6
6
2.8
8
8
3.5
+ 20.0-20.5
0.0
2
1
3
1.3
+ 20.5-21.0
5
2
7
3.2
6
2
8
3.5
+ 21.0-21.5
16
12
28
12.9
11
2
13
5.7
+ 21.5-22.0
43
28
71
32.7
27
6
33
14.4
+ 22.0-22.5
12
32
54
24.9
26
19
45
19.7
+ 22.5-23.0
15
6
21
9.7
22
8
30
13.1
+ 23.0-23.5
8
11
19
8.8
39
15
54
23.6
+ 23.5-24.0
2
4
6
2.8
10
3
13
5.7
+ 24.0-24.5
2
2
0.9
6
6
12
5.2
+ 24.5-25.0
1
2
3
1.3
+ 25.0-25.5
Total
111
96
217
100
165
64
229
100
'January-March, research cruises, 1976, 1977, 1979, 1980.
^Includes mixed spinner + spotted dolphin schools.
632
AU and FERRYMAN: DOLPHIN HABITATS
the spring and summer months (Calkins 1975).
However there is little information from that area
during the winter months (when there is little
fishing), except for results from the January-March
research cruises, which indicated that population
densities there were not high (Fig. 6). This suggests
a summer buildup in the concentration of these
dolphins. This is likely because the offshore habitat
is centered close to or along the divergence zone at
the northern boundary of the North Equatorial
Countercurrent, where the thermocline ridges and
biological production is increased (Cromwell 1958).
During the northern summer, the trade winds over
the offshore habitat abate, ridging intensifies (Wyrt-
ki 1964a, 1974), and porpoise-tuna fishing expands
west of Clipperton Island (at ca. lat. 10°N, long.
109°W). The increase in fishing may be due to bet-
ter weather, but possibly also to an increased abun-
dance of dolphins and tuna.
The seasonal change in environment of the eastern
tropical Pacific most likely to affect the distribution
of dolphins is that due to the movement of the
southern border of the tropical waters. During the
northern winter, tropical conditions usually extend
to about 15° south of the Galapagos Islands, when
a shallow surface layer of warm water develops over
what is actually Subtropical Water. During the north-
ern summer, the cool Peru and South Equatorial
Current strengthen, and a conspicuous thermal
front, marking the southern boundary of Tropical
Surface Water, usually develops. This Equatorial
Front (Wyrtki 1966) is located a few degrees north
of the Equator except for a short section east of the
Galapagos Islands.
We studied the relationship of the Equatorial
Front to dolphin populations during an October-
November 1977 cruise of the David Starr Jordan.
The Equatorial Front was conspicuous, as were the
effects of the cool Peru and South Equatorial Cur-
rents (Fig. 9). Only 4 of 27 sightings of spotted and
spinner dolphins schools in the equatorial region oc-
curred in the cool, Equatorial and Subtropical
Waters south of the front. The majority of the re-
maining 23 sightings were along the Equatorial
Front, at the southern border to the warm Tropical
Surface Water. These same species had occurred
throughout these southern waters during January
to March (Figs. 3, 4), when sea surface temperatures
of 25°C or more prevailed over this entire area. The
apparent redistribution of dolphin schools along the
warm edge of the Peru Current and Equatorial Front
appeared to be restricted to the spotted and spin-
ner species, suggesting their seasonal movements
away from cool southern waters. By implication these
same dolphin species may migrate into southern
waters during the warm season. Seasonal move-
ments of dolphins (unidentified) in the southern
waters is also suggested by results from the 1967
and 1968 EASTROPAC cruises (Love 1971, 1972).
On the other hand, we did see during the October-
November cruise four schools of spotted and spin-
ner dolphins in cool Subtropical Water, and observers
aboard tuna seiners have also reported these same
species there during the cool season.
I30»
IQo —
c -
I0« -
Figure 9.— Distribution of dolphin schools in the equatorial region during October-November 1977,
relative to surface isotherms (°C). Notice the Equatorial Front or zone of rapid temperature change
just north of the Equator. Clumping of sightings along the track is due to nighttime travel by ship.
"Other" dolphins are primarily pilot whales.
633
FISHERY BULLETIN: VOL. 83, NO. 4
Dolphin Communities
The habitat differences discussed also apply to
other delphinid species, so that there seem to be dif-
ferent communities of dolphins in the eastern Pacific
To show how the cetacean communities differ be-
tween the habitats dominated by spotted and spin-
ner and by striped and common dolphins, the eastern
Pacific was divided into Areas I and II (Fig. 10, in-
set) that separate the main habitat areas of these
two species pairs. Area I is primarily Tropical Sur-
face Water and includes most areas where thermo-
cline ridging is a dominant physical feature Area
II is primarily Equatorial-southern Subtropical Sur-
face Water, but also includes the wedge-shaped area
of variable Tropical Water in the Central American
Bight. Area II comprises most of the waters we have
called Upwelling-Modified.
In each of these two areas, only schools sighted
at <1.0 nmi perpendicular to the ship's tracks were
listed. This requirement was imposed so that per-
cent species composition could be based on species
schools, that to the largest practical degree, could
all be sighted with equal probability, if present. The
change in "sightability" with distance is different for
each species because of differences in behavior,
coloration, size, etc
Our data indicate that the species composition of
delphinids is different in these two areas. Percent-
age composition was determined for spotted; spin-
ner; striped; common; bottlenose, Tursiops trun-
catus; rough-toothed, Steno bredanensis; and Risso's,
Grampus griseus, dolphins, and for "blackfish",
Peponocephala electra/Feresa attenuata; pilot whales,
Globicephala macrorhynchus; and others (Tkble 4).
Among 8 of 10 species-groups specifically identified
in Tkble 4, there were significantly higher percent-
ages of spotted, spinner, and rough-toothed dolphin
schools in Area I than in Area II (Fig. 10). Risso's
and bottlenose dolphins were important species in
both areas, and their percentage values did not dif-
fer significantly between the areas. The percentages
due to striped and common dolphins and pilot whales
increased in Area II relative to Area I. Though
reduced, the spotted dolphin remained important in
the Area II dolphin community. The increase in per-
cent composition of the common dolphin in Area II
was not quite significant, reflecting the inclusion in
Area I of that species' distributional lobe off Baja
California. Overall, the species composition differed
significantly between the two areas, as determined
by chi-square contingency test of the frequency of
species other than spotted, spinner, striped, and com-
mon, i.e, the species not initially considered when
delimiting Areas I and II (x^ = 74.4, df = 5, P <
0.005).
Additional evidence for the distinctiveness of the
equatorial and subtropical portions of the Area II
community is provided by observations along
equatorial transects and transects south and south-
30 r
25
(0
§<
W< 20
•^ lU
11. H
O Z
UJ
Q.
15
10
27.5*
Area I
[ 1 Area II
120' 110° 100" 90*
Spotted Bottlenose Spinner Risso's Rough-
toothed
Striped Common
DELPHINID SPECIES
Pilot
Whale
Figure 10.— Percent species composition of some important cetaceans, by Area I and II. See
Ikble 4.
634
AU and FERRYMAN: DOLPHIN HABITATS
Table 4. — Percent composition of species as encountered in two areas' during the January-
March research cruises.
Area 1
Area II
95%3
95%3
Delphinid spp.^
Schools
%
C.I.
Schools
%
C.I.
Spotted,
Stenella attenuata
67
24.7
19.6-29.8
55
13.2
10.0-16.4
Spinner,
Stenella longirostris
41
15.1
10.8-19.4
19
4.6
2.6-6.6
Striped,
Stenella coeruleoalba
22
8.1
4.9-11.3
86
20.6
16.7-24.5
Common,
Delphinus delphis
10
3.7
1.5-5.9
34
8.2
5.6-10.8
Pilot whale.
Globicephala macrorhynchus
5
1.8
0.2-3.4
75
18.0
14.3-21.7
Risso's,
Grampus griseus
31
11.4
7.6-15.2
65
15.6
12.1-19.5
Bottlenose,
Tursiops truncatus
50
18.5
13.9-23.1
58
13.9
10.6-17.2
Rough-toothed,
Steno bredanensis
31
11.4
7.6-15.2
10
2.4
0.9-3.9
"Blackfish",
Peponocephala electra or
Feresa attenuata
8
3.0
1.0-5.0
1
0.2
0-0.6
Other
6
2.2
0.2-4.2
14
3.4
1.7-5.1
Total
271
417
'Areas are shown in Figure 10.
^Species in mixed schools were tabulated separately.
^Normal approximation to binomial distribution.
east of the Galapagos Islands, i.a, off Peru. Unlike
during the January-March cruises, physical ocean-
ography was the primary task on most of these
transects, hence the ships did not usually divert
course toward the schools, and many schools could
not be identified. Nevertheless some idea of the
species compositions can be obtained. The observa-
tions (Ihble 5) showed that pilot whales and Risso's
and bottlenose dolphins were frequently encountered
species during October- December off Peru, and com-
mon dolphins were often seen near the coast. On the
equatorial transects, between long. 85°W and
110°W, striped and common dolphins were the
characteristic species. The common dolphin was seen
most often near the Galapagos Islands. Pilot whales
were relatively abundant during May- July 1981 in
this equatorial section. West of long. 110°W along
the Equator, pilot whales again were the most fre-
quently encountered species. Interestingly, sightings
of Eraser's dolphins, Lagenodelphis hosei, and
"blackfish" (probably Peponocephala electra) were
also relatively frequent, especially between long.
110°W and 145°W. These two species often school
together and appear to prefer equatorial waters
(Perryman et al.'*). In the next section, another
distinctive feature of equatorial waters will be
brought out.
Dolphins, Birds, and Tuna
A conspicuous feature distinguishing the dolphin
communities is the difference in the species-specific
association with tunas. In the eastern tropical
Pacific, spinner dolphins and especially spotted
dolphins are found associated with "surface"
yellowfin tuna. It is these two species, therefore, that
are mainly affected by the porpoise-tuna fishery
(Smith 1983). Surface tunas occur at the sea surface
and can be caught by purse seine, trolling, and pole-
and-line gear. "Deep tunas" of the same species are
caught by longline gear, generally in and below the
thermocline Since these surface tunas drive food to
the surface, making it available to certain seabirds
(Ashmole and Ashmole 1957; Murphy and Shomura
1972), a reliable indication that tuna are accompany-
ing a dolphin school is the presence of a bird flock.
Birds are the most important cue used by fishermen
to locate dolphin-tuna schools.
Birds do not occur equally among the different
dolphin species. During the 1977, 1979, and 1980
January-March cruises (when the best bird observa-
■•Perryman, W. F., D. W. K. Au, and S. Leatherwood. Manuscr.
prep. Melon-headed whale, Peponocephala electra (Gray, 1946)
(with notes on the pygmy killer whale Feresa attenuata). South-
west Fisheries Center La Jolla Laboratory, National Marine
Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA 92038.
635
FISHERY BULLETIN: VOL. 83, NO. 4
05
o
CVI
§
2
o
o
O
C\J 00
L.'
o
o
in
CB
Tt
3
a-
LU
o
<n
c
(Q
o
EC
Ol
c
to
CO
0)
SI
O
(0
X)
c
CO
(0
3
C7
(O
O)
c
o
10
c
0)
(D
CO
CO
g>
o
0}
a.
CO
JO
o
o
.c
o
CO
E
3
in
UJ
m
CO
0
5
o
o
in
CM
^
o
o
o
«
3
T~
(T
ai
CO
o
O o
^' in
c»
CO
3
<T
UJ
CO
o
O
§
6
in
3
CJ>
I
0
CO
00
^
°
K CD .-■ (35
^ Cj
CD Q 00
<U ./, <35
CO O ■^
•C Q.
P CD O
CO — '^
CU 3
Qj ~ 2:
CO o '^
c
coo-
c:i
c
CO
CO
o
Q.
OJ
O)
.c
to
0)
CO
Q
(T
CM
00 OJ 1-
CM CM
CM
CO
CD 1^ •* t^ 00
Cvj
»- CO T- CO 1- ^
O CO CM CO C3> •<* Tj-
CM T-
1- CO
CM
•* CO
CO
•>- •* CO m ■^ CM •>-
1- CD in C3> ^1-
CO
O ■^ CO '-
•>- 1- CM
CM
C3.
Q.
CO
c
ce
*-
j=
CD
Q.
3
O
O
1
■a
CD
.*
CD
CO
e
c:
CD
CD
O
CD
5
CU
iQSSlcofcoE
C Q.
Z) CO
CO CO
.CO
CO
" .C CO
-c o
Ci c
m
CO
CD
O
c:
CO
a
.o
io
5 o'
I
o
CD
E
.CD
CD
-C
&
o
5 ">
o o
rri <o
C3 CO
CO
c:
cu
'"I
C3
■r o
.c c:
ir
cu
CO
C5
-c
.CO
-c
O
CO CD
CO -^1
o
a>
"^ Z
-5 «
CD 3
-C C
Q. m
0) fc
O CD
C5 n.
r- CD
o Q. SI
CQ
CO
CO
C
I
0) CO
s (D . t:
^ p ® o
O Q CO CO
= -Q -C 3
<i> s ■- e
636
AU and FERRYMAN: DOLPHIN HABITATS
tions were taken), 70.7% of 167 spotted, spinner, or
mixed spotted and spinner dolphin schools, sighted
between lat. 5°N and 30°N (where most dolphin-tuna
associations occur), had 10 or more associated birds
(Tkble 6). We assume this minimum flock size in-
dicates associated tuna, although we did not often
actually see the tuna. For the same period and area,
30.6% of 49 common dolphin schools and only 1.6%
of 64 striped dolphin schools were with 10 or more
birds. The different percent occurrences indicate
that tuna are most frequently associated with spot-
ted and spinner dolphins and very seldom with the
striped dolphin.
The bird species most numerous in offshore waters
with dolphin schools are boobies {Sula spp.); wedge-
tailed shearwaters, Puffinus pacificus; and sooty
terns. Sterna fuscata. Frigate birds {Fregata spp.)
are also closely associated with these dolphins,
though their average flock size is only seven (Au and
Pitman^). These bird species are all strongly depen-
dent upon tunas in their feeding. Our observations
are that the birds feed primarly in association with
the fish, not the dolphins.
The dolphin-tuna-bird association appears to be
area- as well as species-specific Assuming flocks of
^10 birds indicate the presence of yellowfin tuna,
this association seems to occur in all areas with
higher relative abundance of spotted and spinner
dolphins (Fig. 11). The association seldom occurs
along the Equator, or in areas outside the traditional
porpoise-tuna fishing grounds (roughly these are
waters within the triangular-shaped area whose base
is formed by the American coasts between lat. 25°N
and 15°S, and whose apex is at lat. 10°N, long.
150°W; see Calkins 1975 and lATTC 1979-81), even
though the required species of dolphins, tuna, and
^Au, D. W. K., and R. L. Pitman. Manuscr. prep. Seabird
interactions with dolphins and tuna in the eastern tropical
Pacific Southwest Fisheries Center La Jolla Laboratory, Na-
tional Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038.
birds may be present there Relatively few of the
spotted or spinner dolphin schools sighted near the
Equator were with bird flocks. South of the Equator
and in the Central Pacific, there are abundant flocks
of sooty terns with fish schools, but dolphins do not
usually co-occur (Au and Pitman fn. 5). The most im-
portant area of the dolphin-tuna-bird association is
centered about the divergence zone near lat. 10°N,
an important porpoise-tuna fishing ground for
yellowfin tuna (primarily Area I of Figure 10).
These areal changes in the interactions among
species are usually clearly apparent during north-
south transects across the eastern Pacific during any
season. An example is the July-September 1980,
NOAA ship Researcher transits between Manzanillo,
Mexico, and lat. 3°S, long. 100°W, via Clipperton
Island. At that time Tropical Surface Water (T >
25°C) extended to the Equator with transition
toward Equatorial Water marked by temperature
and salinity fronts at lat. 5°N-6°N and at the
Equator (Fig. 12). In the tropical waters north of the
front at lat. 5°N there was a conspicuous increase
in abundance of flocks of sooty terns, boobies, and
shearwaters {Puffinus spp.), all broadly centered
about the thermocline ridge at lat. 10°N. The larger
gadfly petrels (Pterodroma spp.) were also abundant.
All of these birds frequently flock over fish and
dolphins. South of this boundary was another avian
group, with Pterodroma leucoptera, a small petrel
from the Southern Hemisphere, and planktivorous
storm petrels (Oceanodroma spp.) predominating,
and peak abundances at the Equator. These latter
birds usually feed independently of fish and seldom
flock over fish and dolphins.
Correlations among water masses, seabirds, and
the different cetaceans along the transect were dif-
ficult to quantify because of the small sample size
of the latter. However, the observations are suppor-
tive of such relationships. There were 39 dolphin
schools, of which 15 were unidentified, and 21 whale
schools along this transect. Spotted and spinner
Table 6. — Dolphin schools associated with seabirds.
5°N-30°N
<5<'N
with
with
Dolphin spp.
Schools
>10 birds
o/o
Schools
>10 birds
%
Spotted
95
56
58.9
40
8
20.0
Spotted and
spinner
55
53
96.4
21
8
38.1
Spinner
17
9
52.9
19
6
31.6
Common
49
15
30.6
10
1
10.0
Striped
64
1
1.6
76
1
1.3
Rough-toothed
40
5
12.5
13
1
7.7
Other/unidentified
388
17
4.4
189
6
3.2
637
FISHERY BULLETIN: VOL. 83, NO. 4
170"
160*
ISO*
140*
130*
120*
no* 100* 90* 80* 70* 1
30°
1
1
1
1
1
NA\ ( SPOTTED AND SPINNER
)\ \ uFYirn i DOLPHIN SCHOOLS AND
«^x MCAH-u * ASSOCIATED BIRD FLOCKS
30-
Hawaiian Islands
• o
o
\ ^
*■§.
\ \ r^
20"
i>
0 °
0
°° •^'S^ ^X-^^TJ U '"®- '^^^' '3^3' '880 ~
• jfVo^capuIco ]' RESEARCH VESSEL CRUISES
20*
10*
_
o*
O
o
• o
•
o
o
oo •
,o o.
•
10*
0
••
o
o
• oo
0*
~
Christmas Island °
o
°."-o
•
o
• o
§°ef
° °°°0 0 J3 . ** • /
Oo " o o [Guayaquil
( SOUTH
o o, o°OoO <v,^ AMERICA
0*
10*
Marquesas Islands
• •• • \Lima
10*
ASSOCIATED BIRO FLOCKS
N
20*
"
O < 10 BIRDS WITH SCHOOL
-
20*
• > 10 BIRDS WITH SCHOOL
1
30' 1
170*
1
160*
1 ._.
ISO*
1
140*
1
130*
1
120*
1 1 1 1 U30*
110* 100* 90* 80* 70*
Figure 11.— Distribution of bird-associated spotted and spinner dolphin schools during the January-March research cruises. Schools with
10 or more birds are assumed to be with tuna.
dolphns did occur coincidentally with bird flocks (and
probably with tuna) in the warmer tropical waters
centered about lat. 10°N, but also were seen at the
Equator, though without associated bird flocks.
Striped and common dolphins occurred in coastal
and equatorial waters, without bird flocks. These lat-
ter dolphins were the characteristic species on the
equatorial transect of this same cruise (see Ikble 5,
col. 4), where only one of the schools seen, a mixed
spotted and spinner dolphin school, had an
associated bird flock. The distinct change in the bird
fauna south of lat. 5°N to species that do not forage
commensally with fish suggests there are changes
with water masses in the nature of epipelagic prey
and how the top predators forag&
DISCUSSION
It should not be surprising that the two major
divergence zones of the eastern Pacific, near lat.
10°N and along the Equator, are important features
of the oceanic habitats of eastern Pacific cetaceans.
Enriched by the effects of wind and the major zonal
currents (Brandhorst 1958; Cromwell 1958; Reid
1962; Wyrtki 1966), the zones are evident areas of
enhanced biological production (Blackburn 1966,
1976; Blackburn et al. 1970; King 1974; Parsons et
al. 1977; Brinton 1979). that are important to tunas
(Calkins 1975; Blackburn 1965; Blackburn and Laurs
1972; Blackburn and Williams 1975; Sund 1981) and
cetaceans as discussed above These two zones are
not qualitatively the same, however; the strong,
shallow thermoclines that have been related to suc-
cessful porpoise-tuna fishing (Green 1967; Miller et
al.^) and to aggregations of dolphins and baleen
whales (Rovnin 1969; Volkov and Moroz 1976) are
characteristic of the lat. 10°N zone, but not of the
Equator. Similarly the oxygen minimum layer, noted
by Perrin et al. (1976) to be correlated with the
distribution of the spotted dolphin, occurs only north
and south of the Equator in the eastern Pacific
Equatorial waters are characterized by shallow, weak
(<2°C/10 m) thermoclines, due to upwelling and the
Equatorial Undercurrent, and cool surface temper-
«Miller, F. R., C. J. Orange, R. H. Evans, and K. A. Bliss.
Manuscr. prep. Analysis of environment related to tuna fishing
in ETR Inter-American Tropical TUna Commission, La Jolla, CA
92038.
638
AU and FERRYMAN: DOLPHIN HABITATS
UJ
o
o
CO
_J
o
o
X
o
o
<
h-
o
o
o
2 -
□ Whales
^ Spotted / Spinner Dolphin
0 Striped / Common Dolphin
□ Other Dolphin
July - Sept. 1980
i
p
i
i
i
f
i
30
28
26
24
22
20°
-
SURFACE "~^^v ^
SALINITY %o -^ \ ^^^,^^'?~^ _ /T
SURFACE TEMPERATURE "C
1 1 1 1 1 1
1 1 1 1 1 1
35.0
34.5
34.0 o
335 -^
330
200
100
Boobies, Shearwaters, Petrels
White Winged Petrel
Terns
Storm Petrel I
LATITUDE
Figure 12.— Transect along long. 110°W, July-September 1980, showing changes in cetaceans, birds, and temperature and salinity. The
relative abundance of dolphin schools include unidentified schools which were prorated according to species ratios of identified schools.
639
FISHERY BULLETIN: VOL. 83, NO. 4
ature from June through December. These waters
support a different cetacean community (Ikble 5),
though school densities there can be as high as in
areas off Mexico and Central America (Au et al.
1980).
Other relationships between distribution and
movements of dolphins and water masses, conver-
gences, and thermal conditions have been described
by Fraser (1934), Gaskin (1968), Kasuya (1971),
Nishiwaki (1975), Evans (1975), and Miyazaki and
Nishiwaki (1978). Hui (1979) found that common
dolphins off California tended to occur over promi-
nent features of bottom topography. The deep depths
of such areas suggest that surface eddies and conver-
gences caused by topography-induced accelerations
to deep reaching currents (Sverdrup et al. 1942;
Neumann 1960) may have concentrated food and at-
tracted the dolphins.
The distributions of dolphin species as seen from
the January-March cruises (Figs. 3-7) are similar to
the all-season school distributions derived from data
of scientific observers aboard tuna seiners. These
data, consisting of thousands of sightings per
species, were recently summarized by Scott (1981)
and Perrin et al. (1983). The same major distribu-
tional patterns as presented here for the January-
March cruises were apparent, including, for spotted
and spinner dolphins, the relative unimportance of
equatorial latitudes and the secondary band of in-
creased concentration of schools 2°5° north of the
Equator. The latter may be related to the Equatorial
Front and increased food concentration and possibly
production in the convergence zone there (Sette
1955; King and Iverson 1962; Blackburn and Laurs
1972; Murphy and Shomura 1972; Pak and Zaneveld
1974; Blackburn and Williams 1975; Greenblatt
1979). Increased abundance of micronekton occurs
at least sometime in this zone (Love 1971, 1972;
Blackburn and Laurs 1972). The purse seiner data,
like those of this paper also showed spotted and spin-
ner dolphins more concentrated in the tropical
waters off Mexico and along lat. 10°N, while striped
and common dolphins tended to be found in the Cen-
tral American Bight and along the Equator. This
complementary type of distribution was less ap-
parent with the more broadly distributed striped
dolphin. It should be noted that our southern
distributional lobe for spotted and spinner dolphins,
at ca. lat. 5°S, may in part be due to the sampling
pattern. However, the density of these dolphins along
the Equator is definitely reduced, and we know of
no information that does not suggest a rapid decline
in density south of our lobe
Our January-March data differs from the all-
season data in indicating fewer schools in the area
around the Revilla Gigedo Islands (at ca. lat. 19°N,
long. 111°W) and between long. 90 °W and 100°W
along lat. 10°N for spotted and spinner dolphins.
Also our data suggested that striped and common
dolphins had a more localized distribution near the
region of the Costa Rica Dome, and were relatively
infrequent between long. 105°W and 120°W, along
lat. 10°N. These differences may be due to seasonal
changes in distribution.
The relative densities of these dolphins, as school
encounter rates in the tuna purse seine fishery, were
recently calculated by Polacheck (1983). The patterns
he derived were fragmentary, but not inconsistent
with those of this paper. He showed, for example,
higher densities of spotted and spinner dolphins ex-
tending to the southwest from off southern Mexico
and reduced densities in the Central American
Bight. For striped and common dolphins, he also
described a three-lobed distribution pattern as in this
paper. However his equatorial lobe was centered just
south of the Equator.
It seems likely that the dolphin community of the
Upwelling-Modified Water differs from the Tropical
Water community because of water-mass specific dif-
ferences in the distribution and availability of food.
This is supported by the different biotic features of
Equatorial and Subtropical Waters relative to
Tropical Waters. The distinction is clearly shown by
the surface distribution of nutrients and primary
production in these waters as measured during the
EASTROPAC cruises (Love 1971, 1972). The
equatorial waters of the eastern Pacific in particular
are different. They support abundant plankton-
feeding storm petrels rather than fish and
cephalopod-feeding flocking birds that are usually
abundant both north and south of the Equator (see
also Love 1971, 1972 and King 1974). Dolphin species
along the Equator tend not to be with fish or birds
(Figs. 11, 12), and the species composition of the
cetacean community appears to be distinct (Tkble 5;
Au and Pitman 1981). Of course it has previously
been known that equatorial waters are notable in
being important sperm whale grounds (Ibwnsend
1935) and have a zooplankton community distinct
from other parts of the eastern tropical Pacific
(McGowan 1972). Finally the fact that the common
dolphin, a species characteristic of coastal upwell-
ing waters from California to Peru, occurs with
greater frequency in the equatorial waters and near
upwelling areas in the Central American Bight, sug-
gests that the shorter and different food chains of
the upwelling environments (Parsons et al. 1977) may
be the basis of the community difference
640
AU and FERRYMAN: DOLPHIN HABITATS
The dolphin-tuna-bird association is one manifesta-
tion of community difference that is both striking
and of ecological interest. The distribution of this
association is notable in that it seems coincident with
both the main habitats of spotted and spinner
dolphins and the distribution of "surface" yellowfin
tuna in the eastern Pacific (see Figure 11, Shingu
et al. 1974, and Suzuki et al. 1978). Since it is
primarily these dolphins that are associated with
birds and with yellowfin tuna, the geography of the
dolphin-bird association also defines that of the
dolphin-yellowfin tuna association. This association
of birds and fish with dolphins occurs in all tropical
waters, including the southern Subtropical Water
during the southern summer. It is apparently rare
in equatorial waters of the eastern Pacific, in the cen-
tral and western Pacific (Myazaki and Wada 1978;
Au et al. fn. 2), and in the eastern tropical Atlantic
(Levenez et al. 1980). In the central Pacific the same
bird species found with spotted and spinner dolphins
in the eastern tropical Pacific can be abundant
(Gould 1974), and sooty terns especially, are fre-
quently associated with small tunas, but these are
most likely skipjack tuna (Murphy and Ikehara 1955;
Waldrom 1964; Hida 1970; Blackburn and William
1975). Apparently those flocks seldom accompany
dolphins or schools of larger yellowfin tuna. Yellowfin
tuna and dolphins seldom seem to associate outside
the eastern tropical Pacific
The obvious feeding activity often seen in these
joint aggregations of birds, spotted and spinner
dolphins, and tuna suggests that these species have
similar food and foraging requirements. Our obser-
vations indicate that the mammals and fish are not
tightly associated in the aggregations (see Au and
Perryman 1982) and probably feed independently
(see also Norris and Dohl 1980a). However the tuna,
birds, and spotted dolphin (at least) do appear to be
feeding at the same time. Both the tuna and spot-
ted dolphins feed on epipelagic fish and on squids
(Perrin et al. 1973; Olson 1982), but the spinner
dolphins feed differently and may forage more at
night (Perrin et al. 1973; Norris and Dohl 1980b);
though they are active in these feeding aggregations,
they may not be directly associated with the tuna.
Judging from the associations of bird and dolphin
species, only spotted and spinner dolphins frequently
find it advantageous to feed with yellowfin tuna. Fur-
thermore the distribution of this association suggests
that the necessary kind and behavior of prey that
is likely the basis of the association appears charac-
teristic of tropical, but not equatorial, waters. It oc-
curs especially where a shallow thermocline may con-
strain the yellowfin tuna to the surface layer with
the dolphins, a complex interaction between environ-
ment and physiology (Sharp 1978) that may cause
the phenomenon known as "surface tuna". Finally
the distribution of the bird-dolphin association in-
dicates that the dolphin-tuna association is
characteristic of areas of higher school density of
spotted and spinner dolphins. High population den-
sities of both dolphins and yellowfin tuna, and
suitable prey are therefore likely requisites for joint
dolphin-tuna schools. The dolphin-tuna association
is a feature of the most productive tuna fishing zones
of these tropical seas. In such rich areas, feeding tac-
tics to exploit clumped prey could lead to multi-
species aggregations of predators, as explained by
Schoener (1982).
ACKNOWLEDGMENTS
This paper was reviewed by the following persons
whose help is much appreciated: David E. Gaskin,
Kenneth S. Norris, Carleton Ray, Gunter R. Seckel,
Paul N. Sund, James G. Mead, Frank G. Alverson,
Richard Pimentel, John A. McGowan, Gary T.
Sakagawa, Jay Barlow, Andy Dizon, Albert C.
Myrick, William Perrin, Steve Reilly Tim Smith, Paul
E. Smith, Rennie S. Holt, Eric D. Forsebergh, and
Michael D. Scott.
We thank the officers and crews of the NOAA
ships involved in this study, especially those of the
Townsend Cromwell and David Starr Jordan, for
their cooperation and help. We particularly thank the
biological technicians who manned the watches
through high-powered binoculars, for their keen
observations and provoking discussions at sea.
Among them we especially appreciate the work of
Gary Friedrichsen, Phillip Unitt, James Lambert,
Dale Powers, Robert Pitman, James Cotton, and
Scott Sinclair.
We sincerely thank Lorraine Prescott and her
staff for careful typing of this manuscript and Ken
Raymond, Roy Allen, and Henry Orr for drafting the
illustrations.
LITERATURE CITED
Alverson, F. G.
1981. Comments on the distribution of spotted, spinner, com-
mon and striped dolphin in the tropical Pacific Ocean. In
P. S. Hammond (editor), Report on the Workshop on lUna-
Dolphin Interactions, p. 109-124. Inter-Am. Trop. Ibna
Comm., Spec Rep. 4, App. 5.
ASHMOLE, N. P., AND M. J. ASHMOLE.
1957. Comparative feeding ecology of seabirds of a tropical
oceanic island. Yale Univ. Peabody Mus. Nat. Hist. Bull.
24:1-131.
641
FISHERY BULLETIN: VOL. 83, NO. 4
Au, D. W., W. L. Ferryman, R. L. Pitman, and M. S. Sinclair.
1980. Cetacean populations and equatorial oceanography.
Trop. Ocean Atmos. Newsl., Univ. Wash., 4:6-10.
Au, D. W. K., and R. L. Pitman.
1981. The equatorial cetacean community of the eastern
Pacific. (Abstr.) Proceedings of the Fourth Biennial Con-
ference on the Biology of Marine Mammals, Dec 14-18, 1981,
p. 95.
Au, D., AND W. Perryman.
1982. Movement and speed of dolphin schools responding to
an approaching ship. Fish. Bull., U.S. 80:371-379.
Bennett, E. B.
1966. Monthly charts of surface salinity in the eastern tropical
Pacific Ocean. [In Engl, and Span.] Inter-Am. Trop. lUna
Comm., Bull. 11:3-44.
Blackburn, M.
1965. Oceanography and the ecology of tunas. Oceanogr.
Mar. Biol. Annu. Rev 3:299-322.
1966. Biological oceanography of the eastern tropical Pacific:
summary of existing information. U.S. Fish. Wildl. Serv,
Spea Sci. Rep. Fish. 540, 18 p.
1976. Review of existing information on fishes in the deep
ocean mining environment study (DOMES) area of the
tropical Pacific Inst. Mar. Res., Univ Calif., IMR NO. 76-1,
77 p.
Blackburn, M., and R. M. Laurs.
1972. Distribution of forage of skipjack tuna (Euthynnus
pelamis) in the eastern tropical Pacific U.S. Dep. Commer.,
NOAA Ifech. Rep. NMFS SSRF-649, 16 p.
Blackburn, M., R. M. Laurs, R. S. Owen, and B. Zeitschel.
1970. Seasonal and areal changes in standing stocks of phyto-
plankton, zooplankton, and micronekton in the eastern
tropical Pacific Mar. Biol. (Berl.) 7:14-31.
Blackburn, M., and F. Williams.
1975. Distribution and ecology of skipjack tuna, Katsuwonics
pelamis, in an offshore area of the eastern tropical Pacific
Ocean. Fish. Bull., U.S. 73:382-411.
Brandhorst, W.
1958. Thermocline topography, zooplankton standing crop,
and mechanisms of fertilization in the eastern tropical Pacific
J. Cons. Int. Explor. Mer 24:16-31.
Brinton, E.
1979. Parameters relating to the distribution of planktonic
organisms, especially euphausiids in the eastern tropical
Pacific Prog. Oceanogr. 8:125-189.
Calkins, T R
1975. Geographical distribution of yellowfin and skipjack tuna
catches in the eastern Pacific Ocean, and fleet and total catch
statistics, 1971-1974. [In Engl, and Span.] Inter-Am. Trop.
llina Comm., Bull. 17:3-116.
Cromwell, T.
1958. Thermocline topography, horizontal currents and
"ridging" in the eastern tropical Pacific [In Engl, and
Span.] Inter-Am. Trop. Ibna Comm., Bull. 3:135-164.
Evans, W. E.
1975. Distribution, differentiation of populations, and other
aspects of the natural history of Delphiniis delphis Linnaeus
in the northeastern Pacific Ph.D. Thesis, Univ. California,
Los Angeles, 164 p.
FORSBERGH, E. D.
1969. On the climatology, oceanography, and fisheries of the
Panama Bight. [In Engl, and Span.] Inter-Am. Trop. Ibna
Comm., Bull. 14:45-385.
Eraser, F C.
1934. Report on cetacea stranded in British coasts from 1927
to 1932. Br. Mus. (Nat. Hist.) No. 11, 41 p.
Gaskin, D. E.
1968. Distribution of delphinidae (Cetacea) in relation to sea
surface temperature off eastern and southern New Zealand.
N.Z. J. Mar. Freshw. Res. 2:527-534.
Gould, P. J.
1974. Sooty tern {Sterna fuscata). In W. B. King (editor).
Pelagic studies of seabirds in the central and eastern Pacific
Ocean, p. 6-52. Smithson. Contrib. Zool. No. 158.
Green, R. E.
1967. Relationship of the thermocline to success of purse sein-
ing for tuna. Trans. Am. Fish. Soc 96:126-130.
Greenblatt, P. R.
1979. Associations of tuna with flotsam in the eastern tropical
Pacific Fish. Bull., U.S. 77:147-155.
HiDA, T S.
1970. Surface tuna schools located and fished in equatorial
eastern Pacific Commer. Fish. Rev 32(4):34-37.
Hofmann, E. E., a. J. Busalacchi, and J. J. O'Brien.
1981. Wind generation of the Costa Rica Dome Science
(Wash., D.C.) 214:552-554.
Hui, C. A.
1979. Undersea topography and distribution of dolphins of the
genus Delphinus in the southern California Bight. J. Mam-
mal. 60:521-527.
Inter-American Tropical Hina Commission.
1979. Annual report of the Inter-American Tropical Ibna
Commission. [In Engl, and Span.] Inter-Am. Trop. Thna
Comm., La Jolla, CA.
1980. Annual report of the Inter-American Tropical Ibna
Commission. [In Engl, and Span.] Inter-Am. Trop. Ibna
Comm., La Jolla, CA.
1981. Annual report of the Inter-American Tropical Ibna
Commission. [In Engl, and Span.] Inter-Am. Trop. Ibna
Comm., La Jolla, CA.
Kasuya, T
1971. Consideration of distribution and migration of toothed
whales of the Pacific coast of Japan based upon aerial
sighting record. Sci. Rep. Whales Res. Inst. 23:37-60.
King, J. E., and R. T. B. Iverson.
1962. Midwater trawling for forage organisms in the central
Pacific 1951-1956. U.S. Fish Wildl. Serv, Fish. Bull. 62:
271-321.
King, W. B. (editor).
1974. Pelagic studies of seabirds in the central and eastern
Pacific Ocean. Smithson. Contrib. Zool. No. 158, 277 p.
Levenez, J., A. Fonteneau, and R. Regalado.
1980. Resultats d'une enquete sur I'importance des dauphins
dans la pecherie thoniere FISM. Int. Comm. Conserv. Atl.
Ibnas, Coll. Vol. Sci. Pap. IX(1):176-179.
Love, C. M. (editor).
1971. Biological and nutrient chemistry data from principal
participating ships, first survey cruise, February-March 1967.
EASTROPAC Atlas, Vol. 2. Natl. Mar. Fish. Serv., Circ 330,
87 p.
1972. Biological and nutrient chemistry data from principal
participating ships, second survey cruise, August-September
1967. EASTROPAC Atlas, Vol. 6. Natl. Mar. Fish. Serv.,
Circ 330, 80 p.
McGowan, J. A.
1972. The nature of oceanic ecosystems. In C. B. Miller
(editor), The biology of the oceanic Pacific, p. 9-28. Proc 33d
Annu. Biol. Colloq., Oreg. State Univ. Press, Corvallis,
OR.
MiYAZAKI, N., AND M. NiSHIWAKI.
1978. School structure of the striped dolphin off the Pacific
coast of Japan. Sci. Rep. Whales Res. Inst. 30:65-115.
642
AU and PKRRYMAN: DOLPHIN HABITATS
MiYAZAKI, N.. AND S. WADA.
1978. Observations of cetacea during whale marking cruise
in the western tropical Pacific 1976. Sci. Rep. Whales Res.
Inst. 30:179-195.
Murphy, G. I., and I. I. Ikehara.
1955. A summary of sightings of fish schools and bird flocks
and of trolling in the central Pacific U.S. Fish Wildl. Serv.,
Spec Sci. Rep. Fish. 154, 19 p.
Murphy, G. I., and R. S. Shomura.
1972. Pre-exploitation abundance of tunas in the equatorial
central Pacific Fish. Bull., U.S. 70:875-913.
Neumann, G.
1960. On the effect of bottom topography on ocean cur-
rents. Dtsch. Hydrogr. Z., 13:132-141.
NiSHIWAKI, M.
1975. Ecological aspects of smaller cetaceans, with emphasis
on the striped dolphin (Stenella coeruleoalba). J. Fish. Res.
Board Can. 32:1069-1072.
Norris, K. S., and T. D. Dohl.
1980a. The structure and functions of cetacean schools. In
L. M. Herman (editor). Cetacean behavior, mechanisms and
functions, p. 211-261. John Wiley and Sons, N.Y.
1980b. Behavior of the Hawaiian spinner dolphin, Stenella
longirostris. Fish. Bull, U.S. 77:821-849.
Olson, R. J.
1982. Feeding and energetic studies of yellowfin tuna, food
for ecological thought. Coll. Vol. Sci. Pap., Int. Comm. Con-
serv Atl. Ibnas XVII(2):444-457.
Parsons, T. R., M. Takahashi, and M. Hargrave.
1977. Biological oceanographic processes. Pergamon Press,
N.Y., 332 p.
Pak, H., and J. R. V. Zaneveld.
1974. Equatorial front in the eastern Pacific Ocean. J. Phys.
Oceanogr. 4:570-578.
Perrin, W E
1975a. Distribution and differentiation of populations of
dolphins of the genus Stenella in the eastern tropical Pacific
J. Fish. Res. Board Can. 32:1059-1067.
1975b. Variation of the spotted and spinner porpoise (genus
Stenella) in the eastern tropical Pacific and Hawaii. Bull.
Scripps Inst. Oceanogr. 21, 206 p.
Perrin, W. E, J. M. Coe, and J. R. Zweifel.
1976. Growth and reproduction of the spotted porpoise,
Stenella attenuata, in the offshore eastern tropical Pacific
Fish. Bull.. U.S. 74:229-269.
Perrin, W. F, D. B. Holts, and R. B. Miller.
1977. Growth and reproduction of the eastern spinner dolphin,
a geographical form of Stenella longirostris in the eastern
tropical Pacific Fish. Bull., U.S. 75:725-750.
Perrin, W. F, G. J. Walker, F M. Ralston, and D. W. K. Au.
1983. Distribution of four dolphins (Stenella spp. and
Delphinus delphis) in the eastern tropical Pacific with an an-
notated catalog of data sources. U.S. Dep. Commer., NOAA
Tfech. Memo. NMFS-SWEC-38, 65 p.
Perrin, W. E, R. R. Warner, C. H. Fiscus, and D. B. Holts.
1973. Stomach contents of porpoise, Stenella spp., and
yellowfin tuna, Tkunnus albacares, in mixed-species aggre-
gations. Fish. Bull., U.S. 71:1077-1092.
Polacheck, T.
1983. The relative abundance of dolphins in the eastern
tropical Pacific based on encounter rates with tuna purse
seiners. Ph.D. Thesis, Univ. Oregon, Eugene, 475 p.
Reid, J. L., Jr.
1962. On circulation, phosphate-phosphorus content, and zoo-
plankton volumes in the upper part of the Pacific Ocean.
Limnol. Oceanogr. 7:287-306.
ROVNIN, A. A.
1969. Distribution of true whales in the tropical part of the
Pacific In V. A. Arseniev, B. A. Zenkovich, K. K. Chapsky
(editors). Transactions of the Third AU-Union Conference on
Marine Mammals, p. 144-149. Nauka, Moskva, U.S.S.R.
Schoener, T. W.
1982. The controversy over interspecific competition. Am.
Sci. 70:586-595.
Scott, M. D.
1981. Dolphin stocks in the eastern tropical Pacific In P. S.
Hammond (editor). Report on the workshop on tuna-dolphin
interactions, p. 98-107. Inter-Am. Trop. llina Comm. Spec
Rep. No. 4, App. 4.
Sette, 0. E.
1955. Consideration of midocean fish production as related
to oceanic circulatory systems. J. Mar. Res. 14:398-414.
Sharp G. D.
1978. Behavioral and physiological properties of tunas and
their effects on vulnerability to fishing gear. In G. D. Sharp
and A. E. Dizon (editors). The physiological ecology of tunas,
p. 397-449. Acad. Press, N.Y.
Shingu, C, p. K. TbMLiNSON, AND C. L. Peterson.
1974. A review of the Japanese longline fishery for tunas and
billfishes in the eastern Pacific Ocean, 1967-1970. [In Engl,
and Span.] Bull. Inter-Am. Trop. TUna Comm. 16:67-230.
Smith, T D.
1983. Changes in size of three dolphin (Stenella spp.) popula-
tions in the eastern tropical Pacific Fish. Bull., U.S. 81:1-13.
SuND, P. N., M. Blackburn, and F. Williams.
1981. Ibnas and their environment in the Pacific Ocean: a
review. Oceanogr. Mar. Biol. Annu. Rev. 19:443-512.
Suzuki, Z., P. K. IbMLiNSON, and M. Honma.
1978. Population structure of Pacific yellowfin tuna. [In Engl,
and Span.] Inter-Am. Trop. TUna Comm. Bull., 17:277-358.
SvERDRUP, H. U., M. W. Johnson, and R. H. Fleming.
1942. The oceans, their physics, chemistry, and general
biology. Prentice-Hall, Inc, N.Y., 1087 p.
TbWNSEND, C. H.
1935. The distribution of certain whales as shown by logbook
records of American whaleships. Zoologica 19:1-50.
Volkov, a. F, and I. F. Moroz.
1976. Oceanological conditions of the distribution of cetacea
in the eastern tropical part of the Pacific Ocean. Int. Whal-
ing Comm. Rep. 27:186-188.
Waldron, K. D.
1964. Fish schools and bird flocks in the central Pacific Ocean,
1950-1961. U.S. Fish Wildl. Serv., Spec Sci. Rep. Fish. 464,
20 p.
Wyrtki, K.
1964a. The thermal structure of the eastern Pacific Ocean.
Erganzungsh. Dtsch. Hydrogr. Z. Reiche A 8(6), 84 p.
1964b. Upwelling in the Costa Rica Dome U.S. Fish Wildl.
Serv., Fish. Bull., 63:355-372.
1966. Oceanography of the eastern equatorial Pacific Ocean.
Oceanogr. Mar. Biol. Annu. Rev. 4:36-68.
1967. Circulation and water masses in the eastern equatorial
Pacific Ocean. Int. J. Oceanol. Limnol. 1:117-147.
1974. Equatorial currents in the Pacific 1950 to 1970 and their
relations to the trade winds. J. Phys. Oceanogr. 4:372-
380.
643
ASPECTS OF THE LIFE HISTORY OF THE FLUFFY SCULPIN,
OLIGOCOTTUS SNYDERI
Mary C. Freeman,^ Nate Neally,^ and Gary D. Grossman^
ABSTRACT
We examined age structure, growth rates, and diets of male and female Oligocottus snyderi Greeley at
Dillon Beach, CA, where this sculpin numerically dominates the mid- and lower intertidal fish assemblage
Two age classes, 0+ and 1 + , were present; maximum lifespan was about 1.5 years. Instantaneous popula-
tion growth rates were highest for the O-t- age class, and most individuals attained spawning size during
the first year of life Growth rates for both age classes were highest during the high productivity Upwell-
ing period and minimal during the low productivity, Oceanic-Davidson Current period.
Males and females primarily consumed gammarid amphipods and polychaetes. Larger individuals (>50
mm SL) of both sexes consumed a wider variety of prey, including shrimps, crabs, and isopods. Among
year and seasonal dietary changes were minimal. Females consumed two times more gammarids by weight
than males during the low productivity Oceanic-Davidson Current period, when ovarian recrudescence
occurs. Females may increase food consumption to meet the increased energetic demands of egg production.
Rapid sexual maturation and growth and the occurrence of recruitment during upwelling probably are
adaptations to the pronounced annual cycle of productivity. These adaptations, together with intense utiliza-
tion of an abundant prey (gammarids) not widely consumed by other assemblage members, probably con-
tribute to 0. snyderi's numerical dominance in the rocky intertidal of central California.
The fluffy sculpin, Oligocottus snyderi Greeley, is a
common species which inhabits the rocky intertidal
from Baja California to Sitka, AK (Miller and Lea
1972). Between central California and British Col-
umbia, 0. snyderi frequently is very abundant (Green
1971; Cross 1981; Yoshiyama 1981; Grossman 1982).
This species occurs primarily in mid- and lower in-
tertidal areas (Green 1971; Yoshiyama 1981), and
often is associated with surfgrass (Green 1971;
Nakamura 1976a). The general absence of this
species from the high intertidal is probably due to
its inability to tolerate higher temperatures which
frequently occur in high intertidal pools (Nakamura
1976b).
Life histories of intertidal fishes, particularly cot-
tids, are poorly known (Gibson 1969, 1982). Publish-
ed information on the demography of 0. snyderi is
restricted to the work of Moring (1981), who ex-
amined age structure of a northern California 0.
snyderi population, and Grossman and deVlaming
(1984), who described the species' reproductive
ecology. This paper presents data on age structure,
growth rates, and dietary habits of an 0. snyderi
population at Dillon Beach, CA, a site that is sub-
ject to pronounced annual cycles of oceanic produc-
tivity (Parrish et al. 1981). Oligocottus snyderi
numerically dominates the intertidal fish assemblage
at Dillon Beach (Grossman 1982); the present study
explores demographic and ecological characteristics
which may account for this species' ecological suc-
cess in the rocky intertidal.
MATERIALS AND METHODS
Collections
Oligocottus snyderi were collected from a series
of mid- and lower intertidal pools at Dillon Beach,
CA, on 15 dates from January 1979 to July 1981 (see
Grossman in press a for sampling dates). Repeated
collecting did not affect assemblage structure (Gross-
man 1982, in press a). Fish were obtained by
spreading a 10% solution of quinaldine in
isopropanol through the pools and then collecting
individuals after anesthetization. Over 1,400 0.
snyderi were collected. Specimens were preserved
in buffered Formalin^ and were later washed and
transferred to 45% isopropanol. Individuals were
measured to the nearest millimeter standard length
(SL) and weighed to the nearest 0.1 g. Sexes of all
1 School of Forest Resources, University of Georgia, Athens, GA
30602.
^Department of Wildlife and Fisheries Biology, University of
California, Davis, CA 95616.
^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Manuscript accepted January 1985.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
645
FISHERY BULLETIN: VOL. 83, NO. 4
individuals collected during 1979 and of specimens
used for gut analysis also were recorded. A complete
description of collecting methods and the study site
are presented in Grossman (1982, in press b).
Collection dates were assigned either to the Up-
welling or the combined Oceanic-Davidson Current
(ODC) oceanographic seasons, based on water tem-
peratui'e and a calculated upwelling index (see Gross-
man in press b). The Upwelling period is character-
ized by frequent upwelling of nutrient-rich waters
and high productivity (Bolin and Abbott 1963; Gar-
rison 1979). In contrast, the ODC period exhibits
minimal upwelling, frequent downwelling, and low
productivity (Bolin and Abbott 1963; Garrison 1979).
Data from individuals collected during the latter
seasons were pooled because these periods were not
readily distinguishable (Grossman in press b). Con-
sequently, comparisons of 0. snyderi food habits and
length-weight relationships represent contrasts
between a high productivity period (Upwelling, all
months from April to August, plus March 1980) and
the low productivity ODC period (October-February,
plus March 1979). Monthly mean water temperatures
ranged from 9.7° to 11.9°C during the Upwelling
period from 11.2° to 14.2° C during the ODC period
(Grossman in press b).
Length-Weight and Growth Calculations
Regressions of individual weight versus standard
length were calculated separately for males and
females collected in the Upwelling and ODC periods.
Regression equations were of the form W = aL'',
fitted as In M^ = In a + 6 In L. Slopes (b) of regres-
sion equations for males and females were compared
for each period by analysis of covariance (ANCOVA).
Seasonal differences between slopes also were ex-
amined for each sex.
Regression slopes for the two sexes and periods
were divided by their correlation coefficients to
estimate slopes for geometric mean functional
regressions of weight versus length (Ricker 1973).
Functional regressions are recommended for
describing relations between weight and length
because both variables are subject to natural
variability (Ricker 1973). Functional regression
slopes were used to derive ^/-intercepts from the
equation y-int. = y - {b/r)x (Ricker 1973). These
slope estimates were employed to calculate instan-
taneous rates of growth in weight (G) as
G = (blr) (In L2 - In Lj), (Ricker 1975),
where b/r = slope of the functional length-weight
646
regression;
Lj = mean length at the time t; and
L2 = mean length at time ^ -1- 1.
Growth rates were calculated for individual year
classes which were separated using length-frequency
distributions. lb compare growth rates for males
and females, ^tests for paired samples were used.
Sex ratios for the 1979 samples were tested for
deviations from unity using chi-square tests cor-
rected for continuity.
Dietary Analyses
Stomach contents were removed from a subsam-
ple (597 total) of the 0. snyderi collected between
January 1979 and July 1981. Ninety-seven percent
of stomachs examined contained food. Prey were
identified to the lowest possible taxon and weighed
(wet) to the nearest milligram. The weights of each
prey type were pooled separately for males and
females from each collection. Diets were then calcu-
lated as the percent of the total stomach content
weight attributable to each prey typa The number
of fish containing each prey type (i.a, prey frequen-
cy of occurrence, henceforth FO) also was recorded.
Dietary data were pooled across collections wdthin
the Upwelling and ODC periods for each sex, to com-
pare feeding habits between sexes and seasons.
Because the study period spanned 3 yr, it also was
possible to quantify among year variability in
seasonal and sex-specific feeding habits. Sex-linked
ontogenetic dietary changes were examined by
separating males and females into 20 mm size classes
and comparing prey consumed by each size class in
different seasons and years. Niche breadth was
calculated as I l/p,;^ (Levins 1968), where p, is the
proportion of the total prey weight comprised of the
ith prey type. Only prey types constituting at least
1% of the total prey weight were included in niche
breadth calculations. Niche breadth was compared
among size classes by using the Wilcoxon signed-
rank test.
RESULTS
Length-Weight Relationships
The slope for the male length-weight regression
for the Upwelling period was significantly greater
than that for females (ANCOVA, F = 12.875, P <
0.001; T^ble 1). Slopes of length-weight regressions
for males and females collected during the ODC
period were not significantly different (ANCOVA,
FREEMAN ET AL.: LIFE HISTORY OF FLUFFY SCULPIN
Table 1.— Length-weight relationships, described as W^ = a/.'', for
Oligocottus snyderi. Coefficients for the least-squares (In W = \r\
a + bin L) and functional (In IV = In a' -h (bir) In L) regressions
are presented, as well as the correlation coefficients for the least-
squares regressions (r) and the number of individuals used in each
regression (A/). ODC = Oceanic-Davidson Current.
Least-squares
regression
Functional
regression
N
r
a
b
a'
bIr
Males
Upwelling
150
0.984
0.0000178
3.097
0.0000146
3.147
ODC
112
0.973
0.0000253
2.991
0.0000182
3.075
Females
Upwelling
164
0.972
0.0000472
2.835
0.0000346
2.917
ODC
131
0.976
0.0000202
3.069
0.0000151
3.143
F = 0.736, P > 0.25). Seasonal comparisons for each
sex showed that tlie male Upwelling and ODC slopes
were not significantly different (ANCOVA, F =
1.483, P > 0.10), whereas the females had a
significantly higher slope during the ODC period
(ANCOVA, F = 6.147, P < 0.025).
Growth Rates
Length-frequency histograms for 0. snyderi at
Dillon Beach indicated that two year classes were
present on most dates (Fig. 1). Recruitment began
in spring and peaked during summer. The onset of
recruitment differed between years. Age O-i- fish
were first taken in May of 1979; however, in 1980
recruitment began in March. Age O-i- individuals of
the 1979 cohort grew 20 mm in length (from 20-25
to 40-55 mm SL) by December of their first year.
Members of the 1978 cohort (= age l-i- fish) in-
creased in length from 40-55 to 60-70 mm SL dur-
ing spring, summer, and fall 1979. Individuals did
not appear to survive a second winter during 1980,
although a few males recruited in 1977 may have sur-
vived until spring of 1979 (Fig. 1).
Sex ratios for the O-i- age class were significantly
different from unity in the August 1979 collection
in which there were significantly more males than
females (1.7:1; x^ = 7.32, P < 0.01). Age 1+ females
significantly outnumbered males in January 1979
(4:1; x^ = 6.05, P < 0.025), July 1979 (1.8:1; x^ =
4.38, P < 0.05), and December 1979 (3:1; x^ = 5.04,
P < 0.025).
Instantaneous growth rates were calculated for
males and females from the two year classes pres-
ent in 1979 (Tkble 2). Prolonged recruitment (lasting
from May through August) resulted in apparent
depressed spring and summer growth rates for the
age O-I- class when all individuals were included in
the calculations of mean lengths (Tkble 2). Therefore,
fish which appeared to have been recruited later than
the majority of the class were excluded from con-
sideration in the June, July, and August calculations,
as shown in Figure 1. Only the very large males col-
lected in January 1979 were excluded from the age
1 + mean length calculations, as these individuals ap-
parently were survivors from the 1977 year class and
probably died shortly thereafter. The highest
monthly instantaneous growth rates were obtained
during May and June, averaging 0.860 and 0.655 for
age O-I- males and females, and 0.209 and 0.188 for
age 1 -I- males and females (Tkble 2, Fig. 2). Growth
rates markedly decreased after August, averaging
0.065 and 0.169 for age O-i- males and females, and
0 and 0.061 for age l-i- males and females during
October and November (Ikble 2, Fig. 2).
Males and females attained nearly equal lengths
in the first season of growth; however, age 1 -i- males
displayed significantly greater mean lengths (^tests,
P « 0.05) than age 1 + females from June through
November 1979 (Fig. 2). Growth rates were not
significantly higher for males than females in either
size class when compared from January to
December 1979 (age 0 + :^ = 1.002, P> 0.1; age 1 + :
t = 1.232, P > 0.1); however, if only the data from
January to October are included for the age 1 + class,
males did have significantly higher growth rates (t
= 2.255, P < 0.05). This discrepancy is caused by the
low numbers of age 1 -i- fish collected in November
(14) and December (24). Length-frequency histo-
grams (Fig. 1) also show that age l-i- males are
larger than females, whereas length distributions are
Table 2. — Instantaneous growth rates of Oligocottus snyderi males
and females in their first (age O-i-) and second (age 1-t-) years of
growth. Rates were calculated for the intervals between the 1979
collections. Values in parentheses were calculated with all in-
dividuals included in the age O-i- cohort (see text).
Instantaneous growth rate
Collection
dates
Age
O-I-
Age
1 +
Males
Females
Males
Females
1-27-79
—
—
0.257
0.079
3-26-79
—
—
0.295
0.171
5-16-79
1.059(1.059)
0.718 (0.562)
0.318
0.204
6-13-79
0.661 (0.429)
0.591 (0.358)
0.099
0.171
7-12-79
0.352 (0.306)
0.295 (0.390)
0.111
0.074
8-09-79
0.303 (0.582)
0.124 (0.419)
0.164
0.063
10-07-79
0.129
0.149
0
0.122
11-04-79
—
0.188
—
—
12-04-79
647
FISHERY BULLETIN: VOL. 83, NO. 4
o
-a
cz
E
Figure L— Length-frequency distributions for
Oligocottus snyderi. Males and females are
separated in the 1979 collections, with females
shown below the axis. Arrows indicate divisions
between year classes 0 + and 1 + , and broken lines
designate limits for inclusion in cohort mean SL
calculations (January, June, July, and August
1979). The 1980 and 1981 collections are included
for comparison, but the sexes are not shown
separately.
Jan. 79
n=23.
^
^ Mar. 79
2- n=33 .
2- *
May '79
21-
2
J^ I
i
t
6 - n=49
t
fi Mar.'SO
^•^ n=32
^ Apr. 80
6- n=""
2 -
30 I
■ I Hi ■■
6r
Jun.79
Jun.'SO
n=98
Jul. 79
n=l45.
,0 Nov 80
2
Aug. 79
n=232
Jul.'8l
^ Nov. 79
2r n=3l
10 30 50 70
2-
•^rr
l^yp
HI
Dec. 79
I 1 1 1 1 1 r
10 30 50 70
Standard Length (nnnn)
648
FREEMAN ET AL.: LIFE HISTORY OF FLUFFY SCULPIN
70
£ 60
01
c
50 -
40 -
o
-o 30
c
o
tr> 20
I I I I
_LJ I
^6^
^51 <s; \ <s>^ "b <^. <?
Collection Dote, 1979
Figure 2.— Growth curves for age 0+ and 1+ Oligocottvs snyderi.
The standard lengths Q ± SE) of each sex in the two age classes
are shown for the 1979 collections. June, July, and August age 0 +
SLs do not include late recruited individuals (see text and Figure 1).
about equal for age 0+ males and females. The low
mean lengths calculated for age 0+ females in Octo-
ber and November resulted from the inclusion of
small individuals probably recruited late in Upwell-
ing, but which were not easily separable from the
remainder of the cohort. Hence, calculated growth
rates probably underestimate age 0 + female growth
from August to October and overestimate growth
from October to December.
Dietary Habits
Oligocottus synderi's diet at Dillon Beach consisted
primarily of gammarid amphipods and polychaetes.
Summed across all collections, gammarids composed
78% and 66% of the gut contents of females and
males, respectively. Polychaetes totaled 10% of the
female diet and 14% of the male diet. Shrimp re-
mains, mainly Heptacarpus taylori, contributed 5%
and 4% to female and male diets, respectively. A
total of 20 prey taxa were consumed by 0. snyderi;
however, no other prey category composed more than
3% of the diet, with the exception of unidentifiable
hard-bodied prey remains, which totaled 5% of the
gut contents of males. Dietary breadth based on all
collections was higher for males than females (2.17
vs. 1.61), because males consumed greater amounts
of minor prey types.
The major seasonal dietary changes for both males
and females were decreased gammarid consumption
and increased polychaete consumption during Up-
welling as compared with the ODC period (Tkbles
3, 4). Dietary breadth also was greater for both sexes
during Upwelling than in the ODC period (2.02 vs.
1.44 for females, and 2.19 vs. 2.09 for males). Dif-
ferences were observed between male and female
diets. Specifically, in the ODC period, gammarids
composed a greater proportion of female than male
diets (83% vs. 68%), whereas males consumed pro-
portionately more eggs, Idotea spp. (Isopoda), and
crabs (Ikble 4). Although standard lengths and
weights of ODC males (138) and females (132) used
for gut analyses were not significantly different (SL:
t = 1.058, P > 0.1; weight: t = 1.036, P > 0.1), females
had significantly greater amounts of food in their
stomachs (t = 4.857, P = 0.0001, Ikble 4). This dif-
ference is attributable to the weight of ingested gam-
marids because 131 (FO) females contained a total
of 8.4 g of gammarids, whereas 132 males contain-
ed only 4.3 g (total weight).
Examination of food habits across size classes
shows that larger individuals generally possessed a
more diverse diet than smaller individuals (Figs. 3,
4). Dietary breadth was significantly higher (Wilcox-
on signed-rank test, n = 12, T = 69, P < 0.01) for
50-69 mm SL fish than for 30-49 mm SL individuals
when compared across both sexes for all years. In-
dividuals <30 mm SL consumed mainly gammarids
and isopods; polychaetes and shrimp were major prey
only for larger fish. Pagurus spp. and crabs, in-
cluding Cancer spp. and Pachycheles spp., were found
only in individuals >40 mm SL.
The general observation of decreased gammarid
consumption by larger 0. snyderi, concomitant with
increased polychaete and shrimp consumption, ap-
plies to collections made throughout the 3-yr study
period. The majority of among year variation in food
habits resulted from the presence of large, rare prey
items in single individuals (Figs. 3, 4). An exception
was the high consumption of polychaetes by males
collected in July 1981 (Fig. 3). In this case, poly-
chaetes occurred in all of the 50-69 mm fish and in
56% of the 30-49 mm fish, and composed a con-
siderably higher proportion of the diet than during
previous Upwelling collections.
DISCUSSION
Age-Structure and Growth
At Dillon Beach, a habitat displaying marked
seasonal fluctuations in productivity (Grossman
1982, in press b; Grossman and deVlaming 1984), 0.
snyderi is short lived, with a maximum lifespan of
about 1.5 yr and a maximum length of about 70 mm
SL. Whereas two age classes were observed in this
study, Moring (1981) observed as many as three age
classes in Trinidad Bay. Standard lengths attained
649
FISHERY BULLETIN: VOL. 83, NO. 4
Table 3.— Food habits of male and female Oligocottus snyderi collected during the
Upwelling period. Values shown for each prey type are total weight ingested, percent
of total prey weight, and frequency of occurrence (FO).
Females, n =
164
Males, n =
150
y <?L + <=5D
45.9
± 11.7
mm
51.3
± 11.8
mm
Prey
Wt. (g)
% Wt.
(FO)
Wt. (g)
% Wt.
(FO)
Gammarids
3.850
68
(125)
3.653
64
(132)
Polychaetes
0.980
17
(19)
1.109
19
(33)
Heptacarpus taylorl
0.202
4
(4)
0.222
4
(5)
Crangon
0.146
3
(2)
0
Other shrimp
0.001
<1
(1)
0.004
<1
(1)
Hard-bodied prey rem.
0.196
3
(18)
0.494
9
(20)
Isopods
0.095
2
(10)
0.074
1
(19)
Idotea
0.006
<1
(2)
0.049
1
(3)
Pagurus
0.067
1
(1)
0
Crabs
0.036
1
(2)
0.026
<1
(1)
Algae
0
0.039
1
(9)
Snails
0.024
<1
(4)
0.010
<1
(3)
Caprellids
0.026
<1
(1)
0.004
<1
(2)
Soft-bodied prey rem.
0
0.014
<1
(1)
Barnacle cirri
0
0.012
<1
(5)
Total
5.629
99
5.710
99
Table 4. — Oligocottus snyder/ feeding habits during the combined Oceanic-Davidson
Current periods. Values shown for each prey are the weight ingested, percent of total
prey weight, and frequency of occurrence (FO).
Females, n =
132
Males, n =
138
X SL ± SD
Prey
49.5
-1- 8.8
mm
50.6
± 9.3
mm
Wt. (g)
% Wt.
(FO)
Wt. (g)
% Wt
(FO)
Gammarids
8.418
83
(131)
4.278
68
(132)
Polychaetes
0.611
6
(20)
0.587
9
(23)
Heptacarpus taylori
0.304
3
(3)
0.308
5
(4)
Crangon
0.089
1
(2)
0
Other shrimp
0.071
1
(1)
0
Eggs
0.008
<1
(1)
0.397
6
(6)
Idotea
0.131
1
(6)
0.252
4
(14)
Isopods
0.255
3
(19)
0.104
2
(16)
Sea anemones
0.147
1
(2)
0
Hard-bodied prey rem.
0.053
1
(2)
0.086
1
(4)
Pachycheles
0
0.091
2
(1)
Barnacle cirri
0.001
<1
(1)
0.075
1
(5)
Pagurus
0.043
<1
(2)
0
Bivalves
0
0.036
1
(1)
Algae
0
0.044
1
(9)
Caprellids
0.015
<1
(2)
0.003
<1
(1)
Cancer
0
0.005
<1
(1)
Crabs
0
0.002
<1
(1)
Snails
0.002
<1
(1)
0
Total
10.148
100
6.268
100
by the O-i- and l-i- age classes observed by Moring
(1981) were similar to those displayed by the Dillon
Beach age O-i- and 1+ classes; however, Moring
observed age 2+ individuals of up to 101 mm SL.
Nakamura (1976a, b) also reported collecting 0.
snyderi >80 mm SL at Port Renfrew, British Colum-
bia. These results indicate that 0. snyderi may have
a longer lifespan at more northerly locations. The
scarcity of individuals >70 mm SL at Dillon Beach
probably did not result from repeated sampling
because such large individuals were absent from the
initial samples and from collections made in
previously unsampled pools near the study site in
August 1979, December 1979, and April 1980. There
was no discernable pattern in sex-ratio deviations
from unity observed in four 1979 collections, which
650
FREEMAN ET AL.: LIFE HISTORY OF FLUFFY SCULPIN
<
c
o
©
20-29mm
n=7
Females
Upwelling Period
30-49mm
n=47
50-69mm
n=59
cj>
<
-3
I 20-29mm
o
n=3
Males
30-49mm
n=2l
50-69mm
n=68
O
00
d
3
■^
wT
Q.
<
20-29mm
n = 4
30-49mm
n=l6
50-69mm
n = ll
O
_oo
d
3
20-29mm
n=5
30-49mm
n=22
50-69mm
n = ll
-» io«
00
3
-3
IO-29mm 30-39mm
n=6 n=5
50-69mm
n = 9
CO
3
-3
30-49nnm
n=9
SnxL-PRS
50-69mm
n = ll
Figure 3.— Sex-specific ontogenetic and among year variation in Oligocottus snyderi feeding habits during the 1979, 1980, and 1981 Upwell-
ing periods. Prey are represented as percent total prey weight, and only prey composing >1% of the total prey weight are shown. Asterisks
indicate prey which occurred in only one individual. Prey abbreviations are G (gammarids); PR (hard-bodied prey remains); Po (polychaetes);
Is (isopods); S (shrimps, all spp.); Ca (caprellids); Sn (snails); Id (Idotea spp.); Pa (Pagurus spp.); Cr (crabs, all spp.); Al (algae); and BC
(barnacle cirri).
suggests that males and females have about equal
lifespans at Dillon Beach.
Oligocottus maculosus Girard, another abundant
intertidal cottid (Nakamura 1976a, b; Moring 1981),
was estimated by Chadwick (1976) to survive as
many as five growing seasons, based on counts of
vertebral rings, at Port Renfrew, B.C., and Bruels
Point, CA. Annuli were not validated in this study,
however, and it is questionable if the rings observed
were actually formed once yearly. In addition, Chad-
wick's (1976) growth rate estimates are extremely
low, suggesting that 0. maculosiis grew no more than
7 mm in any season after the first. Moreover, all
previous studies of both 0. snyderi (Moring 1981)
and 0. maculosus (Atkinson 1939; Green 1971; Mor-
ing 1979) showed that populations of these species
were composed primarily of age 0-t- and l-i- in-
dividuals, as was 0. snyderi at Dillon Beach. Conse-
quently, it appears unlikely that 0. maculosus sur-
vives to age 5-f as suggested by Chadwick (1976),
and in any case such longevity was not observed for
0. snyderi at Dillon Beach.
Intertidal fishes appear to display several distinct
life history patterns. Short lifespan (1-3 yr), early
maturation, and high reproductive effort have been
reported for several intertidal gobies in northern
temperate habitats (Gibson 1969, 1982; Grossman
1979; Miller 1979). In contrast, lifespans of 4 to over
10 yr, accompanied by delayed maturation, have been
observed in many intertidal species, including gobiids
and blenniids (Gibson 1969, 1982; Stephens et al.
1970; Grossman 1979; Miller 1979). Little informa-
tion is available for intertidal cottids. The largest
North American cottid, Scorpaenichthys mar-
moratus Ayers, may live 13 yr, but only inhabits tide-
pools during its first or second year of life (O'Con-
nell 1953; Grossman and Freeman unpubl. data).
Another large sculpin, Leptocottus armatvs Girard,
common in the Pacific coast bays and estuaries, is
known to live to age 3 and reaches sexual maturity
651
FISHERY BULLETIN: VOL. 83, NO. 4
(7>
c
a
cn
Q
>■
o
_co
o"
_CD
O
o
O
Oceanic-Davidson
Females
30-49 mm
n = 2l
PRfls
30-49mm
n=20
30-49mm
n=27
Id D^» r«
50-59mm
n=l3
Current Periods
Males
40-49mm
n=6
50-69mm
n=45
50-69mm
n=5
50-69mm
n=6
o 30-49mm
^ n=24
50-69mm
n=38
^ 30 -49 mm
S n=40
50-69mm
n=20
70-79mm
n=4
Figure 4.— Sex-specific ontogenetic and among year variation in Oligocottus snyderi feeding habits during the
three ODC (Oceanic-Davidson Current) periods encompassed by this study. Prey are represented as percent
total prey weight; only prey composing >1% total prey weight are shown. Asterisks indicate prey occurring
in only one individual. Abbreviations are as in Figure 3, with the addition of E (eggs); An (sea anemones);
and Bi (bivalves).
after 1 yr (Jones 1962; Tksto 1975). Oligocottiis
snyderi and 0. maculosus apparently are best
characterized by the short hfespan, early matura-
tion, life history pattern. This conclusion is based
on growth rate data coupled with the scarcity of in-
dividuals older than 1.5 yr, and data showing early
maturation and high reproductive effort for 0.
snyderi (deVlaming et al. 1982).
The majority of age 0+ 0. snyderi at Dillon Beach
attained sufficient size to spawn during their first
year; it is less certain what proportion of these in-
dividuals survive to spawn in their second year.
Grossman and deVlaming (1984) indicated that, at
Dillon Beach, females mature at about 40 mm SL
and contain vitellogenic oocytes from October
through May. These females also probably spawn
more than once, primarily during winter and spring
(Grossman and deVlaming 1984). Length-frequency
distributions from March and May 1979 and March
and April 1980 show that a single age class
dominated the population. Hence, assuming that
recruitment primarily was derived from this popula-
tion, age 1+ individuals (recruited the previous
spring and summer) must have been responsible for
nearly all spring spawning. The paucity of large in-
dividuals (i.e., >60 mm SL) in winter or spring
samples indicates that if individuals spawned in their
second year, this reproduction must have occurred
prior to January. Substantial numbers of age 1 -i- in-
dividuals were captured from October to December
1979 and in November 1980. Although the earliest
recruitment observed at Dillon Beach occurred in
March 1980, Moring (1981) captured newly recruited
individuals as early as January. This suggests that
fall spawning may occur in more northerly popula-
tions of 0. snyderi.
Reproduction apparently is timed to insure that
larvae metamorphose during upwelling. Grossman
(1982) found a significant correlation between up-
welling activity and the number of resident species
with young-of-the-year present at Dillon Beach.
Grossman and deVlaming (1984) also observed that
0. snyderi recruitment was strongly correlated with
productivity; the authors pointed out that the early
652
FREEMAN ET AL.: LIFE HISTORY OF FLUFFY SCULPIN
recruitment observed in March 1980 coincided with
the onset of upwelling, whereas both recruitment and
upwelHng were delayed until May 1979.
If some individuals do survive to reproduce dur-
ing their second year, the larger sizes attained by
males during their second growing season may be
advantageous during spawning. This is because male
0. snyderi have a lengthened and prehensile first
anal ray with which they clasp females during
copulation, and the larger a male is in relation to a
female, the more efficiently he will be able to clasp
her (Morris 1956).
Dietary Habits
Oligocotttcs snyderi at Dillon Beach consumed
primarily gammarid amphipods and polychaetcs.
These data are consistent with previous observations
(Johnston 1954; Nakamura 1971; Yoshiyama 1980),
although they differ somewhat from results obtain-
ed by Cross (1981) from two sites in northern Wash-
ington. Cross (1981) reported that harpacticoid
copepods were a major prey for 0. snyderi at one
site; similarly, polychaetes also were consumed only
at one site However, Cross (1981) also observed high
gammarid consumption by 0. snyderi, as well as by
most other intertidal species he studied. In addition,
gammarids have been cited as a major prey in other
intertidal fish assemblages (Mitchell 1953; Johnston
1954; Zander 1979, 1982; Grossman in press b). At
Dillon Beach, gammarids frequently were consum-
ed by resident and seasonal intertidal fishes,
although only one other resident (Apodichthys
flavidus Girard) possessed a diet dominated by gam-
marids (Grossman in press b). Among year, seasonal
comparisons, however, show that a variety of minor
prey types also are consumed by 0. snyderi.
Combinations of shrimps, crabs, hermit crabs,
Idotea, and other irregularly consumed prey con-
stituted a considerable proportion of 0. snyderi's diet
throughout the year. This was particularly evident
in larger fish, which suggests that capture of these
prey is either more difficult for small fish due to mor-
phological, physiological, or behavioral constraints,
or involves increased predation risk. Similarly, a shift
from gammarids to larger prey concomitant with in-
creasing length was observed for the majority of
intertidal fishes at Dillon Beach (Grossman in press
b), and for some species studied by Cross (1981). In
contrast, Yoshiyama (1980) was unable to detect
dietary differences between small and large 0.
snyderi, or two other intertidal cottids. Yoshiyama
pooled small samples collected throughout a year,
however, which may have obscured seasonal changes
in prey consumption. Because his samples were
small, Yoshiyama also may have underestimated con-
sumption of rare prey.
Although seasonal dietary changes were minor,
there is evidence that females possessed higher in-
gestion rates than males during the ODC period.
During this season of lowered productivity, females
consumed two times more gammarids (by weight)
than males, although mean fish length and gam-
marid frequency of occurrence were nearly identical
between sexes. This difference between consumption
rates may not be artifactual. Females develop and
carry vitellogenic eggs during this period (Grossman
and deVlaming 1984), and consequently have high
energy demands. There was no evidence that inter-
sexual or ontogenetic dietary differences resulted
from differential distribution or collection
disturbance
The high prey weight observed in males and
females collected during the ODC period is of in-
terest in light of the low growth rates observed dur-
ing winter months. Moring (1979, 1981) also ob-
served cessation of growth during winter for both
0. snyderi and 0. maculosus in northern California.
He suggested that reduced foraging activity caused
by increased wave action during winter might par-
tially explain this growth reduction. Dietary data
from Dillon Beach do not support this conclusion
because ODC specimens contained a greater total
weight of prey than individuals collected during
Upwelling, even though a greater number of in-
dividuals were examined during the latter period.
The Dillon Beach study site probably is more
sheltered from winter storm activity, however, than
the Trinidad Bay sites observed by Moring (Gross-
man pers. obs.). In the absence of ingestion rate data
for both seaons, results based on gut content weight
alone are equivocal. Moring (1981) also suggested
that gonadal development during the winter months
might be responsible for reduced growth; this could
also apply to 0. snyderi at Dillon Beach.
In conclusion, 0. snyderi the most abundant inter-
tidal cottid at Dillon Beach, possesses a suite of
characteristics which suggest that productivity has
influenced the biology and behavior of this species.
For example, 0. snyderi reaches sexual maturity dur-
ing its first year of life, and spawns at a time which
enables recruitment to take place during the season
of highest productivity (i.e, Upwelling (Grossman and
deVlaming 1984)). Grossman (1982, in press b)
presented strong evidence that productivity cycles
also affect many other species at Dillon Beach,
because this assemblage appears to be organized
through interspecific exploitative competition for
653
FISHERY BULLETIN: VOL. 83, NO. 4
food. Recuitment and numerical abundances within
this assemblage also were strongly correlated with
productivity (Grossman 1982). Oligocottus snyderi
possesses a variety of adaptations (ag., rapid matura-
tion, high female reproductive effort, utilization of
an abundant prey not widely consumed by other
assemblage members) which probably are responsi-
ble for its numerical dominance in a fluctuating
environment.
ACKNOWLEDGMENTS
We thank the many friends and colleagues who
aided in the collection and analysis of data. Jeff Bar-
rett, Dan Erickson, Doug Facey, Margi Flood, Steve
Floyd, and Joe Hightower reviewed the manuscript
and their comments are greatly appreciated. We also
appreciate the help of Bonnie Fancher who typed
various drafts of this manuscript.
LITERATURE CITED
Atkinson, C. E.
1939. Notes on the life history of the tidepool johnny (Oligocot-
tus maculosus). Copeia 1939:23-30.
BoLiN, R. L., AND D. P. Abbott.
1963. Studies on the marine chmate and phytoplanliton of the
central coastal area of California, 1954-1960. Calif. Coop.
Oceanic Fish. Invest. Rep. 9:23-45.
Chadwick, E. M. R
1976. A comparison of growth and abundance for tidal pool
fishes in California and British Columbia. J. Fish Biol.
8:27-34.
Cross, J. N.
1981. Structure of rocky intertidal fish assemblage Ph.D.
Thesis, Univ. Washington, Seattle, 259 p.
deVlaming, v., G. D. Grossman, and F. Chapman.
1982. On the use of the gonosomatic index. Comp. Biochem.
Physiol. 73A:31-39.
Garrison, D. L.
1979. Monterey Bay phytoplankton. I. Seasonal cycles of
phytoplankton assemblages. J. Plankton Res. 1:241-265.
Gibson, R. N.
1969. The biology and behavior of littoral fish. Oceanogr.
Mar. Biol. Annu. Rev 7:367-410.
1982. Recent studies on the biology of intertidal fishes.
Oceanogr. Mar. Biol. Annu. Rev 20:363-414.
Green, J. M.
1971. Local distribution of Oligocottus maculosus Girard and
other tidepool cottids of the west coast of Vancouver Island,
British Columbia. Can. J. Zool. 49:1111-1128.
Grossman, G. D.
1979. Demographic characteristics of an intertidal bay goby
(Lepidogobius lepidus). Environ. Biol. Fishes 4:207-218.
1982. Dynamics and organization of a rocky intertidal fish
assemblage: the persistence and resilience of taxocene struc-
ture Am. Nat. 119:611-637.
In press a. Long term persistence in a rocky intertidal fish
assemblage Environ. Biol. Fishes.
In press b. Division of food resources among fish of the rocky
intertidal zone J. Zool. (Lond.).
Grossman, G. D., and V. deVlaming.
1984. Reproductive ecology of female Oligocottus snyderi
Greeley: a North American intertidal sculpin. J. Fish Biol.
25:231-240.
Johnston, R. F.
1954. The summer food of some intertidal fishes of Monterey
County California. Calif. Fish Game 40:65-68.
Jones, A. C.
1962. The biology of the euryhaline fish Leptocottvs anmatus
armatus Girard (Cottidae). Univ. Calif, Publ. Zool. 67:
321-367.
Levins, R.
1968. Evolution in changing environments. Princeton Univ.
Press, Princeton, 120 p.
Miller, D. J., and R. N. Lea.
1972. Guide to the coastal marine fishes of California. Calif.
Dep. Fish Game, Fish. Bull. 157, 235 p.
Miller, P. J.
1979. Adaptiveness and implications of small size in teleosts.
In P. J. Miller (editor), Fish phenology: anabolic adaptiveness
in teleosts, p. 263-306. Zool. Soe Lond. Symp. 44.
Mitchell, D. F.
1953. An analysis of stomach contents of California tidepool
fishes. Am. Midi. Nat. 49:862-871.
Moring, J. R.
1979. Age structure of a tidepool sculpin, Oligocottus macu-
losus, population in northern California. Calif. Fish Game
65:111-113.
1981. Seasonal changes in a population of the fluffy sculpin,
Oligocottus snyderi, from Trinidad Bay, California. Calif
Fish Game 67:250-253.
Morris, R. W.
1956. Clasping mechnisms of the cottid fish Oligocottus
snyderi Greeley Pac Sci. 10:314-317.
Nakamura, R.
1971. Food of two cohabiting tide-pool Cottidae J. Fish. Res.
Board Can. 28:928-932.
1976a. Experimental assessment of factors influencing micro-
habitat selection by two tidepool fishes Oligocottus maculosus
and 0. snyderi. Mar. Biol. (Berl.) 37:97-104.
1976b. Tfemperature and the vertical distribution of two tide-
pool fishes (Oligocottus maculosus, 0. snyderi). Copeia 1976:
143-152.
O'CONNELL, C. R
1953. Life history of the cabezon Scorpaenichthys marmora-
tus (Ayres). Calif Dep. Fish Game, Fish. Bull. 93, 76 p.
Parrish, R. H., C. S. Nelson, and A. Bakun.
1981. Transport mechanisms and reproductive success of
fishes in the California Current. Biol. Oceanogr. 1:175-203.
Ricker, W. E.
1973. Linear regressions in fishery research. J. Fish. Res.
Board Can. 30:409-434.
1975. Computation and interpretation of biological statistics
of fish populations. Fish. Res. Board Can., Bull. 191, 382 p.
Stephens, J. S., Jr., R. K. Johnson, G. S. Key, and J. E.
McCOSKER.
1970. The comparative ecology of three sympatric species of
California blennies of the genus Hypsoblen nius Gill (Tteleo-
stomi, Blenniidae). Ecol. Monogr. 40:213-233.
Tasto, R. N.
1976. Aspects of the biology of the Pacific staghorn sculpin,
Leptocottus armatus Girard, in Anaheim Bay. Calif Dep.
Fish Game, Fish. Bull. 165:123-135.
YOSHIYAMA, R. M.
1980. Food habits of three species of rocky intertidal sculpins
(Cottidae) in central California. Copeia 1980:515-525.
654
FREEMAN ET AL.: LIFE HISTORY OF FLUFFY SCULPIN
1981. Distribution and abundance patterns of rocky intertidal stony ground off M0n, Denmark. Ophelia 18:179-190.
fishes in central California. Environ. Biol. Fishes 6:315-332. 1982. Feeding ecology of littoral gobiid and blennioid fish of
Zander, C. D. the Banyuls area (Mediterranean Sea). I. Main food and
1979. On the biology and food of small-sized fish from the trophic dimension of niche and ecotopa Vie Milieu 32:1-10.
North and Baltic Sea areas. II. Investigations of a shallow
655
VARIABILITY, TRENDS, AND BIASES IN REPRODUCTIVE RATES OF
SPOTTED DOLPHINS, STENELLA ATTENUATA
Jay Barlowi
ABSTRACT
Tfemporal changes were examined in three parameters that affect reproduction of spotted dolphin popula-
tions in the eastern Pacific Of mature females, percent pregnant decreased markedly from the period
1971-73 to the period 1974-83. Within the period 1974-83, percent pregnant remained relatively constant.
Of pregnant females, percent lactating increased during the period 1971-83. The percentage of sexually
mature females did not change Potential biases in the measurement of the three parameters were iden-
tified by examining the effects of sampling conditions. The percentage of mature females that are preg-
nant and the percentage of pregnant females that are lactating were found to be robust to sampling con-
ditions. The percentage of mature females in a sample was found to depend significantly on the number
of dolphins killed per set, and annual variability was too large to be explained by random sampling error.
Comparisons between two populations show that the more exploited population has a lower percent preg-
nant, although the opposite might be expected from density compensatory effects. Percent lactating and
percent immature were higher in the more exploited population.
Changes in the reproductive parameters of cetacean
populations can be used to make inferences about
the status or general "health" of a population. For
instance, increases in pregnancy rates and decreases
in the age at attainment of sexual maturity were link-
ed to reductions in Antarctic whale populations
(Gambell 1975). Re-analysis of these data, however,
revealed unsuspected biases, and Gambell's results
are now being questioned (Mizroch 1983). The pur-
pose of this paper is to examine potential biases in
measuring reproductive rates of spotted dolphins,
Stenella attenuata. This species is taken incidentally
in the tuna purse seine fishery in the eastern tropical
Pacific (Smith 1983). The intent is to determine
whether reproductive rates can be measured with
sufficient precision to monitor intrapopulation
changes or to make interpopulation comparisons.
Previous studies of female reproduction in spot-
ted dolphins of the eastern Pacific have shown an
apparent decrease in pregnancy rates from 1973 to
1975 (Perrin et al. 1977), from 1973 to 1978,^ and
from 1971 to 1978 (Hester 1984). Hester (1984) sug-
gested that this decline in pregnancy rates is related
to the decline in fishing-related dolphin mortality
during the same time period.
'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, La Jolla, CA 92038.
^Henderson, J. R., W. F Perrin, and R. B. Miller. 1980. Rate
of gross annual reproduction in dolphin populations {Stenella spp.
and Delphinics delphis) in the eastern tropical Pacific, 1973-78.
Admin. Rep. LJ-80-02, 51 p.; available from Southwest Fisheries
Center La Jolla Laboratory, National Marine Fisheries Service,
NOAA, P.O. Box 271, La Jolla, CA 92038.
Three indices of the reproductive status of female
spotted dolphins are examined in the present paper:
1) the fraction of sexually mature individuals that
are pregnant, 2) the fraction of pregnant females
that are lactating, and 3) the fraction of females that
are sexually mature These measures have been used
previously in calculating what has been termed the
gross annual reproductive rate (GARR) of spotted
dolphins (Perrin et al. 1976). This paper reexamines
data from 1971 to 1978 plus additional data from
1979 to 1983 to determine whether the previously
noted trends in reproductive rates are real, and if
so, whether they are continuing. Also, factors are ex-
amined which may be biasing estimates of reproduc-
tive rates and which could be causing spurious
changes in apparent pregnancy rates and GARR.
Finally, differences in these reproductive indices be-
tween two geographic stocks of spotted dolphin are
discussed in view of their different histories of in-
cidental fishing mortality.
MATERIALS
Reproductive data were collected from a sample
of the dolphins killed in tuna purse-seining opera-
tions in the eastern tropical Pacific (ETP). Three
stocks of spotted dolphins are recognized in this area
based on morphological differences (Perrin et al.
1979). Samples considered here include two of these:
the northern offshore stock which has been subject
to tuna fishing since 1959 and the southern offshore
stock which has been subject to exploitation since
Manuscript accepted January 1985.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
657
FISHERY BULLETIN: VOL. 83, NO. 4
the early 1970's. In 1971 and 1972, field technicians
collected samples predominantly from females with
the "adult" or fused color pattern (Perrin 1970).
Beginning in 1973, field technicians were instructed
to collect samples nonselectively with respect to size
and sex. Operationally, this meant working-up speci-
mens in the order in which they appeared on the
deck of the tuna vessel. Sampling methods and
laboratory procedures are described in detail by Per-
rin et al. (1976). Sample locations are shown in
Figure 1.
Reproductive tracts of mature and nearly mature
females were preserved in the field for laboratory
examination. In 1971 and 1972, the definition of
"mature and nearly mature" was not explicit. In
1973, "mature and nearly mature" was defined as
individuals with "mottled" or "fused" developmen-
tal color phases (Perrin 1970). Because females in
the younger "speckled" color phase occasionally were
found to be pregnant, "mature and nearly mature"
was redefined operationally (beginning in 1974) as
specimens >150 cm total length (TL, measured from
tip of rostrum to fluke notch). Laboratory examina-
tion of preserved ovaries was used to determine the
presence of corpora from past ovulations. Pregnancy
was determined by visual examination of the uterus
(in later years, fetuses >30 cm TL were removed and
measured in the field). Mammary glands were slit
and checked in the field for the presence of milk.
In addition to the above life history information,
field technicians collected data pertaining to condi-
tions under which the samples were taken. Informa-
tion used in this report includes the observer's
estimate of the size of the school from which the
sample was taken, the duration of the chase before
the net was set, the number of dolphins known to
be killed during fishing operations, and the
geographic location at which the sample was taken.
METHODS
Three indices of female reproduction are con-
sidered in this paper: the percent pregnant, the per-
cent lactating, and the percent mature. Tbmporal
trends in these three indices were examined by
regressing annual means against year (weighting by
the inverse of binomial variances).
In calculating the percentages of mature females
that were pregnant and that were lactating,
specimens were used only if both ovaries were col-
lected and if at least one corpus of ovulation (cor-
pus albicans or corpus luteum) was present.
Previously, 1971 and 1972 samples were excluded
from calculation of percent pregnant because of
undersampling of younger females with a mottled
color pattern (Perrin et al. 1977). This was not deem-
ed necessary in this study, because in 1973-83
samples the percent pregnant for mature mottled
females (31.1%) was essentially the same as that for
mature females with a fused color pattern (31.4%).
In calculating the percentage of females that were
sexually mature, two different criteria were used for
determining maturity. In the majority of cases both
ovaries were examined, and the presence of one (or
more) corpus of ovulation was taken as evidence of
sexual maturity. If ovaries were not collected or ex-
amined (which was true for about 30% of females
over 150 cm TL), a length criterion was used for
maturity. Samples from 1971 and 1972 were ex-
cluded from these analyses because sampling was
not random in those years. i
"Length at attainment of sexual maturity" was
determined by the method used by Perrin et al.
(1977). Based on the sample for which ovaries were
examined, this length was estimated as the length
at which the number of longer immature individuals
equals the number of shorter mature individuals. For
the northern stock, the length at the onset of sex-
ual maturity was determined independently for each
year 1974-83 (176.5, 177.5, 177.0, 177.0, 178.0, 177.5,
179.0, 178.5, 180.0, and 182.0 cm, respectively). In
1973 the decision to collect ovaries was not based
on specimen length. The apparent trend in these
data yields a significant regression (P = 0.0008);
hence, regression estimates were substituted for an-
nual estimates for 1974-83, with an extrapolation to
1973. These values were 175.6, 176.1, 176.6, 177.1,
177.6, 178.0, 178.5, 179.0, 179.5, 180.0, and 180.5 cm,
respectively, for 1973-83. For the southern stock, in-
sufficient data exist to calculate a length at attain-
ment of sexual maturity for individual years, hence
the collective value was used for all years (175.0 cm).
Six factors were examined to determine whether
annual changes in the above percentages of pregnant
females were caused or affected by changing biases
in the sampling methods. These factors include 1)
geographical provenance, based on two strata (Fig.
1) which roughly correspond to the historical tuna
fishing grounds (inside the Commission Yellowfin
Regulatory Area, CYRA) and a more recently ex-
ploited area (outside the CYRA); 2) the quarter of
the year; 3) the length of chase, or the time between
sighting the dolphin school and capture (net set); 4)
the observer's estimate of the dolphin school size
(only available since 1973); 5) the number of dolphins
known to have been killed in the set; and 6) the total
number of tons of tuna caught in the set.
The selection of these six factors was guided to
658
BARLOW: REPRODUCTIVE RATES OF SPOTTED DOLPHINS
N „S£ N ,0£ N „S2 N „02 N „SI N „0I N „S
S ? S „0I S „SI S n2
3aniiiun
3
his]
ter,
in
rs.
ce M
2 (U
3
-5 -^
O
00
^.22
'^ 1^
T3 *
c §
2
*l
o
Ct. s
LT)
a o
OO
03 M
S r
1^
Z
to o
a
35^
S
.S 2
JS ""
a. (u
3
o ^
-O at
IT)
C35
"^ 'i
a "
P (M
:z
-b 9
o
O 00
O
S '-^
O
1-^
3
^'^
.a c
in
o
tl
&,<
o «J n^
2
a,B^
o
O
o|§
1 £<
— •
S -2 <^
3
cS S .f
t^
aj s
i2 ^
00 t3 .
— E-.
2.S^
3 C£)
o 2
o O
f^ _J
3
■K i'^
o
;sc2s^
•-*
-73 ^ =«
a) o , -
3
^ ;S :S
O
to
u 5 ^
<u m
fe .2 ■-»
3
^ So
22 £
.S o if
LD
^ o -S
to
T3 ■" _.
-§ o«
3
:g fe S
O
•—*
a> ^ «.
13 c ^
3
^ fe d"
^ Sfi 'E
g ^ a)
^ -2 S
n! j5 o
3
o
in
x: a> ^
•— «
c« 13 2^
3
22 "o 3
3
§ » .&
LD
m
'^ rA^
o <^
O 00 ^
3
►J 00 <;
3
o
1. ^g
i-H i-H >-l
S "5£.
as <u ^-^
§ P 2J
659
FISHERY BULLETIN: VOL, 83, NO. 4
some extent by previous studies. The sex ratio and
the fraction of yearhng dolphins in a sample were
found to vary with kill size (No. 5 above). The frac-
tion of neonatal animals in tuna-vessel samples was
found to vary significantly with area, season, chase
time, dolphin kill, and tuna catch (Nos. 1, 2, 3, 5, and
6 above)^. Preliminary work by A. A. Hohn* and M.
D. Scott^ has indicated that immature spotted
dolphins may segregate into schools with different
characteristic school sizes (No. 4 above).
The significance of each of the above factors was
tested separately using a Pearson chi-squara For
each test, the null hypothesis was that either per-
cent pregnant, percent lactating, or percent mature
is independent of the factor being tested. If this
hypothesis is shown to be false, then it is likely that
reproductive parameters may be affected by sam-
pling bias. Unfortunately, the above sampling fac-
tors are not independent; a factor may appear signifi-
cant when, in fact, that factor is merely correlated
with a causative factor. Because of this, probabilities
should be interpreted with caution.
Multiway comparisons were used to discriminate
factors which are truly important from those which
are correlated to significant factors. A hierarchical
approach was used, based on the log-linear model
for discrete multivariate analysis (program
BMDP4F, Dixon 1981). The above 2-way tests were
used to identify factors that may be significant. The
factors that were significant in the 2-way tests were
used in 3-way tests. The factors which proved signifi-
cant in the 3-way tests were then included in 4-way
tests (which proved to be a practical upper limit on
multiway tests using our data set). In this manner,
multiway comparisons of factors could be tested,
whereas a 7-way test of all factors would not have
been feasible.
Analysis of variance (ANOVA) was tried and re-
jected as an alternative to the log-linear model for
multiway comparisons. The method used in this trial
was to calculate percent pregnant for each set and
to use sets as replicates in an ANOVA. Although
ANOVA is recognized to be robust to violations in
assumptions, the sample size for individual sets is
very small (mean number of mature females per set
is 1.6, mode is 1). As a result, the percent pregnant
in 72% of sets was either 0% or 100% of mature
females. No transformation was able to normalize
these data. Using an arc-sine transformation, 2-way
ANOVA was not even able to recognize the four
significant factors affecting percent pregnant that
were identified using a simple Pearson chi-squara
Because of these problems, the ANOVA model was
rejected for use in the multiway comparisons.
RESULTS
^Powers, J. E., and J. Barlow. 1979. Biases in the tuna-net sam-
pling of dolphins in the eastern tropical Pacific Doc SOPS/79/31,
7 p.; available from Southwest Fisheries Center La JoUa Laboratory,
National Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla,
CA 92038.
*A. A. Hohn, NOAA, National Marine Fisheries Service; P.O. Box
271, La Jolla, CA 92038, pers. commun. November 1983.
^M. D. Scott, Inter-American TVopical Tlma Commission, P.O. Box
271, La Jolla, CA 92038, pers. commun. November 1983.
Percent Pregnant
The fractions of sexually mature females that were
pregnant are given in Thble 1 for the samples of the
northern and southern offshore stocks collected
from 1971 to 1983. Sample sizes decline in the later
years for the northern stock, but are typically MOO.
Table 1. — Fractions a) of females that were sexually mature, b) of sexually mature females that were pregnant, and c) of preg-
nant females that were lactating. Samples include 1971-83 specimens from the northern and southern offshore stocks of spotted
dolphins. Fraction mature was not sampled in 1971 and 1972.
Year
1971
1972
1973
1974
1975
1976
1977
1978
1979
1980
1981
1982
1983
Overall
Northern stock
a) Fraction mature
0.56
0.53
0.54
0.50
0.61
0.59
0.59
0.55
0.61
0.56
0.50
0.561
Number in sample
1,149
1,013
1,215
751
995
564
593
509
465
579
137
7,970
b) Fraction pregnant
0.48
0.41
0.42
0.29
0.29
0.34
0.27
0.24
0.30
0.30
0.29
0.32
0.38
0.329
Number mature
79
449
573
487
493
291
375
229
205
148
153
148
37
3,667
c) Fraction lactating
0.26
0.08
0.08
0.17
0.14
0.13
0.35
0.15
0.30
0.23
0.24
0.19
0.28
0.162
Number pregnant
38
180
236
138
130
93
94
52
61
43
42
47
14
1,168
Southern stock
a) Fraction mature
0.58
—
0.68
0.63
0.61
0.77
0.58
0.73
0.60
0.70
0.69
0.656
Number in sample
24
0
38
254
23
51
166
59
20
199
106
940
b) Fraction pregnant
—
—
0.75
—
0.49
0.48
0.12
0.28
0.22
0.35
0.00
0.32
0.18
0.364
Number mature
0
0
12
0
23
145
8
25
60
17
8
73
22
393
c) Fraction lactating
—
—
0.00
—
0.22
0.04
0.00
0.16
0.08
0.00
—
0.23
0.00
0.087
Number pregnant
0
0
9
0
9
68
1
6
13
6
0
22
4
138
660
BARLOW: REPRODUCTIVE RATES OF SPOTTED DOLPHINS
Samples sizes for the southern stock are highly
variable between years, and several years have too
few specimens to reliably estimate the fraction of
the population that would be pregnant. For 1973-83,
the overall percentage of pregnant females is,
however, significantly higher for the southern stock,
36.4%, than for the northern stock, 31.4% Oc? =
3.97, P = 0.05). Because of this difference, northern
and southern stocks were not pooled in subsequent
analyses. Due to the small sample size from the
southern stock, examination of trends and biases in
female reproductive rates was limited to the north-
ern stock.
Annual estimates of the percentage of pregnant
females are illustrated in Figure 2 for the northern
offshore stock. The regression is significant; however,
the residuals do not appear randomly distributed.
The negative slopes of the regression lines are large-
ly due to high pregnancy rates in 1971-73. Expected
values for the percent pregnant in each year were
generated in two ways: from the overall percent preg-
nant and from the "de-trended" regression predic-
tions. Chi-square tests using these expected values
show the annual variability in percent pregnant is
greater than would be expected from random sam-
pling of a population with a constant (P < 0.001) or
linearly decreasing (P < 0.001) pregnancy rata
Although natural year-to-year variability in
pregnancy rates cannot be ruled out, a changing bias
in sampling could also cause larger than expected
variability in percent pregnant. Td look for such a
bias, the sample from the northern stock was
stratified by the six sampling factors described
abova The percent pregnant in each of these strata
is given in Tkble 2, with the chi-square probabilities
that the samples could have been drawn randomly
from the pooled sample Of the factors examined,
pregnancy rate was significantly related to sampling
season, dolphin kill-per-set, and tuna catch-per-set
(henceforth the latter two are referred to as kill and
catch).
Because sampling seasons, mean dolphin kills, and
mean tuna catches vary significantly between years,
these factors cannot be considered independent of
year. For instance, the interaction between preg-
nancy rates and dolphin kill might appear significant
due to high kill rates or high catch rates in a year
(or years) that coincidentally had high pregnancy
rates. Conversely, high pregnancy rates in one year
may be due to a sampling bias related to dolphin
kill.
Multiway tests were used to identify possible inter-
actions between the three significant factors and
year effects. In all cases, 3-way tests indicate that
year effects are significant (Tkble 3). First order ef-
fects of kill, catch, and season were not significant;
however, higher order effects involving the latter two
were important (Tkble 3). A 4-way test using catch,
season, and year also shows significant higher order
interactions involving both catch and season (Ikble
3).
Higher order interactions involving year and
another factor indicate that effect of that factor
changes with year. Since pregnancy rates appear to
have changed markedly from 1971-73 to 1974-83
(Fig. 2), the effect of the significant factors was
bU
50
-(79)
•
(449)
(573)
•
40
•
(37)
^_
(291)
#
—
•
(205)
(148) (153)
(148)
•
30
(487)
(493)
•
(375)
•
• •
20
-
(229)
10
n
I 1
1 1
1
1
1
1 1
1 1
1
1
<
z
o
UJ
c
Q.
»-
Z
UJ
o
oc
UJ
&
1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983
YEAR
Figure 2.— Percentages of mature females that were pregnant for the northern offshore stock of spotted dolphins
from 1971 to 1983. Solid line represents weighted regression. Sample sizes are in parentheses.
661
FISHERY BULLETIN: VOL. 83, NO. 4
Table 2.— Percentage of sexually mature females tfiat were
pregnant (1971-83) grouped by 1) the area in which the
specimens were collected; 2) the quarter of the calendar
year; 3) the length of time between sighting the school
and release of the net; 4) the observer's estimate of the
total school size; 5) the number of dolphins known to be
killed in the set; and 6) the tons of tuna caught in the
set. Note that total sample size varies with the availabil-
ity of data on the stratifying variable. Probabilities are based
on chi-square contingency tests. Only samples from the
northern offshore stock of spotted dolphins are included.
CYRA = Commission Yellowfin Regulatory Area.
Pregnant
Prob-
(0/0)
N
ability
1) Geographic area
Inside CYRA
33.5
3,032
0.09
Outside CYRA
30,0
633
2) Season
1st quarter
34.7
1,799
2d quarter
33.5
741
0.04
3d quarter
28.9
584
4th quarter
30.4
542
3) Chase time (min)
<20
31.2
1,081
20-40
34.8
1,440
0.09
>40
31.1
747
4) School size
<500
30.2
443
500-1 ,500
29.8
741
0.49
>1,500
27.4
693
5) Number killed
1-10
29.8
1,104
11-30
30.1
917
<0.001
>30
37.4
1,301
6) Tuna caught (tons)
0-5
29.0
428
6-15
33.0
848
0.02
16-30
30.4
760
>30
35.6
1,280
tested separately for these two time periods. When
the years 1971-73 were excluded (Tkble 4), the inter-
actions between percent pregnant and season,
dolphin kill, and tuna catch are no longer significant.
When tests are performed on data from 1971 to 1973
alone (Ikble 4), season and tuna catch are still
significantly related to pregnancy rate
Percent Lactating
Annual trends in percent lactating for the north-
ern stock of spotted dolphins are illustrated in
Figure 3. Two cases are considered: 1) the percen-
tage of all mature females that are lactating and 2)
the percentage of pregnant females that are lac-
tating. For both cases, a weighted regression shows
a significant increase in the fraction of lactating
females through time (P < 0.05). In the former case,
the regression again appears to be driven by
anomalous values in 1971-73. Percentages and sam-
ple sizes for the latter case are presented in Ikble
Table 3. — Multiway tests of factors affecting per-
cent pregnant. Log-likelihood chi-square was
used to calculate the probability that percent
pregnant is independent of the stated factor(s)
using the log-linear model. Pregnancy state
(pregnant/not pregnant) is implicit as the first
factor in each comparison.
Tests
Probability
3-way
a) Year
<0.0001
Season
0.70
Year x season
<0.0001
b) Year
<0.0001
Kill
0.09
Year x kill
0.31
c) Year
<0.00^
Catch
0.14
Year x catch
0.0004
4-way
Year
<0.0001
Season
0.90
Catch
0.15
Year x season
<0.0001
Year x catch
0.0002
Season x catch
0.003
Year x season x catch
0.07
Table 4. — Percentage of sexually mature females that were
pregnant, grouped by season, dolphin kill, and tuna catch.
The years 1971-73 and 1974-83 are grouped separately.
Probabilities are based on chi-square contingency tests.
Only samples from the northern offshore stock of spotted
dolphins are included.
Pregnant
Prob-
Year
(%)
N
ability
1971-73 overall
41.9
1,101
Season
1st quarter
44.0
722
2d quarter
47.6
210
<0.001
3d quarter
—
0
4th quarter
25.4
169
Number killed
1-10
38.0
171
11-30
39.5
248
0.23
>30
44.1
651
Tuna caught (tons)
0-5
37.6
101
6-15
44.5
247
0.04
16-30
35.0
226
>30
45.5
490
1974-82 overall
29.0
2,566
Season
1st quarter
28.4
1,077
2d quarter
27.9
531
0.39
3d quarter
28.9
584
4th quarter
32.7
373
Number killed
1-10
28.3
933
11-30
26.6
669
0.27
>30
30.6
650
Tuna caught (tons)
0-5
26.3
327
6-15
28.3
601
0.76
16-30
28.5
534
>30
29.5
790
662
BARLOW: REPRODUCTIVE RATES OF SPOTTED DOLPHINS
(J
Z
<
I-
O
<
-J
I-
z
Hi
o
• All mature females
o Only pregnant females
(479) (473)
(358)
(203)
<'»44> (558)
80
70
60
50
40
30
20
10
0
1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983
YEAR
Figure 3.— Percentages of mature females that were lactating and percentages of pregnant females that were lac-
tating for the northern offshore stock of spotted dolphins from 1971 to 1983. Solid lines represents weighted regres-
sions. Sample sizes are in parentheses.
(14)
1 for both the northern and southern stocks. Again
sample size for the southern stock is too small to
examine individual years; however, the overall per-
cent of pregnant females that were lactating in
1973-83 samples shows significant differences be-
tween stocks ixl = 6.50, P = 0.01). Annual
variability for the northern stock is greater than
expected from random sampling of a population
with a constant percent lactating (xfg = 63.5, P <
0.001).
When the sample of pregnant females from the
northern stock is stratified by the six sampling fac-
tors, lactation state was significantly related to sam-
pling season, dolphin kill, and tuna catch (Tkble 5).
Again, 3-way tests showed that the first order effect
of these factors was not significant when year was
included as the third factor (Ikble 6). In each of these
cases, the first order effect of year was important.
In one case, dolphin kill, a second order interaction
between kill and year was also significant.
Percent Mature
The fractions of females that were sexually mature
are given in Ikble 1 by stock and by year (1973-83).
Again the sample sizes are sufficient in all years for
the northern stock but are inadequate in some years
for the southern stock. The southern stock is
significantly different from the northern stock in
percent mature (xj = 31.2, P < 0.001), and
(given its small sample size) the southern stock was
excluded in subsequent stratifications.
The percentage of all females that are mature from
1973 to 1983 is illustrated in Figure 4 for the north-
ern stock. In this case, the weighted regression is
not significant. Using chi-square tests, the level of
annual variability in percent mature is larger than
would be expected from randomly sampling a
population with a constant fraction of mature
females (P < 0.001).
For long-lived animals such as dolphins, annual
variability in percent mature should be small and
changes in this population parameter should be
gradual. Since the annual variability observed in the
data is larger than would be expected from random
sampling error, year-to-year changes in sampling
biases are likely. Percent mature was found to be
significantly related to three of the six sampling fac-
tors examined: sampling season, dolphin kill-per-set,
and tuna catch-per-set (Ikble 7).
Each of these three significant factors was tested
with maturity state and year using 3-way tests (Ikble
8). For each of these factors, year was a significant
factor and all other first order effects were not
significant. Only dolphin kill showed a significant sec-
ond order interaction with year.
663
FISHERY BULLETIN: VOL. 83, NO. 4
Table 5. — Percentage of pregnant dolphins that were lac-
tating (1971-83) grouped by 1) the area in which the speci-
mens were collected; 2) the quarter of the calendar year;
3) the length of time between sighting the school and
release of the net; 4) the observer's estimate of the total
school size; 5) the number of dolphins known to be killed
in the set; and 6) the tons of tuna caught in the set.
Note that total sample size varies with the availability of data
on the stratifying variable. Probabilities are based on chi-
square contingency tests. Only samples from the northern
offshore stock of spotted dolphins are included. CYRA =
Commission Yellowfin Regulatory Area.
Lactating
Prob-
(%)
N
ability
1) Geographic area
Inside CYRA
15.7
988
0.30
Outside CYRA
18.8
181
2) Season
1st quarter
11.9
611
2d quarter
17.2
239
<0.001
3d quarter
26.7
161
4th quarter
20.3
158
3) Chase time (min)
<20
14.8
331
20-40
14.0
479
0.27
>40
18.6
226
4) School size
<500
20.0
130
500-1,000
18.0
211
0.87
>1,500
19.7
183
5) Number killed
1-10
19.1
319
11-30
16.5
267
0.03
>30
12.3
471
6) Tuna caught (tons)
0-5
20.5
117
6-15
16.4
275
0.17
16-30
16.7
221
>30
12.8
444
DISCUSSION
Changes in the reproductive status of the female
segment of a population can be monitored using a
variety of reproductive indices: 1) mean age at sexual
maturation, 2) mean length (or weight) at sexual
maturation, 3) annual pregnancy rates, 4) calving
interval, 5) percentage of mature females that are
pregnant, 6) percentage of females that are lactating,
and 7) percentage of females that are sexually
mature Changes in each of these are examined
below.
Changes in Maturation Parameters
Myrick et al. (1984) have found no significant dif-
ference in the age at sexual maturation (ASM)
between a sample from 1973 to 1978 and another
sample from 1981. In the present study, length at
attainment of sexual maturity is estimated to have
increased 4.4 cm from 1974 to 1983. If these results
hold, dolphins must be growing faster in recent
Table 6. — Multiway tests of factors affecting
the percentage of pregnant females that are
lactating. Log-likelihood chi-square was
used to calculate the probability that per-
cent lactating is independent of the stated
factor(s) using the log-linear model. Lacta-
tion state (lactating/not lactating) is implicit
as the first factor in each comparison.
3-way tests
Probability
a) Year
<0.0001
Season
0.29
Year x season
k
0.007
b) Year
<0.0001
Kill
0.79
Year x kill
0.51
Table 7. — Percentage of female dolphins that were sexual-
ly mature (1973-83) grouped by 1) the area in which the
specimens were collected; 2) the quarter of the calendar
year; 3) the length of time between sighting the school
and release of the net; 4) the observer's estimate of the
total school size; 5) the number of dolphins known to be
killed in the set; and 6) the tons of tuna caught in the set.
Note that total sample size varies with the availability of data
on the stratifying variable. Probabilities are based on chi-
square contingency tests. Only samples from the northern
offshore stock of spotted dolphins are included. CYRA =
Commission Yellowfin Regulatory Area.
Mature
(%)
N
Prob-
ability
1) Geographic area
Inside CYRA 55.7 6,329 0.19
Outside CYRA 57.5 1 ,625
2) Season
1st quarter 54.2 3,495
2d quarter 57.2 1 ,738 0.02
3d quarter 58.2 1,580
4th quarter 57.6 1,155
3) Chase time (min)
<20 54.4 2,067
20-40 56.1 3,084 0.36
>40 56.5 1 ,689
4) School size
<500 53.5 1,183
500-1,500 56.8 1,970 0.19
>1,500 56.0 1,753
5) Number killed
1-10 57.9 2,465
11-30 54.9 2,068 0.02
>30 54.0 2,321
6) Tuna caught (tons)
0-5 53.3 920
6-15 55.1 1,779 0.05
16-30 54.5 1,668
>30 57.7 2,482
years. Given small sample sizes of aged individuals,
significant changes in ASM may be difficult to
detect. Previous studies have shown that the age at
sexual maturation is quite responsive to population
changes in marine mammals (Fowler 1984), while
length at maturation tends to show little change For
fin whales, Balaenoptera physalus, Lockyer (1972)
664
BARLOW: REPRODUCTIVE RATES OF SPOTTED DOLPHINS
80 t-
UJ
H
<
2
UJ
o
tu
0.
70 -
60
50
40
30
(995)
(1149)
(1013)
(1215)
(593)
(564) .
(509)
(465)
(579)
(751)
(137)
±
1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983
YEAR
Figure 4.— Percentages of all females that were mature for the northern offshore stock of spotted dolphins from
1971 to 1983. Sample sizes are in parentheses.
Table 8.— Multiway tests of factors affecting
percent mature. Log-likelihood chi-square
was used to calculate the probability that
percent mature is independent of the stated
factor(s) using the log-linear model. I\/latura-
tion state (mature/not mature) is implicit as
the first factor in each comparison.
3-way tests
Probability
a) Year
0.003
Season
0.49
Year x season
0.08
b) Year
0.003
Kill
0.16
Year x kill
0.002
c) Year
0.0009
Catch
0.09
Year x catch
0.42
showed a decrease in ASM without any change in
the length at which maturity is attained. Laws (1956)
predicted an inverse relationship between ASM and
early growth rates for marine mammals. Spotted
dolphins appear to show an increase in length at
maturation with no change in ASM, and thus do not
follow predicted patterns.
Trends in Percent Pregnant
Annual pregnancy rates, calving interval, and per-
cent pregnant all measure essentially the same thing.
Annual pregnancy rate and calving interval require
knowledge of gestation times. Because density com-
pensatory responses have not been shown in ceta-
cean gestation times, it is more straightforward to
deal directly with percent pregnant.
What appeared to be a rapid decline in dolphin
pregnancy rates from 1973 to 1978 (Henderson et
al. fn. 2), now appears as two eras with distinctly
different pregnancy rates. The fraction of pregnant
females in the 1971-73 samples was quite high. The
10 years since 1973 show a lower and relatively con-
stant fraction of pregnant females. This difference
in results is due largely to use of a larger sample
size and a longer time series.
There is no evidence of the sort of slow, long-term
trends in pregnancy rates that might be associated
with changes in population sizes. The reason for the
dramatic change in pregnancy rates between 1973
and 1974 is not known. At least three hypotheses
could be used to explain this change: 1) it was the
result of a naturally high pregnancy rate in 1971-73;
2) it was the result of heavy fishing-related morta-
lity of nursing calves prior to 1974 that resulted in
artificially high pregnancy rates; or 3) it was the
result of a bias in the sampling by tuna vessels.
The first hypothesis suggests that changing en-
vironmental conditions result in annual changes in
pregnancy rates. In the ETP the largest environ-
mental perturbations are associated with "El Nino"
events which occur on the time scale of from 5 to
10 yr (Rasmusson and Carpenter 1982). El Nifio con-
ditions prevailed in 1972 (moderate), 1975-76 (weak),
and 1982-83 (very strong). These dates do not help
explain the change in pregnancy rates that occurred
between 1973 and 1974.
The second hypothesis is that heavy dolphin mor-
tality in the 1960's and early 1970's may have some-
how affected dolphin pregnancy rates. Large reduc-
665
FISHERY BULLETIN: VOL. 83, NO. 4
tions in dolphin mortality occurred following the
passage of the Marine Mammal Protection Act of
1972 (Tkble 9). If mortality rates were higher for
nursing calves, calving interval might have been
shortened. This would result in higher pregnancy
rates and lower lactation rates, both of which were
observed in 1971-73. Analyses have indicated that
very young calves are more susceptible to tuna-net
mortality (Powers and Barlow fn. 3; Stuntz^). In-
directly, high calf mortality may also result from the
separation of a calf from its mother during long
chases. It is not known if the magnitude of these ef-
fects could have resulted in the observed changes in
pregnancy or lactation rates.
The third hypothesis is that sampling methods
were somehow different between 1971-73 and
1974-83. The only difference in the sampling design
was that in 1971-73, scientific technicians were
placed only on tuna vessels that agreed to cooperate
Beginning in 1974, the selection of vessels was ran-
dom. It is difficult, however, to see how this change
would affect the percent pregnant in the samples.
As was noted above, percent pregnant was signifi-
cantly correlated with sampling season, dolphin kill-
per-set, and tuna catch-per-set during the years
1971-73, but not during the years 1974-83. The
reason for this difference is not known, but this
would seem to be evidence that sampling was more
random in the latter period.
The observed change in percent pregnant from
1971-73 to 1974-83 cannot be explained with certain-
ty. The high pregnancy rates in 1971-73 can be
logically explained by direct or indirect effects of the
fishery or by sampling biases in those years (Hypo-
theses 2 and 3). Determining whether either (or both)
hypothesis is true may not be possible with existing
data.
Trends in Percent Lactating
Changes were also found in the percentage of lac-
tating females. For mature females, the fraction lac-
tating shows low values in 1971-73 and high values
in 1974-83, which is opposite the pattern seen for
fraction pregnant. This inverse correlation would be
expected given that pregnancy state and lactation
state are physiologically linked (i.&, cessation of lac-
tation leads to ovulation and pregnancy). Perhaps
more meaningful is the increase in the fraction of
Table 9. — Estimates of numbers of
spotted dolphins killed by all purse
seine vessels in the eastern tropical
Pacific, 1968-78 (data from Smith
1983).
Spotted dolphins
Year
killed
1968
178,000
1969
365,000
1970
355,000
1971
176,000
1972
288,000
1973
131,000
1974
95,000
1975
105,000
1976
47,000
1977
22,000
1978
19,000
*Stuntz, W. E. 1980. Variation in age structure of the inciden-
tal kill of spotted dolphins, Stenella attenuata, in the U.S. tropical
purse-seine fishery. Admin. Rep. LJ-80-06, 29 p.; available from
Southwest Fisheries Center La Jolla Laboratory, National Marine
Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA 92038.
pregnant females that were lactating. Because being
simultaneously pregnant and lactating represent the
greatest energy drain on female dolphins, this quan-
tity is likely to be very sensitive to changes in en-
vironmental conditions. Because nonpregnant
females are excluded, this quantity should also be
insensitive to sample biases that are related solely
to pregnancy state
Given that no trends were seen in the percent
pregnant from 1974 to 1983, we can infer that the
calving interval, or the mean period between births
for a mature female, also did not change during that
time If calving interval were constant, the increase
in the fraction of pregnant females that were lac-
tating indicates that females may be nursing their
calves for a longer period of time, hence a longer lac-
tation period. This increase in the lactation period
may have resulted from a decrease in fishery related
calf mortality during the 1971-83 period. Because
calves may be more susceptible to death or separa-
tion from their mothers during the chase, capture,
and release of a dolphin school, mean lactation
periods may have been abbreviated during the earlier
years (Hypothesis 2 above).
Trends in Percent Mature
No significant trends in the percentage of females
that were sexually mature during 1971-83 are evi-
dent for the northern stock of spotted dolphins. An-
nual variability was far too great to be explained by
random sampling error. This parameter showed a
significant correlation with dolphin kill-per-set.
Therefore, unless sampling conditions remain con-
stant (which they have not), percent mature is not
a useful index for monitoring reproductive capabili-
ty of the spotted dolphin populations.
666
BARLOW: REPRODUCTIVE RATES OF SPOTTED DOLPHINS
Variability in percent mature with sampling con-
ditions may result from several interacting factors.
Preliminary data have indicated that spotted
dolphins in the ETP may segregate on the basis of
reproductive maturity (A. A. Hohn fn. 4 and M. D.
Scott fn. 5). Schools that consist principally of im-
mature dolphins may have a smaller characteristic
school size, may be less likely to have large numbers
of tuna associated with them, and may be more
vulnerable to high kills-per-set due to the inex-
perience of younger dolphins. Also, the consistent
underrepresentation of immature age classes in the
spotted dolphin age distribution (Barlow and Hohn
1984) indicates that a very significant bias may oc-
cur in the sampling of immature animals. These are
largely speculations, and until a well-supported ex-
planation for sampling variability is presented and
until some method of removing this bias is found,
percent mature should not be used as an index of
changes in spotted dolphin reproduction.
Gross Annual Reproductive Rate
Changes in GARR have been used as a measure
of changes in the net rate of growth for a popula-
tion (Smith 1983). This approach has been faulted
on the basis that it does not consider age structure
effects (Polacheck 1982), and more critically on the
basis that such an approach is theoretically unsound
(Goodman^). These criticisms do not, however,
detract from the usefulness of GARR as an index
of gross per capita reproduction for a popula-
tion.
If GARR were robust to sampling conditions, it
could be one of the most useful indices of popula-
tion reproduction. One advantage is that a GARR
index considers percent pregnant and percent
mature simultaneously, and hence compensatory
changes in these two do not affect the index. Sim-
ply stated, GARR is calculated as (the fraction of
females in a population) x (the fraction of females
that are mature) x (the fraction of mature females
that are pregnant)/(gestation time). Unfortunately,
percent mature is a major component in these
calculations, and this parameter has been found to
be dependent on sampling conditions. Until sampling
problems associated with estimating percent mature
are resolved, GARR is not likely to be a useful in-
dex of change in reproductive rates.
Between-Population Comparisons
The northern and southern stocks of spotted
dolphins have been subjected to very different levels
of fishing-related mortality. Smith* has estimated the
northern stock to be at 38-55% of its 1959 level and
the southern stock to be at 93-98% of its historical
level. Density dependent increases in reproductive
rates might be predicted for the northern stock
relative to the southern stock.
The percentage of mature females that were preg-
nant differs significantly between the northern and
southern stocks. Surprisingly, however, the southern
stock was found to have the higher percent pregnant
(36% vs. 33%). Another exploited population of spot-
ted dolphins in the western Pacific was found to have
an annual pregnancy rate of 0.254 (Kasuya 1976),
which (with a gestation time of 11.2 mo) would give
an average percent pregnant of about 24%. Con-
siderable variability in percent pregnant can thus
exist between spotted dolphin populations, none of
which is obviously related to density compensatory
effects. Sampling of the southern population has,
however, been sporadic, and if annual variability in
pregnancy rates is greater for that stock, a few years'
data may not be sufficient to accurately estimate a
long-term mean. Nonetheless, the tendency for a
more exploited stock to have lower reproductive rates
is worrisome, and future life history comparisons
between the northern and southern stocks would
probably be useful.
Evidence for density compensatory changes in
pregnancy rates were also lacking when two spin-
ner dolphin, 5. longirostris, populations were com-
pared (Perrin and Henderson 1984). They found
similarly that the more heavily exploited stock
(eastern spinners) had a lower percent pregnant than
the less heavily exploited stock (whitebelly spinners).
The opposite would be predicted based purely on
density compensatory effects.
The overall percentage of pregnant females that
are lactating is significantly higher for the north-
ern spotted dolphins than for the southern stock.
The biological significance of this result is ques-
tionable given the year-to-year variability in this
parameter. Between-population comparisons of this
percentage are not likely to be meaningful until the
cause of this large annual variability is identified.
As was noted above, the percentage of females that
'Goodman, D. 1984. Uses of the gross annual reproduction rate
calculation in the dolphin assessment. Admin. Rep. LJ-84-22C, 17
p.; available from Southwest Fisheries Center La JoUa Laboratory,
National Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla,
CA 92038.
*Smith, T. D. (editor). 1979. Report of the status of porpoise
stocks workshop (August 27-31, 1979, La Jolla, California). Ad-
min. Rep. LJ-79-41, 120 p.; available from Southwest Fisheries
Center La Jolla Laboratory, National Marine Fisheries Service,
NOAA, P.O. Box 271, La Jolla, CA 92038.
667
are mature also appears to be higher in the southern
stock than in the northern stock. Given the depen-
dence of this parameter on sampling conditions, lit-
tle confidence should be placed on this result. The
direction of the difference (more immatures in the
northern population) is consistent with a higher
population growth rate in the north. Work is in pro-
gress to determine whether this difference could be
due to differences in the age at sexual maturation
(Myrick^).
No data exist yet on the mean age at sexual
maturation for females in the southern stock. As
mentioned in the Methods section, data do exist on
the "length at sexual maturation" for both the north-
ern and southern stocks. For the northern stock, this
length appears to have increased from 176 cm in
1974 to 181 cm in 1983. For the southern stock this
length was estimated as 175 cm from the pooled
1974-83 data. The length at sexual maturation is
greater for the northern stock, which is consistent
with the greater mean asymptotic length of the
northern specimens (Perrin et al. 1979).
CONCLUSION
My intent in writing this paper was to identify in-
dices that may be of value in monitoring the repro-
ductive health of spotted dolphins in the eastern
Pacific. Two of the indices that were examined (the
percentage of mature females that are pregnant and
the percentage of pregnant females that are lac-
tating) are likely to be useful for this purpose Both
are relatively insensitive to sampling biases, and both
measure important aspects of the female reproduc-
tive cycla Problems exist in measuring the fraction
of females that are mature This parameter is also
an important index of net reproduction in a popula-
tion. It is possible that a stable index of percent
mature could be obtained using some stratification
scheme A first approach might be to examine finer
scale geographic differences in percent mature Addi-
tional work is necessary before significance can be
ascribed to between-population differences in per-
cent mature
ACKNOWLEDGMENTS
Much credit is deserved by the many technicians
who gathered the data upon which this report is
based. Their labors were often under very difficult
working conditions. I also wish to thank the data
^A. C. Myrick, NOAA, National Marine Fisheries Service, P.O.
Box 271, La Jolla, CA 92038, pers. commun. December 1984.
FISHERY BULLETIN: VOL. 83, NO. 4
editing and managing group and the graphics
department, SWFC. Ideas presented in this manu-
script were largely generated in discussions with A.
Hohn and W. Perrin. The current draft of this manu-
script benefited greatly from critical reviews by J.
4Bengtson, D. Chapman, D. DeMaster, F. Hester, A.
Hohn, J. Mean, A. Myrick, W. Perrin, S. Reilly and
G. Sakagawa.
LITERATURE CITED
Barlow, J., and A. A. Hohn.
1984. Interpreting spotted dolphin age distributions. U.S.
Dep. Commer., NOAA Ifech. Mema NOAA-NMFS-SWFC-48,
22 p.
Dixon, W. J. (editor).
1981. BMDP statistical software. Univ. Calif. Press,
Berkeley, 725 p.
Fowler, C. W.
1984. Density dependence in cetacean populations. Rep. Int.
Whaling Comm., Spec Issue 6:373-379.
Gambel, R.
1975. Variations in reproduction parameters associated with
whale stock sizes. Rep. Int. Whaling Comm. 25:182-189.
Hester, R.
1984. Possible biases in the estimates of rates of reproduc-
tion in the spotted dolphins, Stenella attenuata. Rep. Int.
Whaling Comm., Spec. Issue 6:337-341.
Kasu\a, T.
1976. Reconsideration of life history parameters of the spot-
ted and striped dolphins based on cemental layers. Sci. Rep.
Whales Res. Inst. 28:73-106.
Laws, R. M.
1956. Growth and sexual maturity in aquatic mammals.
Nature (Lond.) 178:193-194.
Lockyer, C. H.
1972. The age of sexual maturity of the southern fin whale
(Balaenoptera physalus) using annual layer counts in the ear
plug. J. Cons. Int. Explor. Mer 34:276-294.
MiZROCH, S. A.
1983. Reproductive rates in Southern Hemisphere baleen
whales. MS Thesis, Univ. Washington, Seattle, 103 p.
Myrick, A. C, Jr., A. A. Hohn, J. Barlow, and P. A. Sloan.
In press. Reproduction in the female spotted dolphin, Stenella
attenuata. Fish. Bull., U.S.
Perrin, W. F.
1970. Color patterns of the eastern Pacific spotted porpoise
Stenella graffmani Lonnberg (Cetacea, Delphinidae). Zoo-
logica (N.Y.) 54:135-149.
Perrin, W. F, J. M. Coe, and J. R. Zweifel.
1976. Growth and reproduction of the spotted porpoise,
Stenella attenuata, in the offshore eastern tropical Pacific
Fish. Bull., U.S. 74:229-269.
Perrin, W. F., and J. R. Henderson.
1984. Growth and reproductive rates in two populations of
spinner dolphins, Stenella longirostris, with different
histories of exploitations. Rep. Int. Whaling Comm., Spec
Issue 6:417-430.
Perrin, W. F, R. B. Miller, and P. A. Sloan.
1977. Reproductive parameters of the offshore spotted
dolphin, a geographic form of Stenella attenuata, in the
eastern tropical Pacific, 1973-75. Fish. Bull., U.S. 75:629-
633.
668
BARLOW: REPRODUCTIVE RATES OF SPOTTED DOLPHINS
Perrin, W. F., p. a. Sloan, and J. R. Henderson. NOAA-TM-NMFS-SWFC-19, 9 p.
1979. Tkxonomic status of the "southwestern stocks" of spin- Rasmusson, E. M., and T. H. Carpenter.
ner dolphins, Stenella longiroatris, and spotted dolphins, S. 1982. Variations in tropical sea surface temperature and sur-
attenuata. Rep. Int. Whaling Comm. 29:175-184. face wind fields associated with the Southern Oscillation/
POLACHECK, T. El Nino. Mon. Weather Rev. 110:354-384.
1982. The relationship between changes in gross reproductive Smith, T. D.
rate and the current rate of increase for some simple age 1983. Changes in size of three dolphin (Stenella spp.) popula-
structured models. U.S. Dep. Commer., NOAA Ifech. Memo. tions in the eatern tropical Pacific Fish. Bull., U.S. 81:1-13.
669
NOTES
ANNUAL BAND DEPOSITION WITHIN
SHELLS OF THE HARD CLAM,
MERCENARIA MERCENARIA: CONSISTENCY
ACROSS HABITAT NEAR
CAPE LOOKOUT, NORTH CAROLINA
The presence of periodically repeating features in
the preservable hard parts of various organisms
allows scientists in several disciplines to make im-
portant inferences about the rates and timing of past
events (Jones 1980; Rhoads and Lutz 1980). Analysis
of growth lines deposited in shells of bivalve molluscs,
for example, finds powerful application in the fields
of paleontology (Rosenberg and Runcorn 1975), an-
thropology (Clark 1979), population ecology (Ken-
nish 1980), and fisheries biology (Peterson et al.
1983). Possession of a reliable age marker in a bivalve
shell enables fisheries biologists 1) to construct age-
frequency distributions for various populations,
which reflect the age-specific mortality rates and
help permit estimates of sustainable yield, 2) to
calculate individual growth rates and their variability
among habitats, and 3) to understand age-specific
reproductive schedules in exploited populations.
Unfortunately, the potential rewards in applying
this aging technique have encouraged widespread
use of growth line analysis prior to performing the
necessary controls to test the annual periodicity of
line deposition (Clark 1974; Gould 1979; Jones 1981).
Because of the tremendous potential utility of this
aging technique, we carried out mark-recapture tests
of the annual nature of growth band deposition in
shells of the commercially important hard clam,
Mercenaria mercenaria, in a North Carolina sound
(Peterson et al. 1983). Although these experiments
provided convincing evidence that M. mercenaria
deposits a reliable annual marker in the form of an
internal summer growth band in its shell, this study
was carried out in only a single locality in Back
Sound, NC. Patterns of growth band deposition in
bivalve molluscs may vary with environment on
several scales: 1) over a broad geographic scale, M.
mercenaria deposits summer bands in Back Sound,
NC, and in Chesapeake Bay, but winter bands in all
localities in northeastern states (Pannella and
MacClintock 1968; Rhoads and Pannella 1970; Ken-
nish and Olsson 1975; Clark 1979; Clark and Lutz
1982; Fritz and Haven 1983; Peterson et al. 1983);
2) among habitats within estuaries, Protothaca
staminea appears to deposit unambiguous annual
bands in muddy sand but not in a clean-sand habitat
in Mugu Lagoon, CA (Peterson and Ambrose 1985);
and 3) among nearby individuals within a single
habitat, both Chione fluctifraga and Protothaca
staminea from within the same restricted sample at
Mugu Lagoon exhibit radically different patterns of
daily line deposition (Hughes and Clausen 1980).
We present here results of additional tests of the an-
nual nature of internal growth band deposition in
shells of M. mercenaria placed for 2 yr in several
different field localities and estuarine habitats, in
order to test whether our earlier (Peterson et al.
1983) demonstration of annual banding in North
Carolina's M. mercenaria is robust to change in local
habitat.
Materials and Methods
lb extend the generality and power of our previous
results, we designed a mark-recapture experiment
to examine the frequency and clarity of band deposi-
tion in M. mercenaria at 5 additional sites (Fig. 1)
within Carteret County, NC, near Cape Lookout.
These sites were chosen to represent a wide geo-
graphic spread among several local water bodies, to
permit contrasts between vegetated and unvegetated
habitats, and to include more sandy (coarse) sub-
strate than that in our original site One site was
selected on a fine sand flat in the North River about
12 km from our earlier Middle Marsh study site in
Back Sound. Two sites were chosen about 38 km
from Middle Marsh near the western end of Bogue
Sound by the town of Cape Carteret: one on a fine
sand flat and the other in a seagrass bed with mix-
ed stands of Zostera marina and Halodule wrightii.
The other two sites were situated in Core Sound
about 6 km from Cedar Island Point and about 47
km from our initial Middle Marsh study site: one on
a sand flat and the other in a Halodule wrightii
meadow. All sites were on shallow subtidal bottom,
accessible by wading and amenable to recovery of
marked animals.
Tkble 1 summarizes the results of particle-size
analyses done on duphcate surface (0-5 cm) sediment
cores taken in August-September 1981 at each site
to permit comparisons among the five new and one
previous study sites. The five new sites are clearly
characterized by having much coarser sediments
than the previous study site but differ among them-
selves in sediment grade (Tkble 1). Contemporaneous
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
671
Figure 1.— Geographic locations of study sites (marked by dots near circled numbers) within North Carolina near Cape Lookout (marked
by the arrow on the NC map): the previous site at Middle Marsh (1); new sites at North River (2); Bogue Sound sand (3) and seagrass
(4); Core Sound sand (5) and seagrass (6).
672
Table 1. — Locations and sedimentary characteristics of the one
previous (IVIiddie Marsh) and five new study sites of Mercenaria
mercenaria. Sedimentary data came from seiving and pipetting
(Folk 1974) duplicate surface (0-5 cm) sediment cores taken in sum-
mer 1981 at each site. Percent silt-clay is percent of total sediment
dry weight in fine (>40) size classes.
Mean sediment parameters
Location
(±SD)
Graphic
Percent
Sorting
Site
coordinates
mean
silt-clay
coefficient
Middle Marsh
34"'41'28"N
5.07
47.22
3.00
in Back Sound
76°37'03"W
(0.28)
(12.24)
(0.51)
North River
34°48'22"N
2.35
2.97
0.61
76°36'48"W
(0.02)
(1.72)
(0.01)
Bogue Sound
34°41'29"N
2.83
2.15
0.47
Sand
76°59'06"W
(0.09)
(0.05)
(0.02)
Bogue Sound
34°41'36"N
3.05
9.31
0.95
Seagrass
76°59'05"W
(0.02)
(2.22)
(0.17)
Core Sound
34°57'03"N
2.72
8.81
0.91
Sand
76°12'44"W
(0.07)
(2.03)
(0.16)
Core Sound
34°56'59"N
2.40
3.10
0.60
Seagrass
76°12'43"W
(0.00)
(1.33)
(0.06
water temperature and salinity data are not available
for all sites, but records from a variety of sources
(Brett 1963; Thayer 1971; Williams et al. 1973;
Sutherland and Karlson 1977; H. J. Porter, Univer-
sity of North Carolina, Chapel Hill, unpubl. data; W.
Kirby-Smith, Duke University, unpubl. data) suggest
that 1) water temperature patterns probably do not
differ greatly across sites, with monthly averages
ranging from winter minima of 2°-4°C to summer
maxima of 29°-30°C, and 2) that salinities are slightly
more variable across sites. Localities close to Atlantic
Ocean inlets (Bogue Sound sand and seagrass sites
and the previous Back Sound site at Middle Marsh)
experience uniformly high salinities (30-36°/oo), ex-
cept after severe rainstorms (Brett 1963; H. J.
Porter, unpubl. data). Salinities in the upper portion
of North River are only slightly lower because there
is little freshwater inflow into that system (Thayer
1971). The lowest (22-28o/oo) and probably most
variable salinities on a week-to-week scale occur at
the two Core Sound sites, where exchange with the
ocean is reduced and where any persistent north
winds bring intrusions of low-salinity waters from
Pamlico Sound (Williams et al. 1973).
At each of the five new study sites, we placed
groups of 80 Mercenaria mercenaria in 1 m^ field
plots in late summer 1980, excavated them by hand
in late summer 1981 to estimate growth and mor-
tality and to replace missing and dead clams, and
then finally recovered all living clams present in late
summer 1982 (Ikble 2). All M. mercenaria used in
these experiments were individually marked on the
external shell surface with color-coded dots of Mark-
Ibx Corporation paints and measured initially and
at both yearly samplings by calipers to the nearest
0.1 mm in each of three mutually perpendicular
dimensions (length, height, thickness). Clams used
in these mark-recovery experiments were chosen to
reflect a size range from 1 to 10 cm in length. Before
placing the marked and measured clams into the
field plots, we first installed fences of 6 mm mesh
plastic (VEXARi) around the 1 m^ plots. These
fences were identical to those used and described
previously (Peterson et al. 1983) and were designed
to inhibit emigration and to mark off bottom plots
to improve our ability to recover the marked clams.
At the three unvegetated sites, we removed all ini-
tially present M. mercenaria and other large macro-
fauna before adding marked clams by first using
fingers to plow systematically the top 10 cm of
sediments and then twice systematically sieving in
situ through 6 mm mesh the entire 1 m^ surface to
that same 10 cm depth. This procedure was not used
at the initiation of the experiment at the two sea-
grass sites because it would have removed the sea-
grass itself. This same procedure was employed,
although using a 3.2 mm mesh, at both yearly sam-
plings to recover all marked clams from all 1 m^
plots at each unvegetated site. At the two seagrass
sites, marked clams were recovered by using a
hydraulic suction dredge and collecting the contents
of the top 15 cm on a 3 mm nylon mesh bag (see
Peterson et al. 1983 for data on sampling efficienqr
of this device). Because of the removal of seagrasses,
the locations of all seagrass plots were then shifted
slightly (<3 m) to new, undisturbed positions for the
second and final year.
'Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Table 2. — Dates of experiment initiation and subsequent sampling
of Mercenaria mercenaria for each of the five study sites.
Measuring dates
1980
1981
1982
Sitei
initiation
sampling
termination
North River
6 August
30 July
2 August
Bogue Sound
Sand
15 August
2 September
24 August
Bogue Sound
Seagrass
15 August
24 August
24 August
Core Sound
Sand
3 September
9 September
3 September
Core Sound
Seagrass
3 September
11 September
3 September
'Each site held 1 m ~2 enclosures of Mercenaria mercenaria at 80 m ~^: one
enclosure contained clams derived from a common Back Sound site (sup-
plemented by 10-20 mm clams from other Back Sound origins), and at least
one other enclosure contained only locally derived clams.
673
At each site, all M. mercenaria in these ex-
periments >20 mm in initial length came from one
of two different sources. One enclosure at each site
held clams planted at the constant density ^f 80
m"^ and collected initially from a single source, a
seagrass bed along the southern shore of Back
Sound (described in Peterson et al. 1984). One or two
additional enclosures held clams collected locally at
the specific study site, but again kept at the same
80 m"^ density. Low availability of clams in the
10-20 mm size class from the Back Sound source
forced us to add hatchery-reared clams (spawned
from Back Sound individuals) and wild-caught clams
from Middle Marsh also in Back Sound to represent
the 10-20 mm sizes in the "common source" enclosure
at each sita This smallest size class was available
locally at each site to complete the "local-origin"
enclosures. This design was chosen to enable us to
test whether there were any effects of clam origin
(the single Back Sound source vs. local clams) at each
of the five study sites.
Upon termination of the experiment almost exact-
ly 2 yr after initial planting of the marked clams
(Tkble 2), subsets of those clams that had survived
the complete 2-yr period were selected from each
origin treatment at each study site in as wide a range
of sizes as possible These clams were returned to
the laboratory and killed by steaming. One valve
from each of these 2-yr survivors was then section-
ed, using a diamond blade on a slow-speed Buehler
ISOMET saw, from umbo to ventral margin along
the axis of greatest growth. The shell sections were
sanded and polished when necessary to enhance the
clarity of natural banding patterns. Because the ini-
tial size in August- September 1980 and the inter-
mediate size 1 yr later were known for each of the
marked individuals and could be marked on the shell
surface, and because the marking and measuring
process itself almost invaribly induces deposition of
a disturbance check which serves as a very precise
internal shell marker (Peterson et al. 1983), we were
then able to count with the unaided eye the number
of additional growth bands deposited in the internal
shell matrix of each clam during its final 2 yr of life
We also observed where these bands were deposited
relative to the known sizes at the initial, interme-
diate, and final measuring dates. These observations
permit a test of whether the reliability of using sum-
mer growth bands to age North Carolina's M.
mercenaria varies with site (habitat) or clam origin
in the vicinity of Cape Lookout.
Results
We sectioned shells from a total of 89 M.
mercenaria collected alive in August-September
1982 and known by their paint codes to have been
present in the field since the experiment's initiation
24 mo before (Table 2). Of these 89 individuals, 17
either exhibited insufficient growth to permit an ac-
curate determination of the precise shell size at the
experiment's initiation or else lacked a disturbance
check to mark the precise size at initiation. Of the
remaining 72 individuals, all but 2 deposited exact-
ly 2 additional dark growth bands in the final 24 mo
of life (Tkble 3). This pattern was consistent across
all five study sites and did not change as a function
of clam origin (Ikble 3). The appearance of the dark
Table 3.— For each of five new study sites: 1) numbers of hard clams cut for growth analysis from each origin
treatment, 2) numbers of those with insufficient growth to assess band deposition accurately, 3) range of ini-
tial clam lengths for those clams with sufficient growth, and 4) average number of bands deposited in the
2-yr experimental period.
Clam origin
Back Sound
Local site
No.
Study site
cut
North River
10
Bogue
Sound
Sand
10
Bogue
Sound
Seagrass
3
Core Sound
Sand
10
Core Sound
Seagrass
10
Range in Av. no. of
No. with initial annual bands No. with
insufficient length added in 2 yr No. insufficient
growth (mm) (±1 SE) cut growth
Range in Av. no. of
initial annual bands
length added in 2 yr
(mm) (±1 SE)
1
19-74
2(±0)
17
1
43-80
1.£
M±o.
1
14-57
2(±0)
11
2
21-72
2
(±0)
1
39-69
2(±0)
3
1
44-48
2
(±0)
0
18-75
2(±0)
5
3
63-70
2
(±0)
1
15-72
2(±0)
10
6
46-56
2
(±0)
674
band in cross-section was identical to that previous-
ly described and illustrated by photograph (Peter-
son et al. 1983) of clams harvested from the Middle
Marsh locality.
The pattern of band deposition relative to times
of initial planting, first measurement (12 mo), and
collection (24 mo) was also extremely consistent
across all data sets. Initial planting in 1980 occurred
during the period of annual band deposition for 70
of the 72 clams. (In one clam, the 1980 annual band
was just completed and in another the 1980 annual
band was just about to begin at the time of initial
planting.) The disturbance check caused by the
12-mo measurement fell near the end of the growth
band for 70 clams and just after the band for the
two others. The time of collection in 1982 fell dur-
ing or just immediately after the deposition of the
1982 annual band for all clams except those from
local origin at North River. Of the 16 cut clams in
that data set with sufficient growth for band resolu-
tion, 12 were just beginning to deposit their 1982
band at the time of collection (2 August, 3-4 wk
earlier than the other sites— Ikble 2). Two of the 16
lacked the terminal band, whereas the remaining
two had already deposited a substantial amount of
the 1982 band. This North River local data set was
the only one that contained any clams (only three)
which had bands sufficiently faint to cause any doubt
about recording them.
By counting all presumptive annual bands over the
complete growth record of each clam, we also
estimated the age of each of the 89 M. mercenaria
used in this experiment. The estimated age at the
experiment's initiation for the 17 clams excluded
from our 2-yr tests ranged from 6 to 29 yr and
averaged 15.5 yr (±1.7 SE). For the 72 clams that
grew sufficiently and included a sufficient shell
marker at initiation to be used in our 2-yr tests, age
at experimental initiation ranged from 0 to 17 yr and
averaged 3.9 yr (±0.3 SE). Thus, the average age of
the clams that could not be used for our tests was
significantly (P < 0.01 in a t-test) higher than that
of the 72 clams that were used. Most (16 of 17) of
the excluded clams lacked both sufficient growth and
an obvious disturbance check at initiation. Only one
clam was excluded with sufficient growth but with-
out an adequate disturbance check. Although 16
clams lacked sufficient growth to determine ac-
curately the shell size at the initiation of the experi-
ment and were therefore excluded from our tests,
all of these clams possessed discrete bands in their
shells that could be counted separately. They were,
however, close together at the terminal margin of
the shell where separating them was not always
possible and caused some uncertainty in their age
estimates.
Discussion
Our banding data from recovery of marked and
measured M. jnercenaria after virtually 24 mo of
terminal growth provide a compelling case for the
reliability across different habitats of using major
growth bands in sectioned shells to age hard clams
in the Cape Lookout region of North Carolina. Our
previous test of the annual periodicity of banding
in North Carolina's M. mercenaria (Peterson et al.
1983) was carried out in only single locality, a Back
Sound seagrass bed, characterized by almost equal
proportions by weight of sands and muds in its sur-
face sediments (Tkble 1). Through this study, we ex-
tend our tests of the reliability of annual band deposi-
tion in M. mercenaria to several additional sites,
located in different bodies of water and characterized
by much sandier sediments (Ikble 1). Of the six sites
that we used for these tests, three were vegetated
by seagrasses and three lacked macrophytic cover
(Tkble 1). (Although our initial experiment in Mid-
dle Marsh was situated inside a seagrass bed, sea-
grasses were removed from the experimental plots
during each sampling.) Despite these differences in
local geographic location (and probably salinity),
sediment grade, and seagrass presence, banding pat-
terns were consistent and bands were deposited
annually.
By using relatively high densities of 80 m"^ (over
10 times the average natural density found in a
Bogue Sound seagrass bed by Peterson 1982, in
North River, Bogue, Back, and Core Sounds by Beal
1983, and in Back Sound seagrass beds and sand
flats by Peterson et al. 1984), we ran the risk of
causing inhibition of growth. In fact, we were unable
to analyze growth band deposition in 17 of our 89
clams largely because of insufficient growth in the
terminal 2-yr increment. This problem may have
been induced by our choice of relatively high densi-
ty in these experiments, but it does have a natural
analog. In areas with relatively slow growth and in
older age classes where growth rate slows, aging
North Carolina's M. mercenaria by counting annual
bands in shell cross-section may be more difficult and
lead to greater error than the consistency of band-
ing results on our other 72 clams implies (Tkble 3).
Nevertheless, banding even in these generally older
clams that were excluded from our analyses was
discrete and sufficient to permit us to estimate their
ages. Aging does not appear to imply cessation of
annual band deposition but only an increased dif-
675
ficulty in distinguishing one band from another.
Observations on the timing of annual band deposi-
tion in this study agree well with our previouswesults
(Peterson et al. 1983). The 6 August-3 September
period in 1980 consistently fell within the season of
annual band deposition and near the end of the band
at all five new study sites. P\irthermore, the annual
band was still being formed or had just been com-
pleted in all clams collected 24 August-3 September
1982. The banding of M. mercenaria in North
Carolina appears to be a summertime event in con-
trast to the winter banding in northeastern popula-
tions (Barker 1964; Pannella and MacClintock 1968;
Rhoads and Pannella 1970; Clark and Lutz 1982).
The only clams that failed to deposit two additional
annual bands in the 24 mo of this study were taken
from the North River locals. This is also the only
group that deviated in the timing of final band
deposition relative to the 1982 collection date Most
of these clams had just initiated their 1982 bands
at the time of collection in contrast to those from
all other sites where 1982 band depositon was either
far advanced or even terminated. This difference be-
tween sites is probably a consequence of the 3-4 wk
earlier date of collection at North River (Tkble 2).
Despite an identical, early collection date, the Back
Sound clams transplanted to North River exhibited
a pattern of band deposition in 1982 that more close-
ly resembled the other four sites than did the North
River local clams. This difference provides our only
suggestion of an effect of clam origin, but we have
no explanation for the possible effect and do not con-
sider it a serious cause to doubt the consistency of
annual band deposition in North Carolina's M.
mercenaria.
The tests of consistency of annual band deposition
across habitats in a local estuarine system provide
an additional source of confidence in the accuracy
of using internal banding patterns to age M.
mercenaria in the Cape Lookout region of North
Carolina. Concern over the lack of such controlled
tests had earlier prompted Clark (1974), Gould
(1979), and Jones (1981) to question the widespread
assumption of regular periodicity in repeating shell
features. Our demonstration of consistency in annual
banding across local habitats should remove any
doubts about the general applicability of using an-
nual bands to age M. mercenaria in the Cape Look-
out region of North Carolina. The variation in line
deposition patterns which has been shown across
habitats for Protothaca staminea (Peterson and Am-
brose 1985) and among individuals within habitat for
P. staminea and Chione fluctifraga (Hughes and
Clausen 1980) does not exist for M mercenaria near
Cape Lookout. Our results will not only enable inver-
tebrate fisheries biologists to use growth bands with
confidence to age North Carolina's M. mercenaria
but also should stimulate further research on under-
standing the environmental causes of variation in
bivalve shell deposition patterns.
Acknowledgments
K. Bowers, M. E. Colby S. R. Fegley C. Furman,
C. Groat, S. A. Hughes, K. C. Pierce, G. W. Safrit,
Jr., S. Smith, N. T Sterman, and J. Tbcker provided
field and laboratory assistance V. Page drafted and
H. Page photographed Figure 1, adapted from Beal
(1983). Reviews by S. R. Fegley W. Sutherland, and
M. C. Watzin improved the paper. This study was
sponsored by the Office of Sea Grant, NOAA, U.S.
Department of Commerce, under grant No.
NA81AA-D-00026, North Carolina Department of
Administration.
Literature Cited
Barker, R. M.
1964. Microtextural variation in pelecypod shells. Malaco-
logia 2:69-86.
Beal, B. F.
1983. Effects of environment, intraspecific density, predation
by snapping shrimp and other consumers on the population
biology of Mercenaria mercenaria near Beaufort, North
Carolina. M.S. Thesis, Univ. North Carolina, Chapel Hill, 180
P-
Brett, C. E.
1963. Relationships between marine invertebrate infauna
distribution and sediment type distribution in Bogue Sound,
North Carolina. Ph.D. Thesis, Univ. North Carolina, Chapel
Hill, 212 p.
Clark, G. R., H.
1974. Growth lines in invertebrate skeletons. Ann. Rev.
Earth Planet. Sci. 2:77-99.
1979. Seasonal grow^th variations in the shells of recent and
prehistoric specimens of Mercenaria mercenaria from St.
Catherine's Island, Georgia. Am. Mus. Nat. Hist. Anthropol.
Pap. 56:161-179.
Clark, G. R., II, and R. A. Lutz.
1982. Seasonal patterns in shell microstructure oi Mercenaria
mercenaria along the U.S. Atlantic coast. Geol. Soc Am.
Abstr with Programs 14:464.
Folk, R. L.
1974. Petrology of sedimentary rocks. Hemphill Publ. Co.,
Austin, TX, 182 p.
Fritz, L. W., and D. S. Haven.
1983. Hard clam, Mercenaria mercenaria: Shell growth pat-
terns in Chesapeake Bay Fish. Bull., U.S. 81:697-708.
Gould, S. J.
1979. Time's vastness. Nat. Hist. 88(4):18-27.
Hughes, W. W., and C. D. Clausen.
1980. Variability in the formation and detection of growth
increments in bivalve shells. Paleobiology 6:503-511.
Jones, D. S.
1980. Annual cycle of shell growth increment formation in two
676
continental shelf bivalves and its paleoecologic significance
Paleobiology 6:331-340.
1981. Repeating layers in the moUuscan shell are not always
periodic J. Paleontol. 55:1076-1082.
Kennish, M. J.
1980. Shell microgrowth analysis. Mercenaria mercenaria as
a type example for research in population dynamics. In D.
C. Rhoads and R. A. Lutz (editors), Skeletal growth of aquatic
organisms: Biological records of environmental change, p.
255-294. Plenum Press, N.Y.
Kennish, M. J., and R. K. Olsson.
1975. Effects of thermal discharges on the microstructural
growth of Mercenaria merce7iaria. Environ. Geol. 1:41-64.
Pannella, G., and C. MacClintock.
1968. Biological and environmental rhythms reflected in
molluscan shell growth. Paleontol. Soc. Mem. 2:64-80. [J.
Paleontol. 42 (Suppl. to No. 5)].
Peterson, C. H.
1982. Clam predation by whelks (Biisycon spp.): experimen-
tal tests of the importance of prey size, prey density, and sea-
grass cover. Mar. Biol. (Berl.) 66:159-170.
Peterson, C. H., and W. G. Ambrose, Jr.
1985. Potential habitat dependence in deposition rate of
presumptive annual lines in shells of the bivalve Protothaca
staminea. Lethaia 18:257-260.
Peterson, C. H.. P. B. Duncan, H. C. Summerson, and G. W.
Safrit, Jr.
1983. A mark-recapture test of annual periodicity of internal
growth band deposition in shells of hard clams, Mercenaria
mercenaria, from a population along the southeastern United
States. Fish. Bull., U.S. 81:765-779.
Peterson, C. H., H. C. Summerson, and P. B. Duncan.
1984. The influence of seagrass cover on population structure
and individual growth rate of a suspension-feeding bivalve,
Mercenaria mercenaria. J. Mar. Res. 42:123-138.
Rhoads, D. C., and R. A. Lutz (editors).
1980. Skeletal growth of aquatic organisms: Biological records
of environmental change Plenum Press, N.Y., 750 p.
Rhoads, D. C., and G. Pannella.
1970. The use of molluscan shell growth patterns in ecology
and paleoecology. Lethaia 3:143-161.
Rosenberg, G. D., and S. K. Runcorn (editors).
1975. Growth rhythms and the history of the earth's rotation.
John Wiley and Sons, Lond., 559 p.
Sutherland, J. P., and R. H. Karlson.
1977. Development and stability of the fouling community at
Beaufort, North Carolina. Ecol. Monogr. 47:425-446.
Thayer, G. W.
1971. Phytoplankton production and the distribution of
nutrients in a shallow unstratified estuarine system near
Beaufort, N.C. Ches. Sci. 12:240-253.
Williams, A. B., G. S. Posner, W. J. Woods, and E. E. Deubler,
Jr.
1973. A hydrographic atlas of large North Carolina sounds.
Univ. North Carolina Sea Grant Publ. UNC-SG-73-02, 130
p. (U.S. Fish Wildl. Serv., Data Rep. 20, 130 p.)
Charles H. Peterson
P. Bruce Duncan
Henry C. Summerson
Brian F. Real
Institute of Marine Sciences
University of North Carolina at Chapel Hill
Morehead City, NC 28557
STANDING STOCK OF JUVENILE
BROWN SHRIMP, PENAEUS AZTECUS,
IN TEXAS COASTAL PONDS
The increased demand for timely information con-
cerning management of shrimp stocks has renewed
interest in developing reliable methods of predicting
brown shrimp, Penaeus aztecus, crop size for the off-
shore Gulf of Mexico fishery. Advance information
regarding shrimp abundance would also enable
elements of the shrimp industry to prepare for a
potentially good or poor harvest. Studies exploring
the feasibility of predicting the annual abundance
of brown shrimp off the Tfexas coast, initiated in 1960
(Baxter 1963), are based on the premise that post-
larval and juvenile shrimp abundances are propor-
tionally related to the subsequent commercial
harvest (Berry and Baxter 1969).
A "good" predictor is one that is precise, timely,
and cost effective The abundance of postlarval
shrimp as they move from the Gulf of Mexico into
coastal bays is determined from semiweekly collec-
tions made by the National Marine Fisheries Ser-
vice, Galveston, at the entrance to Galveston Bay be-
tween late February and early May (Baxter 1963).
The postlarval shrimp index gives the earliest but
least reliable indication of potential harvest. A more
accurate but less timely prediction is derived from
landings of the bait shrimp fishery. Statistics for bait
shrimp landings since 1960 provide the basis for a
predictive model developed by K. N. Baxter (Klima
et al. 1982) defining the relationship between the bait
abundance index and subsequent offshore catch.
However, this prediction is not available until mid-
June, just prior to the seasonal opening, because
recruitment of brown shrimp into the bait fishery
does not begin until May (Chin 1960). A third possi-
ble indicator is the standing stock size of juvenile
shrimp in estuarine nursery areas measured before
shrimp emigrate and become vulnerable to the bait
fishery. This would provide an estimate earlier in the
season than the bait index and may be a more ac-
curate predictor than the postlarval abundance
Predictive capability increases with each successive
life stage because of the decreased time span be-
tween the estimate and subsequent commercial
harvest.
Tb examine the relationship between juvenile
brown shrimp standing stock and offshore harvest,
and to determine the suitability of juvenile brown
shrimp abundance as a predictor, we conducted a
mark-recapture study in Galveston Bay, TX, during
the first week of June 1983. In this report we sum-
marize the results of our study, compare estimates
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
677
obtained by mark recapture and an alternative drop
sampler method, and discuss previously unreported
results of 1970-71 studies (Welker and Baxter^).
Methods
Sydnor Bayou is a shallow coastal tidal pond in
Galveston Bay (Fig. 1). The site was chosen because
the single narrow entrance could be blocked easily
with netting, thus preventing immigration and
emigration of shrimp during the experiment, and
because Sydnor Bayou was the site of a similar study
in 1970.
The pond covers 32.4 to 36.4 ha, depending on the
tide, is about 0.9 km long and 0.2 km at its widest
point, narrowing to 6 m at the mouth. Maximum
depth is about 1.5 m at high tide, with a 0.25 m tidal
difference Average salinity during the marking was
20.5 ppt and mean surface temperature was 28°C.
Weekly sampling of Sydnor Bayou with a 3 m otter
trawl (25 mm stretched mesh) began 25 April 1983
to monitor the size of the juvenile shrimp. By 23 May
1983, most shrimp caught in the trawl were larger
than the 40 mm TL (total length) minimum needed
for tagging, and we decided to begin the mark-
recapture experiment the next week.
Sydnor Bayou was blocked at dawn on 31 May 1983
across bridge B-1 (Fig. 1) with a 45.7 m net having
a 6 mm mesh. The net was anchored to the bottom
and remained in place for the duration of the
experiment.
A 1.8 m diameter, 0.8 m deep round tank with con-
tinuous water flow and two 147 L aerated ice chests
were set up on shore to hold shrimp during the mark-
ing process. Shrimp were caught in 49 5-min trawl
hauls and transported to the marking site in aerated
45 L ice chests. lb minimize marking mortality, only
shrimp 40 mm TL and larger were marked and held
in the large tank. Marking was accomplished by in-
jection with pink fluorescent pigment as described
by Klima (1965). Representative length -frequency,
species-composition, and sex ratio information was
obtained from shrimp captured in one trawl haul.
Marked shrimp were released within the hour
after the target number (4,100) had been marked.
Shrimp were scattered along the shallow grassy
shoreline from moving skiffs. No dead or moribund
shrimp were released, and release operations ceased
whenever shore birds were attracted.
Four 61 cm x 61 cm x 20 cm wire cages, each
SYDNOR BAYOU
36.4 HA
CORPUS
CHRIS
COW TRAP 1 AND 2
27.5 AND 2.8 HA
MUD LAKE
6.4 HA
Figure 1.— Tfexas ponds selected for brown shrimp mark-recapture
studies: Sydnor Bayou (1970 and 1983); Cowtrap, Mushroom, Caran-
cahua, and Mud Lake (1971).
containing 25 marked and 25 unmarked shrimp,
were set out in the pond and remained submerged
through all tidal stages. After 24 h, cages were raised
and all shrimp, dead and alive, were counted,
measured, and recorded for an estimate of marking
mortality.
Recapture trawling began 18 h later, allowing
marked shrimp time to distribute themselves in the
unmarked population. For three consecutive days,
all trawlable bottom was sampled by 5-min trawl
hauls. Shrimp were returned to the laboratory where
marked shrimp were identified under ultraviolet
light. All marked and up to 100 unmarked recoveries
were measured per tow. Length-frequency distribu-
tions for releases, marked recoveries, and unmark-
ed recoveries are shown in Figure 2.
We estimated an initial population of juvenile
brown shrimp using Bailey's (1951) modification of
the Petersen formula
^Welker, W., and K. N. Baxter. Juvenile brown shrimp popula-
tion estimates in Itexas tidal marsh ponds. Unpubl. manuscr., 8 p.
Southeast Fisheries Center Galveston Laboratory, National Marine
Fisheries Service, NOAA, 4700 Avenue U, Galveston, TX 77550.
678
N = M
(C + 1)
R + 1
N=122
where M = number of marked shrimp released,
corrected for marking mortahty,
C = number of shrimp examined for marks,
R = number of recaptured marked shrimp
in the sample
The 95% confidence limits for the true population
were estimated using the standard error of the large
sample variance formula (Bailey 1951)
V(N) =
M^jC + 1){C - R)
(R + 1)2 (R + 2)
Application of this method is justified under the
following conditions (Ricker 1975):
1) Marked shrimp suffer the same natural mor-
tality as unmarked.
2) Marked and unmarked shrimp are equally
vulnerable to fishing.
3) Marked shrimp do not lose their mark.
4) Marked shrim.p become randomly distributed
among unmarked.
5) All marks are recognized and reported on
recovery.
6) There is not emigration or immigration occur-
ring in the catchable population.
Results and Discussion
Overall marking mortality was 9%. One cage had
unusually high mortality. Nineteen of 25 marked
shrimp were alive at the end of 24 h, and the only
evidence of the other 6 marked shrimp was pieces
of exoskeleton. They apparently molted and were
cannibalized. Holt (1982) suggested that the condi-
tion of shrimp prior to tagging dictates the survival
of the tagged animals. When stressed animals were
tagged, mortality more than doubled. Howe and
Hoyt (1982) hypothesized that tags and marks may
indirectly cause mortality by attracting predators.
Farmer and Al-Attar (1979) found shrimp marked
with subcutaneous pigment suffered high mortality
(compared with controls) only when held with un-
marked conspecifics. Clark and Caillouet (1973),
however, found negligible marking mortality in a
mark-recapture experiment with white shrimp, R
setiferus, when 50 marked and 50 unmarked con-
trol shrimp were held in a large pen in a pond rather
than in several small cages. Costello and Allen (1962)
stated that stained shrimp may be expected to sur-
1
20
40 60 80 100
TOTAL LENGTH (MM)
120
Figure 2.— Length-frequency distribution of brown shrimp in Syd-
nor Bayou, June 1983: A) representative sample of shrimp col-
lected during marking; B) unmarked shrimp caught during recap-
ture operations; and C) marked shrimp caught during recapture
operations.
vive at essentially the same rate as unmarked
shrimp, regardless of presence of predators, lb avoid
overestimating marking mortality, we did not include
the counts in the high cage in the calculation. The
resulting 4% (3 dead marked shrimp out of 75) was
similar to the marking mortalities of past studies in
Sydnor Bayou, Mud Lake, and Mushroom (Welker
and Baxter fn. 1).
1983 Population Estimate
A total of 223 marked shrimp were among 12,304
shrimp caught in 94 recapture tows. Tides during
the recovery period were low in the morning, ap-
proaching high tide in the afternoon. Areas along
the shore and the south end of the bayou were
shallow for trawling in the mornings, but could be
adequately sampled in the afternoon. Distribution
679
of marked shrimp was random (one-sample runs test,
P = 0.960; Siegel 1956). ^
The population estimate of 207,786 shrimp deter-
mined from mark-recapture data compared favorably
with the results of a concurrent drop sampler ex-
periment (Ikble 1). Shrimp densities were obtained
using a 2.8 m^ drop sampler at high tida Detailed
methodology has been described by Zimmerman et
al. (1984). Drop samples were taken in two sets, four
pairs each, in vegetated and nonvegetated areas,
divided between the south and north ends of the
bayou. Vegetated habitat was sampled along the
bayou margins, while nonvegetated area sampling
was in open waters of the bayou. Numbers of shrimp
within the sampler were extrapolated to represent
the shrimp population in the vegetated, nonvege-
tated, and total areas of Sydnor Bayou. Confidence
intervals for the drop sampler were much wider than
those for Petersen estimate because drop sampler
estimates were based on a small number of samples.
The drop sampler estimate for 36 ha was higher by
about 92,000 shrimp. One reason for this difference
is that the mark-recapture estimate reflects only that
part of the population >40 mm TL, while the drop
sampler measures density of small (<40 mm) shrimp
more effectively, and these small shrimp are included
in the estimate (Ikble 2). We calculated the drop sam-
pler population estimate using only shrimp larger
than 40 mm TL (Tkble 1). A chi-square test shows
a significant difference between the drop sampler
and mark- re capture size-frequency samples, cate-
gories 41-50 mm and higher (x^ = 109.45, df = 6,
P very small). The high chi-square value is due main-
ly to the greater number of 41-50 mm shrimp and
the lower number of larger shrimp (81-90 mm), which
may avoid the sampler, in the drop sampla Length-
frequency composition of the drop sampler catch in-
dicates that 23% of the 103 shrimp taken were
smaller than 40 mm TL, while no shrimp smaller
than 40 mm were captured by the otter trawl.
1970-71 Population Estimates
Our methodology for conducting a Petersen single
census mark-recapture experiment with juvenile
brown shrimp was developed during June and July
1971 studies of five Tbxas coastal ponds (Fig. 1). All
ponds ranged from 0.3 to 0.9 m in depth during a
normal summer tidal (ycle Cow Trap 1 and 2 had
considerable emergent vegetation along their shore-
lines and were part of a large marsh complex. Ex-
tensive flooding of the marsh surrounding these
ponds at flood tide greatly increased the area ac-
cessible to shrimp, but this shallow, vegetated area
Table 1. — Sydnor Bayou brown shrimp population
estimates determined by mark-recapture and drop sampler
methods, June 1983.
Estimated
Method
population
95% C.I.
Mark-recapture^
32.4-36.4 ha
207,786
180,884-234,688
Drop sampler
32.4 nonvegetated ha
185,000
41 ,900-479,000
4.0 vegetated ha
115,000
49,000-248,000
36.4 total ha
300,000
90,800-727,000
Drop sampler'
32.4 nonvegetated ha
157,000
113,000-423,000
4.0 vegetated ha
88,000
53,500-183,000
36.4 total ha
245,000
166,000-606,000
'Estimate of shrimp population >40 mm TL.
Table 2. — Length-frequency composition
of Sydnor Bayou brown shrimp samples
taken with the otter trawl (N = 8,197) and
drop sampler (W = 83), 1-3 June 1983.
Length
Otter trawl
Drop sampler
(mm)
(0/0)
(0/0)
<20
0.0
9.7
21-30
0.0
1.9
31-40
0.0
11.7
41-50
3.8
19.4
51-60
17.3
19.4
61-70
32.2
22.3
71-80
25.7
12.6
81-90
16.0
1.9
91-100
4.2
0.0
>100
0.6
0.8
could not be sampled. Shrimp could move from pond
to pond via flooded marsh and ditches, rendering
block nets ineffective Evidence of this movement
was the netting of marked shrimp released in Cow
Trap 1 and recaptured in Cow Trap 2. These
problems precluded reasonable population estimates
for the Cow Trap ponds, and large marsh complexes
were avoided for future studies of this typa
Mud Lake, Carancahua, and Mushroom had
generally well-defined shorelines, even during flood
tide, and were not contiguous with other ponds or
ditches. Mark-recapture methods were essentially
the same as described for the 1983 study. Marking
and holding operations were conducted on a portable
barge rather than from shore (Emiliani and Marullo
1973). Population estimates determined by Bailey's
(1951) formula ranged from 7,490 to 17,119 brown
shrimp per hectare (Ikble 3). The lowest estimate
was recorded in Mud Lake, where the highest
percentage of total catch was <40 mm TL, while the
highest estimate was for Carancahua. The density
in Mushroom was close to that in Carancahua.
Although marking methods differed, a 1970 mark-
680
recapture study in Sydnor Bayou provided a popula-
tion estimate for comparison. Marking was accom-
plished by spraying shrimp >40 mm TL with
granular fluorescent pigment (Benton and Lightner
1972). Data analysis was as described for the 1983
Sydnor Bayou study. The average density of shrimp
in Sydnor Bayou during the 1983 study was 37% of
the May 1970 density and was the lowest per hec-
tare estimate of any pond previously sampled (Tkble
3).
We believe that juvenile brown shrimp population
density, determined by the mark-recapture method,
may prove to be a good predictor of offshore pro-
duction as we compile a longer term data base
Although the drop sampler (area-density method)
may measure shrimp density more accurately, the
Peterson mark-recapture method gives a more
precise (having less variance) population estimate
Acknowledgments
We thank the many people who helped us in the
field and processing shrimp; also, Roger Zimmer-
man, for supplying drop sampler data. We are
especially grateful to Don Hanson for allowing us
the use of his property along Sydnor Bayou during
the study.
Literature Cited
Bailey, N. J.
1951. On estimating the size of mobile populations from recap-
ture data. Biometrika 38:293-306.
Baxter, K. N.
1963. Abundance of postlarval shrimp - one index of future
shrimping success. Proa Gulf Caribb. Fish. Inst. 15:79-87.
Benton, R. C, and D. Lightner.
1972. Spray marking juvenile shrimp with granular fluo-
rescent pigment. Contrib. Mar. Sci. 16:65-69.
Berry, R. J., and K. N. Baxter.
1969. Predicting brown shrimp abundance in the north-
western Gulf of Mexico. FAO Fish. Rep. 57, 3:775-798.
Chin, E.
1960. The bait shrimp fishery of Galveston Bay, Ifexas. TVans.
Am. Fish. Soc 89:135-141.
Clark, S. H., and C. W. Caillouet, Jr.
1973. White shrimp {Penaeus setiferus) population trends in
a tidal marsh pond. Mar. Fish. Rev. 35(3-4):27-29.
Costello, T. J., and D. M. Allen.
1962. Survival of stained, tagged, and unmarked shrimp in
the presence of predators. Proa Gulf Caribb. Fish. Inst.
14:16-19.
Emiliani, D. a., and F. Marullo.
1973. Portable barge for estuarine research. Mar. Fish. Rev.
35(l-2):27-29.
Farmer, A. S. D., and M. H. Al-Attar.
1979. Results of shrimp marking programmes in Kuwait.
Kuwait Bull. Mar. Sci. 1:1-32.
Holt, B.
1982. Short term mortality of tagged shrimp during field tag-
ging experiments. U.S. Dep. Commer., NOAA Tfech. Memo.
NMFS-SEFC-97, 9 p.
Howe, N. R., and P. R. Hoyt.
1982. Mortality of juvenile brown shrimp Penaeus aztecus
associated with streamer tags. Trans. Am. Fish Soa 111:
317-325.
Klima, E. F.
1965. Evaluation of biological stains, inks, and fluorescent
pigments as marks for shrimp. U.S. Fish WOdl. Serv., Spea
Sci. Rep. 511, 8 p.
Klima, E. F, K. N. Baxter, and F. J. Patella, Jr.
1982. A review of the offshore shrimp fishery and the 1981
Ifexas Closure Mar. Fish. Rev. 44(9-10):16-30.
RiCKER, W. E.
1975. Computation and interpretation of biological statistics
of fish populations. Bull. Fish. Res. Board Can. 191, 382 p.
SlEGEL, S.
1956. Nonparametric statistics for the behavioral sciences.
McGraw-Hill, N.Y., p. 52-60.
Zimmerman, R. J., T. J. Minello, and G. Zamora.
1984. Selection of vegetated habitat by brown shrimp, Penaeus
aztecus, in a Galveston Bay salt Marsh. Fish. Bull., U.S.
82:325-336.
Loretta F Sullivan
Table 3.— Summary of juvenile brown shrimp population studies in Texas coastal ponds.
Number
Percent
Number
Number
marked
released
Percent
40+ mm
95%
Start
5-min
shrimp
Percent
and
and
marking
population
confidence
Location
date
tows
caught
<40 mm
released
recovered
mortality
per hectare
intervaP
Sydnor Bayou
32.4 ha
5/31/83
49
5,188
0.3
3,994
5.9
4.0
6,412
5,583-7,244
36.4 ha
5,709
4,970-6,448
Sydnor Bayou
32.4 ha
5/21/70
32
8,045
—
7,718
1.7
4.0
17,933
14,198-20,042
36.4 ha
15,238
12,637-17,839
Mud Lake
6.4 ha
6/3/71
27
6,750
20.0
6,120
10.8
4.0
7,490
6,956-8,025
Carancahua
3.5 ha
6/7/71
26
6,301
7.0
4,574
9.8
8.0
15,697
11,815-17,087
Mushroom
1.8 ha
7/2/71
24
8,348
6.0
4,142
28.8
4.0
14,375
13,628-15,120
'Bailey (1951) large sample variance.
681
Southeast Fisheries Center Galveston Laboramry
National Marine Fisheries Service, NOAA
Jt700 Avenue U
Galveston, TX 77550
Present address: 1 78 Plaza Circle
Danville, CA H526
Dennis A. Emiliani
K. Neal Baxter
Southeast Fisheries Center Galveston Laboratory
National Marine Fisheries Service, NOAA
4700 Avenue U
Galveston, TX 77550
A POSSIBLE LINK BETWEEN COHO
(SILVER) SALMON ENHANCEMENT AND
A DECLINE IN CENTRAL CALIFORNIA
DUNGENESS CRAB ABUNDANCE
Dungeness crab, Cancer magister, are taken com-
mercially along the west coast of the contiguous
United States from Avila, CA, to Destruction Island,
WA (Fig. 1). During the early years of the Califor-
nia Dungeness crab fishery, effort was concentrated
on the central California population which produced
most of the state's landings (Fig. 2). The northern
population subsequently became the major con-
tributor to California's landings after an expansion
of the fishery there during the 1940's.
Northern California landings (Fig. 2) generally
have followed a fluctuating pattern similar to one ex-
pressed in Oregon and Washington; however, land-
ings from the relatively isolated central California
population failed to recover from a coastwide low
during the early 1960's. The lower landings reflect
a long-term reduction in abundance which has been
variously attributed to egg predation by a nemer-
tean worm Carcinonemertes errens (Wickham 1979)
and to the effects of a long-term change in oceanic
conditions (Wild et al. 1983).
The failure of the central California population to
recover from the coastwide period of low abundance
also occurred about the time coho salmon, Oncorhyn-
chus kisutch, reared in Oregon and Washington
hatcheries began to make a significant contribution
to the west coast salmon fishery (Oregon Depart-
ment of Fish and Wildlife 1982). The effect of
salmonid predation on commercially important
marine crustaceans has received little attention,
although it is suspected that predation by salmonids
introduced into a number of both small and large
freshwater lakes (Nilsson 1972; Morgan et al. 1978)
has substantially altered the abundance and species
composition of their planktonic crustacean com-
munities. Since numerous salmonid food habit
studies (Heg and Hyning 1951; Petrovich 1970; Reilly
1983a) show that planktonic Dungeness crab
megalops are a major component of the coho salmon
diet, it is conceivable that an increase in the coho
predation rate associated with an influx of hatchery
coho into the central California region is at least par-
tially responsible for the prolonged decline in
Dungeness crab landings.
In this paper I first present evidence showing that
a large portion of the coho salmon ultimately caught
each summer off the west coast are in California
waters during spring, the period Dungeness crab
megalops are most abundant. I then compare and
contrast survival indices to determine if the temporal
variation in survival of both species is consistent with
the predator-prey hypothesis.
Oregon Production Index Area Coho
Each spring and summer, a single coho salmon
brood (year class) is recruited to the commercial
salmon fishery off California, Oregon, and southern
Washington, an area collectively referred to as the
Oregon Production Index area or O.P.I, area (Oregon
Department of Fish and Wildlife 1982). These fish
entered the ocean to feed in May and June of the
previous year, after having spent about 18 months
in freshwater. Coho caught in the O.P.I, area before
1961 (Fig. 3) were predominately wild stocks. These
stocks had declined to extremely low levels by 1960;
however, the successful introduction of Oregon and
Washington hatchery-reared coho resulted in a
return to historical landing levels during the 1960's
and 1970's. Much of the hatchery fish responsible
for the increased landings are derived from early
return Tbutle River coho, which tend to enter
fisheries south of their stream of origin (Hopley
1978).
Coho salmon made up only 10% or less of Califor-
nia's ocean salmon catch prior to the development
of Oregon and Washington enhancement programs
(FVy 1973). Most of these wild coho originated in the
streams and rivers of Oregon and Washington (Allen
1965) and were landed primarily in the northern
California ports of Crescent City and Eureka. The
recruitment of hatchery fish increased the average
annual coho contribution to 25% of the total ocean
salmon catch, with the central California ports of
San Francisco and Fort Bragg accounting for a con-
siderably larger portion of the total coho catch.
682
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
Figure 1.— Commercial fishing areas for
Dungeness crab off Washington, Oregon, and
Cahfornia. (Pacific Fishery Management
Council (1979).)
Before 1973, the California salmon season (coho
and Chinook) opened on 15 April, although few coho
were landed before June because of a minimum size
restriction. As Oregon and Washington hatchery
coho became available, a substantial increase in the
hook and release of sublegal ("shaker") fish developed
during the latter half of April to the middle of Juna
In an attempt to reduce the shaker problem, the
season opening for coho was delayed until 15 May
and the minimum size was reduced in 1973 (O'Brien
and Lesh 1975).
California coho catches generally peak in July, then
drop sharply in August, 2 mo before the salmon
season closure The midsummer decline is attributed
to the northward exodus of fish returning to their
natal stream to spawn (Fry 1973). It is however
unclear when and by what route these fish entered
California waters.
A general migration model (Loeffel and Forster
1970; Godfrey et al. 1975; Hartt 1980) proposes that
newly emigrated west coast coho move immediate-
ly northward into the Gulf of Alaska, then during
winter, undertake a southeasterly migration which
brings them back into California, Oregon, and Wash-
683
10
<
Hi
o
r;
t/J
o
f )
to
a
«i
2
i^
ti,
^
c
00
m
CO
r^
00
02
>,
T— I
-a
m
3
ho
0)
O
5
PQ
T— I
lO
cS
o
?.
o
"~^
m
n!
C
U
B
m
c
i3
£
-a
c
^
(fl
r/l
-o
hn
i-;
S'
S
B3
CO
3
m
u
c
fc
"
bo
c
O
CO
O 0)
U
C
3
a
.3 -3
.2 %
^ i
!- . .
2
I
gffi
gOI. X SNOl Diyi3W
684
m
r>.
o
(]}
e
o
r^
•s
01
§
3
O
in
J3
(O
C ,<
■~ (M
_- «
•-H OS
00 ^
Oi —
^ £
o
^ 3
u>
bD-a
3 :73
ti-S:
J3
-w -a
§§
in
2-S
c^-i^
<V '^rl
U. O
CS ^
CC
o <
ndex
tmen
i« UJ
" S
>
O 4>
•*3 Q
o _
3 C
-o P
o bo
in
^ O
§ F
t* o
0) k.
i, ««
O^
o
^
•>-' a
.£"§
be ^
.£ a
in
c £
CO
^
CQ
C C
o O
E ^
13
at
o
en
%
1
CO
a
»
in
p
(M
o
.OL X SNOl Diai3W
685
ington coastal waters each spring. Coho returning
to the coast south of their natal stream would subse-
quently undergo the observed northward spawning
migration. Each of these authors conceded however,
that certain stocks or different portions of the same
stocks may follow entirely different migratory
routes. Scarnecchia (1981) felt that many coho pro-
duced along the west coast may either remain in ad-
jacent coastal waters or move directly south after
emigration from freshwater.
The dispersal pattern of 437 coho salmon tagged
off northern California early in the 1971 and 1972
seasons clearly showed the northward movement of
adult coho out of California (O'Brien 1973). Nearly
all of the tagged fish recaptured in California were
caught in May and June of each year while tagging
was still being conducted. Oregon recoveries peak-
ed in July and the first half of August, while most
Washington recoveries occurred during the latter
half of August through September.
California's share of the recaptured coho tagged
off northern California (O'Brien 1973) was 9.3% in
1971 and 8.8% in 1972. These percent returns are
very similiar to California's 13.0% and 8.3% share
of the O.P.I, area catch in 1971 and 1972 respective-
ly. Because, for practical purposes, one can assume
that all of the coho caught in California originate
to the north, the similarity between California's catch
and tag returns would indicate that nearly all O.P.I,
area coho stocks were off California during the tag-
ging period. This supposition is extreme, but the
results do suggest that a major portion of the coho
ultimately caught in the O.P.I, area each year are in
California waters during spring. The northward
migration of large numbers of coho is further sup-
ported by the northward progression of peak
monthly catches within the O.P.I, area (Pacific
Fishery Management Council 1983), and the
monthly catch distribution of hatchery marked coho
(Hopley 1978).
Survival Indices Comparison
and Discussion
Dungeness crab, unlike coho salmon, do not move
any appreciable distance, therefore local landings are
considered to be a good indicator of local abundance
In California seasonal landings are composed of at
least three year classes, however northern Califor-
nia landings are generally dominated by 4-yr-old crab
(Warner 1985), while central California landings,
because of a faster growth rate, are dominated by
3-yr-old crab (Collier^).
An alignment of Dungeness crab seasonal landings
with their dominant or "primary" year classes (Fig.
4) generates reasonably representive year class in-
dices, if it is taken into consideration that extreme-
ly abundant year classes, such as the 1966 and 1972
year classes in northern California, probably
dominate landings for more than 1 yr (Methot and
Botsford 1982). The Dungeness crab year class in-
dices (Fig. 4) suggest that a period of poor landings
in both central and northern California during the
early 1960's (Fig. 2) reflects poor survival of the
1958-60 year classes.
As mentioned earlier, northern California landings
have been characterized by large seemingly cyclic
fluctuations, the cause of which has been the sub-
ject of considerable research and debate (see Methot
and Botsford 1982; Botsford 1984, for a review of
this work). Of the hypotheses generated by these in-
vestigations. Wild et al. (1983) presented, in my opin-
ion, the most tenable explanation for this particular
period of low survival. They attributed the drop dur-
ing this period to a reproductive failure caused by
an unprecedented warming of coastal waters
associated with the 1957 El Nino (the "warm water
years" 1957-59, Radovich 1961).
The apparent recruitment of Dungeness crab to
the northern California population of a "normal"
year class in 1961 (Fig. 4), with the return of "nor-
mal" environmental conditions, ushered in several
years of good survival. This recovery was not
duplicated in the central California population,
where a drop in the strength of the 1961 year class
anteceded an extended period of poor survival. Wild
et al. (1983) further proposed that a major change
in the oceanic regime off central California is the
primary cause of the continued poor survival there,
although they do concede that ocean temperatures
in certain years appear to have been favorable to
Dungeness crab survival. Wickham (1979), on the
other hand, suggested that the central California
population has reached a new equilibrium, with
worm predation now being the dominant biological
control. It has yet to be proven which, if either, of
these mechanisms is the primary cause of the con-
tinued poor survival in central California.
Alternatively, a direct comparison of O.P.I, catches
with central California Dungeness crab year class
indices (Fig. 5) illustrates a long-term inverse rela-
tionship which developed with the first recruitment
of hatchery-reared coho salmon stocks in 1961. O.P.I,
area landings are used to express the annual sur-
vival of coho potentially impacting central Califor-
'P. Collier, California Department of Fish and Game, 619 Second
St., Eureka, CA, 95501, pers. commun. November 1984.
686
<
_l
o
q:
<
UJ
>-
>-
<
Q.
T3
C
OS
►J
B
o
a?
:S
to
bo
.S ca
J I
cS -^
c cS
O Q
CO
cS C
CO a>
. — . u
o >,
°9 ^
-* -o
OS C
»—* c^
to S
en r
C3 O
m _
m a
a) .—
C s_
C 00
- ho
>^ ^
^ CQ
CS —
Q
0)
1
O
,01 X SNOi OiaiBW
687
CO
<
a:
O
NORTHERN CALIFORNIA
j:;::: central California
i:
—
o
ID
9
1
o
X
o
o
>■
a
u
z
o
»-
<
0
u
X
«
Q
to
in
■
z
u.
tM
Ifl
-J
c
u
3
00
1
CM
1 1 1
O 00 (0
* CM
CM »t
I
CO
1
00
O CM
I
Tt
0)
&
13
r~
t-
t^
Tf
Oi
f— 1
cd
o
Li
o
(fl
on
>vOO
!^
Cfl
£
be
a.
c
CD
-a
-H
c
o
m
H
cfl
<?
o
13
o
8
n
Bj
(Tl
?*
t,
>-H
o
ed
m
y
0)
1
C
c
3
o
Q
1^
oi
3
1
-a
i
•a
u
"(3
c
0)
t)
TS
Gl3
g
0)
.c
t:
o
1
U)
m
a
D
O
,01 X SNOi Oiai3W
688
nia Dungeness crab because of the evidence that
California catch statistics underestimate the number
of fish actually in the state during spring. These land-
ings provide a straightforward measure of brood sur-
vival that is independent of distribution and local
catchability.
Even though the relatively low O.P.I, area landings
in 1961, 1962, 1963, 1977, and 1980 are comparable
with the predecline era, the general pattern of cor-
respondence in Figure 5 is consistent with an in-
crease in the coho salmon predation rate on Dunge-
ness crab megalops. Within the framework of the
predator-prey hypothesis, the association of low O.P.I,
area coho catches during the early years of the hatch-
ery era with reduced Dungeness crab survival would
indicate that a relatively small number of hatchery
coho can effectively surpress megalops survival. This
is particularly apparent when it is considered that
hatchery production was at a minimum during
the 1961-63 period and wild fish still dominated the
catch (Oregon Department of Fish and Wildlife
1982).
The proposed impact of hatchery coho salmon on
the Dungeness crab resource is best explained by the
differences in the "functional response"^ of wild and
hatchery coho salmon. In controlled behaviorial ex-
periments, Glova (1978) found that hatchery fry
(43-88 mm) were largely nonterritorial, exhibiting
a stronger tendency to aggregate than the wild fry.
This behavioral pattern is believed to be the direct
result of the unnaturally high densities found in
hatchery operations. If adult hatchery coho retain
this behavior, the tendency for Dungeness crab
megalops to aggregate or "swarm" in coastal sur-
face waters (Lough 1976) would theoretically make
them more susceptible to predation (Eggers 1976).
Also a reduction in the number of "search images"
available to hatchery fish is believed to result in a
more homogenous diet (Sosiak et al. 1979). Under
these circumstances Dungeness crab megalops may
become a more important component of the hatch-
ery coho salmon diet.
The apparent good survival of the 1961-66 year
classes in northern California (Fig. 5) suggests that
the majority of the hatchery coho salmon produced
during those years concentrated to the south of that
population during the period when Dungeness crab
megalops are most abundant. This supposition,
together with recently acquired evidence that the
central California Dungeness crab population is at
least partially dependent on the recruitment of
southward drifting megalops (Hatfield 1983; Reilly
1983b), further suggest that the theoretical
predation zone critical to the central California
population lies somewhere in the region of strong
upwelling and high productivity between the two
populations (Fig. 1). Not surprisingly, commercial
fishermen have found coho salmon concentrated
either before or early in the season in this region.
The coho salmon stocks initally released during the
early 1960's may possess an inate affinity for these
waters.
Northern California landings of the Dungeness
crab declined again during the 1970-71 season (Fig.
2). This period of low landings is apparently due to
poor survival of the 1967-71 year classes (Fig. 5),
which cannot be readily explained by an extended
period of warmer than normal water. The various
hypotheses to explain the northern California fluc-
tuations notwithstanding, it is possible that hatchery-
reared coho salmon began to limit Dungeness crab
survival in northern as well as central California,
concomitant with increased hatchery production^
and/or environmental caused changes in distribution.
There is some evidence from coho tagging that sup-
ports this supposition.
O'Brien (1973) reported that 17.3% of his return-
ed tags were found in Oregon and Washington hatch-
eries during the 1971 season, whereas in 1972 only
3% were found in the hatcheries. An exceedingly
strong 1972 Dungeness crab year class in northern
California (Warner 1984) is in direct contrast with
the very weak 1971 year class (Fig. 5) and is inversely
related to the small number of tags found in hatch-
eries during the 1972 season. The small percentage
of hatchery returns in 1972 suggest that there were
fewer hatchery coho available for tagging in the
northern California area during the 1972 season, and
this could indicate relatively poor survival of hatch-
ery fish throughout the O.P.I, area. It should be
remembered that hatchery-reared coho theoretical-
ly have a much larger effect on Dungeness crab sur-
vival than wild fish.
Between 1972 and 1977 (Fig. 5), O.PI. area coho
survival and northern California Dungeness crab
survival became more erratic. The association of
relatively good Dungeness crab survival with good
coho landings in 1974 and 1976 may, however, only
indicate that coho were farther south than usual.
McLain and Thomas (1983) showed that both 1973
^In predator-prey theory "functional response" is defined as the
relationship between the rate at which individual predators con-
sume prey and the density of that prey (Holling 1959).
^The number of hatchery-reared coho salmon released in the O.P.I,
area increased from 7.5 million fish in 1960 to 60.8 million fish in
1981 (Oregon Department of Fish and Wildlife 1982).
689
and 1975 were years with an unusually weak Califor-
nia Countercurrent, or conversely, stronger than nor-
mal southward flow and cooler than normal coastal
waters. If yearling coho do move directly into Califor-
nia waters after emigration from freshwater, then
these anomalous conditions may have caused these
fish to move farther south than usual, with the result
that adult coho would have been south of the preda-
tion zone critical to the northern California Dunge-
ness crab population in the spring of 1974 and 1976.
Since 1976 O.P.I, area coho landings have under-
gone an inexplicable decline in spite of increasing
hatchery production. Theoretically, an increase in
Dungeness crab survival should have accompanied
this drop in coho survival. The drop in Dungeness
crab survival, evident in Figure 5, is obviously in-
consistent with the general theory but can be ex-
plained in two ways. First, it should be considered
that the earlier O.P.I, area coho landings contained
far fewer hatchery fish than those during the later
years. It has been estimated that hatchery fish com-
prised 75% of the west coast coho catch by 1977
(Scarnecchia and Wagner 1980). Secondly, a coastal
warming trend that began in 1976 (McLain 1983)
may have resulted in a northward shift in coho
distribution with a concomitant reduction in Dunge-
ness crab megalops survival.
If coho have become the major limiter of Dunge-
ness crab megalops survival within California, then
the observed survival patterns suggest that a group
of coho, possibly representing the original hatchery
stocks, still experience consistently good survival
and continue to move into the predation zone critical
to the central California population. On the other
hand, the more irregular Dungeness crab survival
observed in northern California suggest that
megalops survival there is more dependent on the
vagaries of hatchery-reared coho distribution
associated with environmental nuances.
Admittedly, most of the evidence used to support
the predator-prey hypothesis is circumstantial.
Nevertheless, three of the considerations presented
—1) the fact that coho feed heavily on Dungeness
crab megalops, 2) the evidence showing that many,
if not most, Oregon and Washington hatchery coho
are in California during the period megalops are
most abundant, and 3) the coincidence of the ex-
tended central California Dungeness crab decline
with a large increase in the number of hatchery coho
within the O.P.I, area— suggest a possible relation-
ship that deserves attention.
The capricious nature of predation on the early life
stages of commercially important invertebrates un-
doubtedly contributes to the difficulties encountered
when attempting to manage these relatively short-
lived species on a sustained yield basis. If the hypo-
thesized relationship between coho salmon and
Dungeness crab eventually proves to be correct, then
the salmonid enhancement process itself can be con-
sidered an experiment, offering insight into the role
predators play in controlling the commercial abun-
dance of many marine species.
Acknowledgments
I would like to thank Bob Tksto, John Geibel, Ron
Warner, and two anonymous reviewers for review-
ing the manuscript. Special thanks are also due Bob
Tksto, who offered considerable encouragement, and
Anita Thomas for drafting the figures.
Literature Cited
Allen, G.
1965. Estimating error associated with ocean recoveries of
fin-marked coho salmon. Trans. Am. Fish. Soc 94:319-326.
BOTSFORD, L. W.
1984. Effect of individual growth rates on expected behavior
of the northern California Dungeness crab {Cancer magister)
fishery. Can. J. Fish. Aquat. Sci. 41:99-107.
Eggers, D. M.
1976. Theoretical effect of schooling by planktivorous fish
predators on rate of prey consumption. J. Can. Fish. Res.
Board 33:1964-1971.
Fry, D. H., Jr.
1973. Anadromous fishes of California. Calif. Dep. Fish
Game, Resourc Agency, 111 p.
Glova, G. J.
1978. Behavioral differences between wild and hatchery-
produced coho salmon juveniles and their management im-
plications. In B. G. Shepherd and R. M. J. Ginetz (Rap-
porteurs), Proceedings of the 1977 Northeast Pacific Chinook
and Coho Salmon Workshop, p. 84-88. Can. Fish. Mar. Serv,
Tfech. Rep. 759.
Godfrey, H., K. A. Henry, and S. Machidorl
1975. Distribution and abundance of coho salmon in offshore
waters of the North Pacific Ocean. Int. North Pac Fish.
Comm., Bull. 31:1-80.
Hartt, a. C.
1980. Juvenile salmonids in the oceanic ecosystem— the
critical first summer. In W. J. McNeil and D. C. Himsworth
(editors), Salmonid ecosystems of the North Pacific, p.
25-27. Oreg. State Univ. Press.
Hatfield, S. E.
1983. Distribution of zooplankton in association with Dunge-
ness crab, Cancer magister, larvae in California. In P. W.
Wild and R. N. Tksto (editors). Life history, environment, and
mariculture studies of the Dungeness crab. Cancer magister,
with emphasis on the central California fishery resource, p.
97-123. Calif. Dep. Fish Game, Fish Bull. 172.
Heg, R., and J. Van Hyning.
1951. Food of the chinook and silver salmon taken off the
Oregon coast. Oreg. Fish. Comm., Res. Briefs 3(2):32-40.
HOLLING, C. S.
1959. The components of predation as revealed by a study of
690
small mammal predation of the European pine sawfly. Can.
Entomol. 91:293-320.
HOPLEY, B. B.
1978. Genetic effects on Ibutle-Cowlitz coho studies on the
Columbia River. In B. G. Shepherd and R. M. J. Ginetz (Rap-
parteurs), Proceedings of the 1977 Northeast Pacific Chinook
and Coho Salmon Workshop, p. 103-121. Can. Fish. Mar.
Serv. Tfech. Rep. 759.
LOEFFEL, R. E., AND W. 0. FORSTER.
1970. Determination of movement and identity of stocks of
coho salmon in the ocean using the radionuclide zinc-65.
Oreg. Fish. Comm., Res. Rep. 2(l):15-27.
Lough, R. G.
1976. Larval dynamics of the Dungeness crab, Cancer
magister, off the central Oregon coast, 1970-1971. Fish.
Bull, U.S. 74:353-376.
McLain, D. R.
1983. Coastal ocean warming in the northeast Pacific, 1976-
1983. In W. G. Pearcy (editor). The influence of ocean con-
ditions on the production of salmonids in the North Pacific
- A workshop, p. 61-86. Sponsored by the Cooperative In-
stitute for Marine Resources Studies, Oregon State Univer-
sity Sea Grant College Program, ORESU-W-83-001,
Newport, OR.
McLain, D. R., and D. H. Thomas.
1983. Year-to-year fluctuations of the California Counter-
current and effects on marine organisms. Calif. Coop.
Oceanic Fish. Invest. Rep. 24:165-181.
Methot, R. D., Jr., and L. W. Botsford.
1983. Estimated preseason abundance in the California
Dungeness crab {Cancer magister) fisheries. Can. J. Fish.
Aquat. Sci. 39:1077-1083.
Morgan, M. D., S. T. Threekeld, and C. R. Goldman.
1978. Impact of the introduction of kokanee (Oncorhynchus
nerka) and opossum shrimp (Mysis relicta) on a subalpine
lake J. Fish. Res. Board Can. 35:1572-1579.
Nilsson, N.-A.
1972. Effects of introductions of salmonids into barren lakes.
J. Fish. Res. Board Can. 29:693-697.
O'Brien, R
1973. An evaluation of the California troll silver salmon regu-
lations. Calif. Dep. Fish Game, p. 1-12. (Mimeogr.)
O'Brien, P., and E. W. Lesh.
1975. Preliminary evaluations of the effects of California's new
silver salmon troll regulations on the 1973 and 1974 troll
seasons. Appendix 2 - Special report. In Pacific Marine
Fisheries Commission, 27th Annual Report for the Year 1974,
p. 49-53.
Oregon Department of Fish and Wildlife.
1982. Comprehensive plan for production and management
of Oregon's anadromous salmon and trout. Part 2, Coho
salmon plan. Oreg. Dep. Fish Wildl., var. pag.
Pacific Fishery Management Council.
1979. Draft management plan for the Dungeness crab fishery
of Washington, Oregon, and California. Portland, OR, 93
P-
1983. Proposed plan for managing the 1983 salmon fisheries
off the coasts of California, Oregon, and Washington. An
amendment and supplemental environmental impact state-
ment to the "Fishery Management Plan for Commercial and
Recreational Salmon Fisheries off the Coasts of Washington,
Oregon, and California Commencing in 1978." Pacific
Fisheries Management Council (526 S.W. Mill Street,
Portland, OR), var. pag.
Petrovich, A. A., Jr.
1970. Biota of nearshore waters off Humboldt Bay and
Trinidad Head 1960-1964, as shown by the diet of Pacific
salmon. M.S. Thesis, Humboldt State Univ, Areata, CA, 69
P-
Radovich, J.
1961. Relationships of some marine organisms of the north-
east Pacific to water temperature Calif. Dep. Fish Game,
Fish Bull. 112:1-62.
Reilly, P N.
1983a. Predation on Dungeness crabs. Cancer magister, in
central California. In P. W. Wild and R. N. Tksto (editors).
Life history, environment, and mariculture studies of the
Dungeness crab. Cancer magister, with emphasis on the cen-
tral California fishery resource, p. 155-164. Calif. Dep. Fish
Game, Fish Bull. 172.
1983b. Dynamics of Dungeness crab. Cancer magister, larvae
off central and northern California. In P. W Wild and R.
N. Iksto (editors), Life history, environment, and mariculture
studies of the Dungeness crab. Cancer magister, with em-
phasis on the central California fishery resource, p.
57-84. Calif. Dep. Fish Game, Fish Bull. 172.
Scarnecchia, D. L.
1981. Effects of streamflow and upwelling on yield of wild
coho salmon {Oncorhynchus kisutch) in Oregon. Can. J. Fish.
Aquat. Sci. 38:471-475.
Scarnecchia, D. L., and H. H. Wagner.
1 980. Contribution of wdld and hatchery-reared coho salmon,
Oncorhynchus kisutch, to the Oregon ocean sport fishery.
Fish. Bull., U.S. 77:617-623.
Sosiak, a. J., R. G. Randall, and J. A. McKenzie.
1979. Feeding by hatchery- reared and wild Atlantic salmon
(Salmo salar) parr in streams. J. Fish. Res. Board Can.
36:1408-1412.
Warner, R. W.
1985. Age and growth of male Dungeness crabs. Cancer
mngister, in northern California. In Proceedings of the Sym-
posium on Dungeness Crab Biology and Management, p.
185-187. Lowell Wakefield Fish. Symp. Ser., Univ. Alaska,
Sea Grant Rep. 85-3.
Wickham, D. E.
1979. Carcinonemertes errans and the fouling and mortality
of eggs of the Dungeness crab, Cancer magister. J. Fish.
Res. Board Can. 36:1319-1324.
Wild, P W, P M. W. Lav^^, and D. R. McLain.
1983. Variations in ocean climate and the Dungeness crab
fishery in California. In P. W. Wild and R. N. Tksto (editors),
Life history, environment, and mariculture studies of the
Dungeness crab. Cancer magister, with emphasis on the cen-
tral California resource, p. 175-188. Calif. Dep. Fish Game,
Fish Bull. 172.
David H. ThoMAS
Marine Resources Region
California Department of Fish and Game
If 11 Burgess Drive
Menlo Park, CA H025
691
THE EFFECTS OF NET ENTANGLEMENT ON
THE DRAG AND POWER OUTPUT OF
A CALIFORNIA SEA LION,
ZALOPHUS CALIFORNIANUS
Interactions between pinnipeds and fisheries can be
broadly divided into two categories: the role of pin-
nipeds on the mortality of commercially important
fish species and the effect of commercial fisheries
on the dynamics of pinniped populations. Although
the former has received considerable attention
(Hirose 1977; Fiscus 1979, 1980; Matkin and Fay
1980; DeMaster et al. 1982), the importance of the
latter has been addressed only recently (Shaugh-
nessy 1980; Fowler 1982; Scordino and Fisher
19831).
Fishery interactions may affect pinniped stocks
through changes in prey abundance, incidental takes,
or entanglement in discarded fishing gear and plastic
packing bands. Scordino and Fisher (fn. 1) have
shown that the number of entangled northern fur
seals, Callorhinus ursiniLS, on the Pribilof Islands,
AK, has recently increased, and now comprises 0.4%
of the harvested animals. Fowler (1982^) reviewed
existing data concerning the accumulation of plastic
litter on beaches of several Alaskan islands. Using
the number of net fragments found on shore as a
rough estimate of the size distribution of material
adrift at sea, he concluded that at least 60% are
larger than those measured on fur seals. Because
most nets found on these animals weigh <600 g, a
significant mortality undoubtedly occurs at sea from
entanglement in larger fragments.
This paper evaluates the hydrodynamic effect of
net entanglement and documents the behavior of an
entangled animal. A California sea lion was trained
to allow itself to become entangled in a twine trawl
net fragment and the subsequent rise in drag was
measured. Increased energy consumption and swim-
ming power requirements associated with dragging
net fragments were calculated from these measure-
ments. The results provide an initial basis for assess-
^Scordino, J., and R. Fisher. 1983. Investigations on fur seal
entanglement in net fragments, plastic bands and other debris in
1981 and 1982, St. Paul Island, Alaska. Background paper sub-
mitted to the 26th Annual Meeting of the Standing Scientific Com-
mittee, North Pacific Fur Seal Commission, 33 p.
^Fowler, C. W. 1982. Entanglement as an explanation for the
decline in Northern fur seals of the Pribilof Islands. Background
paper submitted to the 25th Annual Meeting of the Standing Scien-
tific Committee, North Pacific Fur Seal Commission, 24 p.
y
C
Figure 1.— Instruments and cart used in the drag experiments. The sea lion was towed passively underwater and the resultant force
recorded. See text for further details.
692
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
ing the possible role of net entanglement on the mor-
tality of pinnipeds at sea.
Materials and Methods
A female California sea lion, Zalophus califor-
nianus, was used in this work. The animal was kept
in large seawater holding tanks at Scripps Institu-
tion of Oceanography. Its weight (45 ± 0.5 kg) re-
mained constant throughout the course of this study,
conducted during April 1983.
lb measure drag, the sea lion was trained to bite
onto a neoprene mouthpiece and be towed through
the water behind a moving cart (Fig. 1). The cart,
powered by a variable speed electric motor, travel-
led around a circular "ring" tank which had a depth
of 3.5 m and inner and outer diameters of 14.5 and
21 m, respectively. A line was connected to the
mouthpiece and the other end secured to a load cell
(Western Scale Co.) which produced a voltage out-
put proportional to the amount of tension on the lina
The tow line extended down from the load cell,
through a streamlined strut and around a teflon
pulley attached to the end of the strut (Fig. 1). The
pulley, enclosed by a streamlined fiberglass housing,
was set at a depth of 1 m (>3 body diameters) to
eliminate surface wave effects on drag (Hoerner
1959).
Drag was measured by continuously recording the
signal output from the load cell during each towing
session. The signal was amplified and recorded on
a Brush^ 220 strip chart recorder (Gould In-
struments). At the end of each session, the load cell
was calibrated using a hand-held dynamometer. A
tachometer, attached to one of the outer cart wheels,
was used to determine cart velocity. This was
simultaneously recorded on the strip chart. The sea
lion's velocity, while it was being towed down the mid-
dle of the tank, was computed using the speed of the
outer wheel and the tank's circumference After each
experiment the data were smoothed by eye and drag
and velocity determined. Only steady traces which
varied less than ±3% were analyzed. Drag was then
converted to newtons by multiplying the kilogram
force reading of the load cell by the acceleration of
gravity.
Once the sea lion's drag without a net was
measured, the animal was trained to place its head
through an opening cut in the mesh of a 1/8-in (3.2
mm) nylon twine trawl net. The opening was near
the center of the net which measured 1.4 m x 5 m,
with a stretched mesh size of 19 cm. The net had
a dry weight of 580 g. After several trials, the sea
lion became accustomed to the procedure and would
allow itself to be towed with the net trailing from
its neck. The net was removed after each session.
Results
Drag on the sea lion, both with and without the
net, increased with velocity (Fig. 2). This rise,
however, was significantly greater when the animal
was entangled, with the difference between the two
curves increasing throughout the range of speeds.
At the highest velocity of 3.5 m/s, the entangled drag
was 111 N greater than that of the free animal (Tkble
1). Therefore, to maintain a cruising speed of 2.0 m/s
an animal of this size, entangled in a net with similar
hydrodynamic characteristics, would experience the
equivalent drag of a free animal swimming at speeds
above 4 m/s.
Power that the sea lion must expend for swimming
can also be calculated from these measurements.
Since drag is a force, power output (in watts) is a
product of drag times swimming velocity (Webb
1975): Pq = drag x velocity. Tkble 1 shows the
results of such calculations and the effect of the net
on the sea lion's required output.
Power output is a measure of the mean rate of
energy expended by the swimming muscles at a
given velocity (Webb 1975). It does not, however,
reveal the total energetic requirements of the sea
150t
CO
§100
LU
o 50
<
tr
o
"t
WITH NET /
. _--v
^^-^» WITHOUT
,y-rfr' NET
^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
0 12 3 4
VELOCITY (M/S)
Figure 2.— Drag of a 45 kg sea lion with and withoug a net trail-
ing from its neck. In both cases drag increased geometrically with
speed. The regression equation with the net was 17.19 vel.'^^, SEE
(standard error of estimate) = 0.052. The equation for drag without
the net was 2.93 vel.^•"^ SEE = 0.118.
693
Table 1.— The increase in drag and power output, and the estimated power
input of the entangled sea lion. Drag with and without the net was calculated
from the best fit regressions determined by the experiments. Power output
was calculated by multiplying drag and the appropriate velocity. Weight
specific power input is based on an efficiency (power out/power in) of 10%.
Velocity (m/s)
1.0
1.5
2.0
2.5
3.0
.3.5
Drag (N)
Without net
2.93
6.75
12.21
19.33
28.13
38.64
With net
17.19
34.66
57.01
83.87
114.97
150.11
Power output (W)
Without net
2.93
10.13
24.42
38.65
84.40
135.24
With net
17.19
51.99
114.02
167.74
344.91
525.39
Power input (W/kg)
Without net
0.7
2.3
5.4
8.6
18.8
30.0
With net
3.8
11.6
25.3
37.3
76.6
116.8
lion. Animals are not 100% efficient in converting
metabolic energy to mechanical power needed for
locomotion (Hicker 1975). Studies of penguins and
fish which swim with their pectoral fins show that
efficiency (power output/power input) varies between
5 and 15% (Webb 1973; Hui 1983). Female north-
ern fur seals consume about 8 W/kg while at sea
(Costa and Gentry in press). Using this number, the
power output values estimated for the sea lion, and
an assumed cruising speed of 2.5 m/s, an efficiency
for fur seals of roughly 10% is obtained. Tkble 1
shows estimated energy requirements based on this
efficiency for the sea lion with and without the net.
Again it can be seen that to maintain a swimming
speed of 2.5 m/s the sea lion would need to increase
its metabolic expenditure by 50-fold, an impossibly
high figure (Bartholomew 1977).
Discussion
There is little doubt that for an animal of this size,
entanglement in a 600 g net will substantially in-
crease its chance of mortality at sea. Drag, and hence
the power required for swimming, is increased by
the presence of a net. As a result, these animals will
swim slower, at a greater energetic cost than free
animals. Drag of the net, which rises geometrically
with velocity, will prevent activities requiring high
speeds as would be the case if such animals engaged
in the pursuit of rapidly moving or evasive prey
species. Additionally, migration or travel to and from
the rookery will be energetically more costly. It is
likely, then, that once an animal becomes entangled
in net fragments of this size or larger, it enters a
state of negative energy balance
The animal's size as well as the size of the net plays
an important role in the amount of drag experienced.
A larger net will present more surface area to the
water. Since drag is dependent on surface area
(Vogel 1981), larger net fragments will result in
greater drag. Similarly, if two different-sized animals
are entangled in nets of the same dimensions, the
smaller will experience a larger relative increase in
its drag and power requirements. If animals of dif-
ferent age classes encounter net fragments with
equal probability, it is expected that the younger age
classes will suffer a proportionally higher mortality.
Although starvation is undoubtedly the long-term
result of net entanglement, other factors may have
a more immediate effect. This was particularly evi-
dent during an observation of an actual entangle-
ment. In the initial training phase of the sea lion,
a net with a larger mesh size was used. At one point,
while the net was floating in the water, the sea lion
swam up from below and inserted its head through
one of the mesh openings. Upon sensing the net
around its neck it gave a strong backwards stroke,
trying to retract its head. The backward movement
brought some of the trailing net in front of it and
when the animal then swam forward and dived
underwater, another strand slipped onto its neck.
This caused a violent reaction with the sea lion
twisting and thrashing wildly. The twisting further
entangled the animal and tightened the net. Within
IV2 to 2 min the animal was completely entangled
with three or four loops of mesh tight around its
neck.
The net was so tight that an observer on the side
of the tank was unable to pull it from the sea lion's
head, and it was necessary to drain the holding tank.
During this time, the animal swam around the tank
barking and often thrashing about while trying to
bite the net. This appeared to further tighten the
net which, when finally removed, was so tight that
a finger could not be slipped between the net and
the animal's neck.
694
If the behavior of otariids at sea is similar to that
exhibited by the entangled sea lion, then drowning
may be another more immediate cause of mortality.
Twisting and rolling could foul the foreflippers and
prevent the animal from swimming. This seems par-
ticularly likely if it became caught in a larger net.
Additionally, because the net was so tightly wrap-
ped around the sea lion's neck, necrosis of the skin
tissue and an open wound may have occurred within
a matter of hours to a few days. Constant swimming
could continue to tighten the net. Although several
authors (Scordino and Fisher fn. 1) have speculated
that neck wounds indicate a period of entanglement
longer than 4 mo, these observations suggest that
beached animals with open wounds may have become
tangled only a few days prior to sighting.
Acknowledgments
The sea lion was made available for this research
by L. H. Cornell, Sea World of San Diego. The
assistance provided by Phil Thorson and Tferrie
Williams in feeding and training the sea lion is grate-
fully acknowledged and appreciated. C. Fowler, J.
Graham, G. Kooyman, and T Williams provided
useful comments on the manuscript.
This study was supported by NOAA grant
82ABC-02743 from the National Marine Mammal
Laboratory to G. L. Kooyman.
Literature Cited
Bartholomew, G. A.
1977. Energy metabolism. In M. S. Gordon (editor), Animal
physiology: Principles and adaptations, p. 57-110. Macmillan
Publ. Co., N.Y.
Costa, D. P., and R. L. Gentry.
In press. Free ranging energetics of northern fur seals. In
R. L. Gentry and G. L. Kooyman (editors), Fur seals: Mater-
nal strategies on land and at sea. Princeton University
Press.
DeMaster, D. P., D. J. Miller, D. Goodman, R. L. DeLong, and
B. S. Stewart.
1982. Assessment of California sea lion fishery interactions.
Trans. N. Am. Wildl. Nat. Resour. Conf. 47:253-264.
Fiscus, C. H.
1979. Interactions of marine mammals and Pacific
haka Mar. Fish. Rev. 41(10):l-9.
1980. Marine mammal-salmonid interactions: a review. In W.
J. McNeil and D. C. Himsworth (editors), Salmonid eco-
systems of the North Pacific Ocean, p. 121-131. Oregon
State Univ. Press, Corvallis.
Fowler, C. W.
1982. Interactions of northern fur seals and commercial
fisheries. Trans. N. Am. Wildl. Nat. Resour. Conf. 47:278-
292.
Hirose, p.
1977. Incidence of seal-damaged salmonids sampled from the
lower Columbia river gillnet fishery, 1972-1976. Oreg. Dep.
Fish Wildl, Inf. Rep. 77-4, 6 p.
Hoerner, S. F.
1959. Fluid-dynamic drag. Practical information on aero-
dynamic drag and hydrodynamic resistance [Published by
the author.] Midland Park, N.J. 416 p.
Hui, C. A.
1983. Swimming in penguins. Ph.D. Thesis, Univ. California,
Los Angeles, 185 p.
Matkin, C. 0., and F H. Fay.
1980. Marine mammal-fishery interactions on the Copper
river and in Prince William Sound, Alaska, 1978. Final
Report to U.S. Marine Mammal Commission for contract
MM8AC-013, 71 p. Publ. No. PB80-159536, Natl. Tfech. Inf.
Serv., Springfield, VA.
Shaughnessy, p. D.
1980. Entanglement of Cape fur seals with man-made objects.
Mar. Pollut. Bull. 11:332-336.
Hjcker, V. A.
1975. The energetic cost of moving about. Am. Sci. 63:413-
419.
VOGEL, S.
1981. Live in moving fluids: The physical biology of flow.
Willard Grant Press, Boston, MA, 352 p.
Webb, R W.
1973. Efficiency of pectoral-fin propulsion of Cymatogaster
aggregata. In T. Y. -T. Wu, C. J. Brokaw, and C. Brennen
(editors). Swimming and flying in nature. Vol. 2, p. 423-1005.
Plenum Press, N.Y.
1975. Hydrodynamics and energetics of fish propulsion. Fish.
Res. Board Can. Bull. 190, 158 p.
Steven D. Feldkamp
Scripps Institution of Oceanography
Physiological Research Laboratory A-004
La Jolla, CA 92093
Present address: Long Marine Laboratory
University of California at Santa Cruz
Santa Cruz, CA 9506Jt
NOTES ON THE LIFE HISTORY OF
THE CATSHARK, SCYLIORHINUS MEADI
The catshark, Scyliorhinus meadi (family Scylio-
rhinidae) is a rare, poorly known species, easily iden-
tified by the eight dark saddle-like blotches along the
dorsal surface Springer (1966) first described S.
meadi and Springer and Sadowski (1970) assigned
it to subspecies status of S. retifer. In Springer's
(1979) revision of the family, it was again given
species status. At present only 10 immature
specimens of 5. meadi have been collected, seven
males (180-490 mm in length), two females (235 and
385 mm in length), and one 190 mm specimen of
unknown sex. This paper reports on the collection
of an additional specimen of S. meadi and provides
valuable life history information.
During a cruise aboard the RV Delaware II on 5
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
695
May 1984, a specimen of S. meadi was collected at
a depth of 412 m using a 17 m otter trawl at lat.
28°59.85'N, long. 79°55.98'W. The shark measured
430 mm in length and weighed 0.4 kg. This shark,
together with its stomach contents, is deposited at
the Ichthyological Museum of the Florida Depart-
ment of Natural Resources, St. Petersburg (FSBC
16208). Examination of the reproductive system
revealed a developing right ovary measuring 4.4 cm
long and 0.6 cm wida The left ovary was atrophied.
Follicles teased from the right ovary measured 0.75
mm in diameter. The nidamental glands were 3.0 mm
wide and 8.0 mm long. The oviduct, from nidamen-
tal gland to vagina, was 82 mm long and 1.0 mm
wide Gut content examination revealed several
cephalopod beaks and tentacles, shrimp remains, and
the articulated caudal skeleton from a relatively
large, unidentified teleost.
This specimen of S. meadi is the third and largest
female collected to date. Burgess et al. (1979)
reported on the collection of a 385 mm total length
female in which the right ovary measured 33.2 mm
and the left 8.9 mm in length. This represents about
8.6% of the total length of the shark. The right ovary
of the specimen reported in this paper represents
about 10.2% of the shark's total length. This
specimen is immature, but the allometric increase
in ovary length, and the fact that the left ovary was
completely atrophied suggests that the specimen
might be considered a subadult (maturation begun).
The small size of the Florida Bahama specimens
compared with the North Carolina examples led
Burgess et al. (1979) to suggest geographical size
segregation. This large specimen from off the cen-
tral Florida east coast does not support this segrega-
tion. Discovery, in gut content examination, of the
large, teleost caudal skeleton suggests an unexpected
ability to prey on relatively large fishes.
Acknowledgments
I would like to thank David Camp, Mark Leiby, Bill
Lyons, Mike Murphy Jim Quinn, Steve Ealsh, and
the captain and crew of the RV Delaware II.
Literature Cited
Burgess, G. H., G. W. Link, Jr., and S. W. Ross.
1979. Additional marine fishes new or rare to Carolina waters.
Northeast Gulf Sci. 3(2):74-87.
Springer, S.
1966. A review of western Atlantic cat sharks, Scyliorhinidae,
with descriptions of a new genus and five new species. U.S.
Fish. Wildl. Serv., Fish. Bull. 65:581-624.
1979. A revision of the catsharks, Family Scyliorhinidae U.S.
Dep. Commer., NOAA Ttech. Rep. NMFS Cir. 422, 152 p.
Springer, S., and V. Sadowsky.
1970. Subspecies of the western Atlantic cat shark,
Scyliorhinus retifer. Proa Biol. Soc Wash. 83:83-98.
Glenn R. Parsons
Department of Marine Sciences
University of South Florida
HO Seventh Avenue South
St. Petersburg, FL 33701
A COMPARISON OF SCALE AND
OTOLITH AGING METHODS FOR THE
ALEWIFE, ALOSA PSEUDOHARENGUS '
Beginning in 1971, the Maine Department of Marine
Resources monitored the harvests of anadromous
alewives ascending the Damariscotta River (Libby
1982). Part of this monitoring assessed changes in
age composition within and between years. Aging
was done by interpreting the number of scale annuli
in terms of fish age as has been done in earlier in-
vestigations (Havey 1961; Rothschild 1963; Marcy
1969). However, scale annuli were sometimes difficult
to interpret, so in 1979, methods for removing and
reading alewife otoliths were studied. A relatively
fast and efficient method was developed for remov-
ing otoliths. The ease with which the otoliths were
processed to age fish prompted an analysis of which
method (scales or otoliths) was best for determin-
ing the age of an alewife This paper compares the
precision of reproducibility and accuracy between the
scale and otolith methods.
Materials and Methods
Alewives, Alosa pseudoharengus, were taken daily
from the commercial harvest throughout the fishing
period for their otoliths and scales. The fish were
taken to the laboratory sexed, and measured for
length and weight. About 10 scales were removed
from the left side above the lateral line just posterior
to the dorsal fin. The scales were cleaned and put
into envelopes labeled with the length and sex of the
alewife In 1963, Rothschild described the alewife
scale and characteristics of the annuli.
Otoliths were collected and stored as follows: A
"This study was conducted in cooperation with the U.S. Depart-
ment of Commerce, National Marine Fisheries Service, under
Public Law 89-304, as amended, Commercial Fisheries Research
and Development Act, Project AFC-21-1.
696
FISHERY BULLETIN; VOL. 83, NO. 4, 1985.
transverse cut was made at the point of attachment
of the operculum, which severed the head leaving
some attachment of skin to the body. The head was
then pulled away from the body removing the gills,
leaving the skull clear of the gills and viseral blood.
When time did not permit for further processing,
all the heads from a day's sample were placed onto
a tray and frozen for later analysis. For otolith
removal, the head was held ventral side up and a
transverse cut was made into the skull at the point
of dorsal musculature attachment (Fig. la). A cor-
rect cut was sliced through the ends of the semicir-
cular canals containing the sagitta otolith (Fig. lb).
Kornegay, in 1978, described the sagitta otolith that
is used for age determination of the alewifa
Each otolith was extracted with microforceps,
placed on absorbent paper, and rubbed lightly to
remove any adhering tissue. After drying, otoliths
were placed in depressions in black Plexiglas^ trays
and covered with Permount (see Libby 1982).
Williams and Bedford (1974) described the growth
and collection of otoliths and interpretation of otolith
annuli in general. The Atlantic herring, Clupea
harengus, otolith which is similar to the alewife
otolith, was described by Watson (1964). He reported
on the high validity of its use for aging and the high
reproducibility of readings between readers.
Scales and otoliths were collected from 536 fish.
Thirty-one fish were discarded because the otoliths
or scales were unreadable or the shape of the otolith
revealed that the fish was a blueback, A. aestivalis.
Price (1978) explained the difference in otolith mor-
phology between the two species. A final count of
^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service^ NOAA.
Figure 1.— a) Ventral side of head of Alosa
pseudoharengtis. Dark line shows muscula-
ture attachment to the skull where transverse
cut is made b) Section of skull cut away
showing posterior ends of the semicircular
canals containing the sagitta otoliths.
697
505 alewives was used for the analysis. Otoliths and
scales were read using a binocular dissecting scope
at 30x-60x.
Each otolith and scale for an age shown in Figure
2 was collected from the same fish. The otoliths were
taken from the left side of the head and each scale
was chosen for the best annuli appearance of all
scales from that fish. The scale annuli shown are at
the anterior portion of the scale that is normally
covered by surrounding scales. The otoliths were
photographed with a 35 mm camera mounted on a
microscope at 11 x.
Aging was done independently by two people
(readers; subsequently referred to as R^ and Rg).
Ages derived from scales and otoliths by each reader
were referred to as an age set. Scales and otoliths
were read without knowledge of fish length or sex.
A true age was established for each fish by reexamin-
ing scales and otoliths together with length and sex.
The five age sets were compared to show 1) the preci-
sion of aging reproducibility (measurement of how
close the ages are for two or more readings); and
2) the aging accuracy (age determinations compared
with the true age).
Three analyses were used to evaluate precision and
accuracy. Percent agreement (PA) compared two to
three age sets to reveal what portion of the fish were
aged alike between age sets. An index of average per-
cent error (APE) developed by Beamish and Four-
nier (1981) was used to show the degree of varia-
tion between age sets. APE is expressed as
1
N
I
1
R
I
l^y
X,
where N is the number of fish aged; R is the number
of ways each is aged; X^ is the ith determination of
3yr. 259mm (f
4yr. 2 8 I mm (f
5yr. 293mm <f
Figure 2.— Gross comparisons of otoliths and scales of alewives from ages 3 through 7. The otolith and scale were taken from the
same fish for each age The age-3 otolith shows: A - anterior; P - posterior; D - dorsal; and V - ventral orientation of the otoliths
698
the jth fish; the Xj is the mean age calculated for
the jth fish. The third method used the mean coeffi-
cient of variation (V) (Chang 1982). This was an alter-
native index to APE that provided a statistical test
of reproducibility between agings. The coefficient
was a measure of the standard deviation between
all ages of fish divided by the mean age. The sum
of the coefficients was then divided by the number
of fish aged. PA, APE, and V are all expressed as
percents.
The difference between PA and APE or V is that
the former measures the actual agreement between
age sets and the latter measures the amount of varia-
tion between age sets. TWo treatments (a treatment
was the comparison of two or more age sets) that
had the same PA values might have differing degrees
of variation and therefore different values of APE
or V. The smaller the APE or V values, the less varia-
tion there was between age determinations.
Values for PA, APE, and V were computed for 10
treatments: scales vs. otoliths from R^; scales vs.
otoliths from Rg; scales from Rj vs. R2; otoliths
from Rj vs. R2; scales from Rj and R2 vs. true age;
otoliths from R^ and Rg vs. true age; male scales
from Rj vs. R2; female scales from R^ vs. R2; male
otoliths from R^ vs. R2; and female otoliths from Rj
vs. R2. Treatments were also compared as to the
relative sizes of the PA, APE, and V values.
Results
Figure 2 compares the physical appearance of
otoliths and scales for ages 3 through 7. The photo-
graph of the age-3 otolith shows its orientation as
it lies in the sacculus. The dorsal side, including the
anti-rostrum, shows the best contrast between the
light opaque (summer growth) regions and the dark
hyaline (winter growth) regions. The annular rings
6yr. 328mm 9^
7yr. 326 mm %
in the sacculus. Lines drawn on the otoliths and scales show annular growth.
699
at this site are, for the most part, continuous and
distinct. The annular markings on the scales are not
as distinct or as sharp in contrast as on the otoliths.
The scale annuli from the first three ages are well
defined, but in ages 6 and 7 the outer annuli start
to run together and the scale margin shows wear
from resorption and deterioration. In contrast, the
age-6 and -7 otoliths still reveal distinct annular
rings.
PA, APE, and V values for all 10 treatments are
presented by treatment comparisons in Tkble 1. The
scale vs. otolith treatments were compared to deter-
mine how similar the two readers were in inter-
preting scale and otolith annuli. The PA values
(82.6%, 80.4%) are relatively close to one another
along with the values for APE and V. These values
did reveal that R^ had more agreement and less
variability between aging scales and otoliths than did
Rg. Tkble lb shows a higher percentage agreement
and less variability between Rj and R2 for otoliths
than for scales.
Comparisons made between treatments of scales
to true age and treatments of otoliths to true age
are shown in Tkble Ic The agreement of otolith ages
to true ages was 10% greater and had half the varia-
tion of scale ages. Treatment comparison between
male and female scale values were about the same
(Ikble Id), whereas the otolith values between sexes
are quite different (Ikble le). The female otolith
treatment had a higher PA value and lower APE and
V values than did the male treatment.
Discussion
The scale vs. otolith treatment (Tkble la) reveal-
ed no real difference in the aging ability of each
reader. There were also higher PA and lower V
values for the treatment of otolith to true age (Tkble
Ic). Therefore, the outcome for other treatments
could be attributed to differences in the aging
methods rather than the aging ability of the readers.
The results of the statistical tests (Tkble lb) sug-
gest that the method of estimating alewif e ages from
otoliths is superior to the method using scales. Ages
derived from otoliths revealed a higher reproduc-
ibility and less variability than those obtained from
scales. These differences between methods were in-
herent within the otoliths of female alewives, which
provided the greatest accuracy and lowest variabil-
ity (Tkble le) within all types of statistical
comparisons.
Female alewives, at one time during their lives,
possibly achieve a faster rate of growth than males.
Cooper (1961), Havey (1961), and Libby (1982) show-
ed that females are larger than males at aga This
attribute of females would have the same effect on
the growth of the otolith resulting in wider opaque
zones with more distinct hyaline rings than male
otoliths. Female scales would also have greater
growth but possibly because of scale resorption and
deterioration they were less easy to read than
otoliths.
Other investigators have mentioned the ease of in-
terpreting annuli of otoliths compared with scales,
but have remarked that otoliths are less convenient
to collect and store (Norden 1967; Kornegay 1978).
The method presented in this paper was found to
be more effective in obtaining both otoliths, un-
broken, than the commonly used transverse cut
made to the side of the head. The method of storage
eliminated transferring and handling individual
otoliths each time they were used. A disadvantage
in using otoliths was that the fish had to be sacri-
ficed. More care was required initially to obtain
otoliths than scales, but the technique was quickly
learned. The use of otoliths for aging alewives was
more accurate and less subjective than aging with
the use of scales.
Acknowledgments
I wish to thank Sherry Collins, Maine Department
Table 1.— Percent agreement (PA), average percent error (APE), and mean coefficient of varia-
tion (V) values for five treatment comparisons: a) scales and otoliths for R, against Rji b)
scales of R^ and Rj against otoliths of R, and Rg; c) scales of R, and Rg and true age against
otoliths R, and Rj and true age; d) scales of R, and Rg for males against scales of R, and
Rj for females; and e) otoliths of R, and Rj for males against otoliths of R, and Rg for
females. S = scales;
0 = otoliths;
1 = R,; 2 = R2;
A = true age.
Treatment cmparisons
a
b
c
d
e
S^O, S2O2
S1S2 O1O2
S^SgA OiOgA
S^S^cr S1S29
O1O2CT 0,029
PA 82.6 80.4
APE 1.9 2.3
V 2.7 3.2
85.0 89.0
1.8 1.1
2.5 1.6
78.8 87.7
2.1 1.2
2.8 1.5
84.0 85.8
1.9 1.6
2.7 2.3
86.5 92.2
1.5 0.8
2.1 1.2
700
of Marine Resources, for her help and expertise in
being a "reader"; Robert Guillard and James Rollins,
Bigelow Laboratory for Ocean Sciences, for photo-
graphic services; and Vicki Averill, Maine Depart-
ment of Marine Resources, for typing this
manuscript.
Literature Cited
Beamish, R. J., and D. A. Fournier.
1981. A method for comparing the precision of a set of age
determinations. Can. J. Fish. Aquat. Sci. 38:982-983.
Chang, W. Y. B.
1982. A statistical method for evaluating the reproducibility
of age determination. Can. J. Fish. Aquat. Sci. 39:1208-1210.
Cooper, R. A.
1961. Early life history and spawning migration of the alewife,
Alosa pseudoharengus. M.S. Thesis, Univ. Rhode Island,
Kingston, 58 p.
Havey, K. a.
1961. Restoration of anadromous alewives at Long Pond,
Maine Trans. Am. Fish. Soc 90:281-286.
KORNEGAY, J. W.
1978. Comparison of ageing methods for alewife and blueback
herring. North Carolina Dep. Nat. Resour. Community Dev.,
Div. Mar. Fish., Spec Sci. Rep. 30.
LiBBY, D. A.
1982. Decrease in length at predominant ages during a spawn-
ing migration of the alewife, Alosa pseudoharengiis. Fish.
Bull., U.S. 80:902-905.
Marcy, B. C, Jr.
1969. Age determinations from scales of Alosa pseudo-
harenffus (WUson) and ^Zosa aestivalis (Mitchill) in Connect-
icut waters. Trans. Am. Fish. Soa 98:622-630.
NORDEN, C. R.
1967. Age, growth and fecundity of the alewife, Alosa pseudo-
harengiis (Wilson), in Lake Michigan. Trans. Am. Fish. Soc
96:387-393.
Price, W. S.
1978. Otolith comparison of Alosa pseudoharengiis (Wilson)
and Alosa aestivalis (Mitchill). Can. J. Zool. 56:1216-1218.
Rothschild, B. J.
1963. A critique of the scale method for determining the age
of the alewife, Alosa pseudoharengus (Wilson). Trans. Am.
Fish. Soc. 92:409-413.
Watson, J. E.
1964. Determining the age of young herring from their
otoliths. Trans. Am. Fish. Soc 93:11-20.
Williams, T, and B. C. Bedford.
1974. The use of otoliths for age determinations. In T. B.
Bagenal (editor), The ageing of fish, p. 114-123. Unwin
Brothers Limited, Surrey, Engl.
David A. Libby
Maine Department of Marine Resources
Marine Resources Laboratory
West Boothhay Harbor, ME 0^575
PROBABLE CAUSES OF THE RAPID GROWTH
AND HIGH FECUNDITY OF WALLEYE,
STIZOSTEDION VITREUM VITREUM,
IN THE MID-COLUMBIA RIVER'
The introduction of walleye, Stizostedion vitreum
vitreum, into the Pacific Northwest of the United
States is not documented; however, they are now
found throughout the mid-Columbia River (Fig. 1)
and downstream of Bonneville Dam (Durbin^). The
construction of dams has transformed the Colum-
bia River from a free-flowing river into a series of
low water-velocity impoundments with physical
characteristics (Ikble 1) that closely match the model
for ideal walleye habitat proposed by Kitchell et al.
(1977a).
We studied basic life history factors of mid-
Columbia River walleye for 2 yr to determine how
well these exotic predators have adapted to their new
environment. We found that our walleye grew at a
rate approaching the highest previously reported,
that they were highly fecund, and that they matured
at an early age We evaluated these high growth and
reproductive rates against environmental and
genetic variables. We believe these data will help to
identify the ever increasing role of walleye in the
aquatic ecosystem of the Columbia River and similar
river-reservoir systems.
^Tfechnical paper no. 6723, Oregon Agricultural Experiment Sta-
tion, Oregon State University, Corvallis, OR 97331.
^Durbin, K. 1977. News column. Oregon Department of Fish
and Wildlife, P.O. Box 3503, Portland, OR 97208. Mimeogr., 3 p.
Pacific
Ocean
Figure 1.— Map of the lower and mid-Columbia River showing the
locations of the major dams and the John Day pool study area where
walleye were collected during 1980-81.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
701
Table 1. — Summary of limnological data for the John Day pool of
the Columbia River, from Hjort et al. (1981). All data collected in
August 1979 except for surface temperatures, which were taken in
1981.
Range for
Range for
Characteristic
John Day pool
study area
Water velocity (m/s)
0.1-1.4
0.5-1.4
SecchI depth (m)
1 .0-2.2
1.5-1.7
Dissolved O2 (ppm)
surface-bottom
16.0-8.0
14.0-10.0
Average surface temp.
Apr.-July-Sept. (max.)
7.0°-24.5°-
20.5°(24.8°)C
Temperature profile
surface-bottom
22.0''-20.8°C
21.0°-21.0°C
Pool width (km)
0.8-4.2
0.8-1.8
Mid-pool depth (m)
11-48
11-20
Pool length (km)
120
23
Methods
We collected walleye for this study in the first 23
km (tailrace) downstream of McNary Dam in the
John Day pool of the Columbia River at lat. 45°55'N
(Fig. 1). Walleye were collected from 2 April to 30
September 1980 and from 30 March to 30 Septem-
ber 1981. In 1980, we captured walleye with either
a 38.1 X 1.8 m sinking gill net with 3.81, 5.08, 6.35,
7.52, and 10.16 cm variable stretch mesh, or a
76.2 X 3.7 m monofilament floating gill net with
15.25 cm stretch mesh. All gill net sets were of a
maximum 2.5-h duration. In 1981 we used these
gill nets and a 6.15 m electroshock boat with a
3,500-W generator and front-mounted electrodes,
utilizing pulsed DC current of 1-4 A to capture
walleya Sampling was conducted in the day and
night.
We recorded the fork length (FL, mm), weight (g),
sex and whether or not the fish were sexually mature
(Eschmeyer 1950), and removed a scale sample from
beneath the tip of the left pectoral fin of each wall-
eya Many authors report difficulty using scales to
determine the age of older walleye (Carlander
and Whitney 1961; Campbell and Babaluk
1979); therefore, we took a subsample of sagitta
{n = 86), which we preserved in 50:50 glycerine and
water.
We mounted scales between two glass microscope
slides and viewed them using a microfiche projec-
tor at 43x. We identified annuli using the criteria
described by Carlander and Whitney (1961). We
found that the easiest way to detect annuli on sagit-
tae was to burn the whole otolith in a flame, immerse
it in oil or alcohol, and examine it under a dissect-
ing microscopa Reburning was often necessary un-
til very distinct, dark annuli appeared. Christensen
(1964) proposed a similar technique; however, he
broke the burned otolith and examined the cross sec-
tion. There was 92% agreement between at least one
otolith reading and one scale reading so we ter-
minated the collection of otoliths. We examined
scales and otoliths twice and a person experienced
in reading walleye scales (W. R. Nelson, U.S. Fish
and Wildlife Service, Vancouver, WA) examined a
subsample of scales (n = 63).
Age determinations for walleye collected in 1980
were based on either two scale readings, three scale
readings, two scale readings and two otolith
readings, or three scale readings and two otolith
readings. All age determinations of walleye collected
in 1981 were based on two scale readings. There was
90% agreement between at least two of the five
possible age determinations for walleye collected in
1980, and 75% agreement between the two age
determinations for walleye collected in 1981. After
the final age determination, we measured the scale
radius and scale length to each annulus (43 x) at
about 45° off of a straight line from the focus
through the anterior field. In this area of the scale
it was much easier to detect the annuli because of
crowding and anastomosis of circuli in the lateral
fields.
We back-calculated length at each annulus
(i.e, year of life) assuming a straight line body-
scale relationship (r^ = 0.69) and using the
Fraser-Lee method as recommended by Carlander
(1982):
L, = a -t- i,-
where L^ = fish fork length at capture
Lj = calculated fork length at age i
S(. = scale radius at capture
Si = scale measurement at annulus i
a = intercept of body-scale regression = 55
mm.
We converted these back-calculated fork lengths to
total lengths (TL) using a conversion factor of 1.06
FL, which is the unweighted mean of the TL/FL
relationships reported by Colby et al. (1979). This
conversion allowed us to more easily compare our
data with data from other areas.
During the spring 1981 spawning season, we
removed the ovaries from 27 mature, but unspawn-
ed walleye We preserved the ovaries in Bouin's solu-
tion and subsequently estimated the number of eggs
by means of the gravimetric method recommended
by Wolfert (1969). We performed regressions of life
702
history characteristics by use of an interactive
statistical computer program.
Results
We sampled over 250 walleye in each year, and they
varied in length from 208 to 765 mm FL (220-810
mm TL) (Fig. 2). The weight (WT)/length (FL) rela-
tionship for 324 walleye was best described by the
equation:
Loge WT = -11.426 + 3.010 Loge FL (r^ = 0.966).
The slopes and intercepts of similar weight-length
regressions for walleye collected in 1980 versus 1981
and males versus females were not significantly dif-
ferent (F = 4.61; a = 0.01; df = 2; 247).
We had no difficulty detecting annuli in the scale
samples from older walleye because of their rapid
growth and apparently short life span (Ikble 2).
Although females are larger than males in each year
A majority of males and females were mature by age
III (Fig. 3); however, the maturity at fork length data
show a more gradual increase than do the maturity
BO
70
60
S 50
E
Z 40
30
20
10
S
D
CD 1980 (n=268)
E3 1981 (n^266)
Ml
i=E3
225 275 325 375 425 475 525 575 625 675 725 775
Fork Length (Midpoint of SO mm Increments)
Figure 2.— Length-frequency distribution of walleye collected from
the John Day pool of the Columbia River, April-September 1980-81.
Table 2. — Average back-calculated fork length (FL), SE, and annual growth incre-
ment tor walleye collected in the John Day pool of the Columbia River, April-
September 1980-81.
Age
1
II
MM
IV1
V1
VM
VIM
VIII
Males
FL (mm)
241
363
434
484
533
562
596
SE
2
3
6
7
9
10
7
N (cumulative)
134
86
35
25
21
18
8
increment (mm)
241
122
71
50
49
29
34
Females
FL (mm)
243
371
466
527
590
643
684
701
SE
2
3
4
4
5
5
6
11
N (cumulative)
197
150
122
95
69
57
23
8
increment (mm)
243
128
95
61
62
54
41
17
Combined^
FL (mm)
244
368
458
515
575
623
664
701
SE
2
2
3
4
4
5
8
11
N (cumulative)
446
277
189
142
104
85
40
8
increment (mm)
244
124
90
57
60
8
41
37
'Females versus males significantly different, P < 0.01, Student's f-test.
^Includes some fisti whose sex was not determined.
of life, the difference is not statistically significant
until after the second year.
The mean fecundity of 27 walleye, between 520 to
764 mm FL and 1,720 to 5,905 g weight, was 82,900
eggs/kg body weight (Tkble 3). We found fecundity
(FEC) linearly related to fish weight (WT):
FEC = -28,100 + 93.8 WT, r^ = 0.969
and curvilinearly related to fork length (FL):
Loge FEC = -8.4 + 3.2 Loge FL, r^ = 0.905.
Table 3.— Fecundity of walleye from the John Day pool of the Col-
umbia River, 30 March to 18 April 1981, compared with fecundities
from Norris Reservoir, TN (Smith 1941), Lake Gogebic, Ml
(Eschmeyer 1950), and western Lake Erie (Wolfert 1969).
Eggs/kg body weight^
Location
N
Range!
Mean'
John Day pool
27
69,000-101,000
82,900 -1- 1,550
(1SE)
Norris Reservoir
28,400-32,700
29,700
Lake Gogebic
34
57,900-67,800
61 ,800
Western Lake Erie
78
56,300-123,200
82,500
Walues converted from eggs/pounds body weigtit and rounded to nearest
100 eggs, except John Day pool.
703
data by age and, inexplicably, males were not 100%
mature at any length (Fig. 3).
Discussion
The transplanted walleye population of the John
Day pool of the Columbia River grows at a rate ap-
proaching the highest previously reported (Fig. 4).
Concomitant with rapid growth these walleye are
very fecund (Ikble 3) and mature at an early age
(Fig. 3). We suggest that these life history charac-
teristics result from the combination of a favorable
temperature regimen and a nonlimiting food supply.
High growth rates are generally found in walleye
populations of more southerly latitudes where higher
temperatures and longer growing seasons occur.
Figure 4 contains data from Norris Reservoir, TN
(Stroud 1949), Lake Gogebic, MI (Eschmeyer 1950),
Lac la Ronge, Saskatchewan (Rawson 1957); as well
as the composite high and low length-at-age values
reported by Colby et al. (1979). Relative to the
latitude of the John Day pool (lat. 45°55'N), Norris
Reservoir is south (lat. 36°15'N), Lac la Ronge is
north (lat. 55°07'N), and Lake Gogebic is at approx-
imately the same latitude (lat. 46°47'N). The mean
growing degree-days (GDD) above 5°C (GDD >5°C)
100
80
. (1). 'Vi
- (14^ V,
(1)
(18)
•
(11L_
,^* '(lO)
'•(5)
60
40
20
. .•(54)
-'•(36)
c
cr
(3)'^5E^
y,(22)
>^46)
,(17)
100
80
60
<24)^
. X^) •
9
(19)(29)
(13)
(23)
9
(5) (30)
(14) ''^<'"""23)
^l"'* y^*(36)
40
- /
20
^^/,(36)
1 1 1 t . . 1
(15)''?i-»^.(27)
(5)1 .--• (38) •
1 2 3 4 5 6 7 8 0 ^^»?3t?»'^«^..<?3>3U'?D'5>-j
Age
Fork Length (Midpoint o( 50mm increments)
Figure 3.— Percent mature walleye by age and length and by sex for
specimens collected in the John Day pool of the Columbia River, April-
September 1980-81. Curves were drawn by eye (Sample size in
parentheses.)
800
700
-g 600
E
£ 500
c
«
-J 400
a
t- 300
200
100
-
0,(2730)
.
o ^
^S/-" o »
O
o
(1178)7 o
-o —
o
^°^
^(3900)
-
oX
.y /°^
..o-'
O
o
-O
ft^
A-^-— ^"^
"^
o-;:::^(i9oi)
o
- \/
D*^
^8^
O
// -
::o^°'^
o
—
o
o
0-John Day Pool
o
A-Norrls Reservlor
n-Lake Gogebic
o-Lac la Ronge
. ° o
O-Hlghest Values Reported
o
OLowest Values Reported
6 7 8
Age (Years)
10
11
12 13
Figure 4.— Comparison of length-at-age for walleye from the John Day
pool, Columbia River; Norris Reservoir, Tfennessee (Stroud 1949); Lake
Gogebic, Michigan (Eschmeyer 1950); Lac la Ronge, Saskatchewan
(Rawson 1957) and the composite high and low values reported by Colby
et al. (1979). Numbers in parentheses are the mean growing degree-days
above 5°C, John Day value is from Anonymous (1969), all others are from
Colby and Nepszy (1981).
704
(Colby and Nepszy 1981) for each area are included
in Figure 4 as a measure of solar energy input to
the system. Colby and Nepszy (1981) found that
walleye growth was directly correlated to ODD >5°C
and that the optimum range was from 2,500 to 4,000
GDD >5°C. While the GDD >5°C for the John Day
pool is within this range, the walleye growth reported
here is greater than would be predicted using this
variable
Water temperature may be the most important
factor governing the growth of fishes (Brett 1979).
Kitchell et al. (1977b) presented a bioenergetics
model for walleye growth and indicated that ther-
mal optima and maxima for weight specific con-
sumption are 22°C and 27°C, respectively and 27°C
and 32 °C, respectively, for weight specific respira-
tion. Water temperatures in the John Day pool
during the growing season remain at or near the
thermal optimum for consumption and, perhaps
more importantly, do not approach the thermal max-
ima for consumption or respiration (Tkble 1). Many
northern lakes may not reach the thermal optima
(Rawson 1957; Swenson 1977) and the southern lakes
or lakes which stratify in the summer may exceed
the thermal maxima (MacLean and Magnuson 1977)
not only reducing consumption but increasing
respiration. Dendy (1948) reported that in June 1944
the surface temperature of Norris Reservoir was
about 30 °C and that walleye appeared to prefer
water temperature of about 24 °C, even though these
areas had oxygen concentrations <3.0 mg/L. Con-
versely, water temperature of Lac la Ronge did not
exceed 20°C (Rawson 1957), well below the thermal
optima.
Exceptions to the north-south trend in high wall-
eye growth occur in systems of high exploitation
(Forney 1965) and/or where there have been
decreases in interspecific competition (Wolfert 1969;
Forney 1977) which results in density dependent in-
creases in growth rates. The quantity and quality of
food are important factors in walleye growth (Kelso
1972; Kerr and Ryder 1977; Kitchell et al. 1977b)
and fecundity (Colby and Nepszy 1981). Schupp
(1978) looked at the growth of walleye from several
areas within Leech Lake, MN, and found food of
walleye from areas of highest average growth was
almost totally young-of-the-year yellow perch,
whereas small walleyes from slow growth areas had
eaten mostly invertebrates and small minnows. We
have found (Maule and Horton 1984) that about 99%
by volume of Columbia River walleye stomach con-
tents were fish (ag., sculpins, suckers, cyprinids) and
that 61% of walleye sampled contained food.
Eschmeyer (1950) reported that 89% of the volume
of stomach contents from Lake Gogebic walleye was
fish, but he did not report percent empty stomachs.
Dendy (1946) reported that Norris Reservoir wall-
eye stomachs contained 99% fish by volume, but only
45% of the walleye examined contained food. Rawson
(1957) studied Lac la Ronge walleye and reported
that fish comprised 97% of the volume of stomach
contents and that 39% of the walleye stomachs con-
tained food.
Colby and Nepszy (1981) stated that age to matu-
rity is indirectly correlated to growth, but that fecun-
dity is probably a function of population density and
food availability. They further suggested that the
wide variability in walleye fecundities is a mechanism
by which walleye can adjust production in response
to environmental conditions. Ikble 3 includes fecun-
dity data from Norris Reservoir (Smith 1941), Lake
Gogebic (Eschmeyer 1950), and western Lake Erie
(Wolfert 1969). Based on a comparison of growth,
stomach content analysis, and fecundity the
mid-Columbia River walleye have a more favor-
able food supply than the other areas considered
hera
Hackney and Holbrook (1978) suggested that there
is a southern race of walleye that is characterized
by rapid, large growth and short life span, and a
northern race characterized by slow growth and long
life span. They suggested that the pattern of rapid
walleye growth seen after the impoundment of
southern waters, followed by decreased growth rates
some years later is due to a shift from the southern
race to the northern race as the result of walleye
stocking programs. The movements of young-of-the-
year walleye downstream past Columbia River dams
has been documented (Brege 1981). Assuming that
this is a means by which walleye have colonized the
Columbia River, it is biologically similar to impound-
ing waters already containing walleye populations,
in that new habitat is available for population growth.
Although we cannot discount the possibility that the
extreme life history characteristics reported here are
the result of genetic stock differences, we suggest
that they can more reasonably be explained by a
favorable temperature regimen and an abundant,
high quality food supply.
Acknowledgments
We thank Hiram Li and Carl Bond for their
reviews of the manuscript. Funding was provided by
the U.S. Army Corps of Engineers contract DACW
57-79-C-0067, the Oregon Agricultural Experiment
Station, and the Milne Computer Center, Oregon
State University, Corvallis, OR.
705
Literature Cited
Anonymous.
1969. Climatological handbook. Columbia Basin states. Ttem-
perature Volume 1, part A. Meteorology Committee, Pacific
Northwest River Basins Commission, Vancouver, WA, 268 p.
Brege, D. A.
1981. Growth characteristics of young-of-the-year walleye,
Stizostedion vitreum vitreum, in John Day Reservoir on the
Columbia River, 1979. Fish. Bull., U.S. 79:567-569.
Brett, J. R.
1979. Environmental factors and growth. In W. G. Hoar, D.
J. Randall, and J. R. Brett (editors), Fish physiology. Volume
VIII. Bioenergetics and growth, p. 599-676. Acad. Press,
N.Y.
Campbell, J. S., and J. A. Babaluk.
1979. Age determination of walleye, Stizostedion vitreum
vitreum, (Mitchill), based on the examination of eight dif-
ferent structures. Can. Fish. Mar Serv., Ttech. Rep. 849, 23 p.
Carlander, K. D.
1982. Standard intercepts for calculating lengths from scale
measurements for some centrarchid and percid fishes.
Trans. Am. Fish. Soa 111:332-336.
Carlander, K. D., and R. R. Whitney.
1961. Age and growth of walleyes in Clear Lake, Iowa, 1935-
1957. Trans. Am. Fish. Soa 90:130-138.
Christensen, J. M.
1964. Burning of otoliths, a technique for age determination
of soles and other fish. J. Int. Counc. Explor. Sea 29:73-81.
Colby, P. J., R. E. McNicol, and R. A. Ryder.
1979. Synopsis of biological data on the walleye, Stizostedion
vitreum vitreum (Mitchill 1818). FAO Fish. Synop. 119, 139
P-
Colby, P. J., and S. J. Nepszy.
1981. Variation among stocks of walleye (Stizostedion vitreum
vitreum): management implications. Can. J. Fish. Aquatic
Sci. 38:1814-1831.
Dendy, J. S.
1946. Food of several species of fish, Norris Reservoir, Tfen-
nessee J. Ifenn. Acad. Sci. 21(1):105-127.
1948. Predicting depth distribution of fish in three TVA
storage-type reservoirs. Trans. Am. Fish. Soc 75:65-71.
ESCHMEYER, P. H.
1950. The life history of the walleye, (Stizostedion vitreum^
vitreum (Mitchill)), in Michigan. Mich. Dep. Conserv., Bull.
Inst. Fish. Sci. 3.
Forney, J. L.
1965. Factors affecting growth and maturity in a walleye
population. N.Y. Fish Game J. 12:217-232.
1977. Evidence of inter- and intraspecific competition as fac-
tors regulating walleye (Stizostedion vitreum vitreum)
biomass in Oneida Lake^ New York. J. Fish. Res. Board Can.
34:1812-1820.
Hackney, P. A., and J. A. Holbrook II.
1978. Sauger, walleye, and yellow perch in the southwestern
United States. In R. L. Kendall (editor). Selected coolwater
fishes of North America, p. 74-81. Am. Fish. Soc Spec Publ.
11.
Hjort, R. C, B. C. Mundy, and P. L. Hulett.
1981. Habitat requirements for resident fishes in the reser-
voirs of the lower Columbia River Final report. U.S. Army
Corps Eng. Contract No. DACW57-79-C-0067. Portland,
OR.
Kelso, J. R. M.
1972. Conversion, maintenance and assimilation for walleye,
Stizostedion vitreum vitreum, as affected by size, diet and
temperature J. Fish Res. Board Can. 29:1181-1192.
Kerr, S. R., and R. A. Ryder.
1977. Niche theory and percid community structure J. Fish.
Res. Board Can. 34:1952-1958.
KiTCHELL, J. F, M. G. Johnson, C. K. Minns, K. H. Loftus, L. G.
Greig, and C. H. Olver.
1977a. Percid habitat: The river analogy. J. Fish. Res.
Board Can. 34:1936-1940.
KiTCHELL, J. F., D. J. Stewart, and D. Weininger.
1977b. Applications of bioenergetics model to yellow perch
(Percajlavescens) and walleye (Stizostedion vitreum vitreum).
J. Fish. Res. Board Can. 34:1922-1935.
MacLean, J., and J. J. Magnuson.
1977. Species interactions in percid communitltes. J. Fish.
Res. Board Can. 34:1941-1951.
Maule, a. G., and H. F. Horton.
1984. Feeding ecology of walleye, (Stizostedion vitreum
vitreum) in the mid-Columbia River, with emphasis on the
interactions between walleye and juvenile anadromous fishes.
Fish. Bull., U.S. 82:411-418.
Rawson, D. S.
1957. The life history and feeding ecology of the yellow wall-
eye, Stizostedion vitreum, in Lac la Ronge; Saskatchewan.
Trans. Am. Fish. Soc 86:15-37.
ScHUPP, D. H.
1978. Walleye abundance, growth, movement, and yield in
disparate environments within a Minnesota Lake In R. L.
Kendall (editor), Selected coolwater fishes of North America,
p. 58-65. Am. Fish. Soc Spec Publ. 11.
Smith, C. G.
1941. Egg production of walleyed pike and sauger Norris
Reservoir fish differ from same species in other
localities. Prog. Fish-Cult. 54:32-34.
Stroud, R. H.
1949. Growth of Norris Reservoir walleye during the first
twelve years of impoundment. J. Wildl. Manage 13:157-177.
Swenson, W. a.
1977. Food consumption of walleye (Stizostedion vitreum
vitreum) and sauger (S. canadense) in relation to food
availability and physical conditions in Lake of the Woods,
Minnesota, Shagawa Lake, and western Lake Superior J.
Fish. Res. Board Can. 34:1643-1654.
WOLFERT, D. R.
1969. Maturity and fecundity of walleyes from the eastern and
western basins of Lake Erie J. Fish. Res. Board Can. 26:
1877-1888.
Alec G. Maule
Oregon Cooperative Fisheries Research Unit
Department of Fisheries and Wildlife
Oregon State University
Corvallis, OR 97331
Howard F. Horton
Department of Fisheries and Wildlife
Oregon State University
Corvallis, OR 97331
706
BIOLOGICAL ASPECTS OF
THE SPRING BREEDING MIGRATION OF
SNOW CRABS, CHIONOECETES OPILIO, IN
BONNE BAY, NEWFOUNDLAND (CANADA)
The occurrence of an annual (April-May) deep- to
shallow-water breeding migration of snow crabs,
Chionoecetes opilio, in Bonne Bay, on the west coast
of Newfoundland, has been documented by Hooper
(in press). In addition to being the first record of this
phenomenon in this species, his observations con-
tradict some generally accepted conclusions regard-
ing the species' reproductive biology. The most
significant of these are that females undergo a ter-
minal molt to maturity and do not mate in the hard
shell condition (Ito 1967; Watson 1972; Tkkeshita and
Matsuura 1980).
Little morphometric sampling data are included
in Hooper's general description of the breeding
migration. The purpose of this paper is to provide
a more detailed description of various biological
aspects of the phenomenon, such as size difference
between paired males and females, and condition of
the external egg masses, ovaries, and spermathecae
during the breeding period.
Materials and Methods
Three hundred and three sexually paired snow
crabs were collected during three field trips to Bonne
Bay from 24 April to 29 May 1984 by scuba diving
(10-30 m depth). Each pair was kept in a separate
mesh bag. At the surface, each crab was measured
to the nearest millimeter (maximum carapace width
(CW)) and its shell condition (soft, new/hard, or
old/hard) determined. The eggs of females were ex-
amined to determine their stage of development.
Following this, males were tagged with Floy vinyl
"T-bar" tags (Tkylor 1982) and released, and females
were either tagged and released, or retained for later
examination of their ovaries and spermathecae in the
laboratory.
Results
Size Distribution
Size distributions were unimodal for each sex but
with no overlap in their carapace widths (Fig. 1).
Males ranged from 89 to 140 mm (x = 116.4 mm)
CW and females from 55 to 86 mm (x = 67.8 mm).
Other than the fact that males were invariably larger
than females, there was no discernible relationship
between size of the male and size of the female with
which it was paired (Fig. 2). Mean sizes of females
paired with small, medium, and large size males were
the same (P < 0.005, Bartlett's test of homogeneity
of variance).
Male CW (mm)
Female CW (mm)
Range
Range
Mean
N
89-109 (small)
55-86
69.2
59
110-120 (medium)
59-86
69.6
136
121-120 (large)
59-84
70.9
108
Ibtal 303
The mean difference in carapace width between
paired males and females increased from 21 mm at
89 mm male CW to 70 mm at 140 mm. Only 3 males
in 303 pairs were smaller than 95 mm, the legal size
limit.
Female Reproductive Condition
During the 24-27 April sampling period, 92% of
the females carried full clutches of eyed eggs and
the remainder had liberated all or most of the lar-
vae (Table 1). By 7-11 May, 59% had empty brood
pouches indicating that hatching was well advanced.
However, during 22-25 May, 53% of the females
were carrying full clutches of eyed eggs and only
39% had empty brood pouches. This increase in
relative abundance of females with eyed eggs could
have resulted from a return to deeper water of
females that had liberated larvae or an influx of new
animals from deeper water. Dead eggs were carried
by 1.4% of females examined. All females dissected
(77) had ripe (extrusion imminent) ovaries (Table 2);
however, only two with partially extruded clutches
Table 1. — Summary of observations on external
egg masses of female Chionoecetes opilio col-
lected in Bonne Bay, Newfoundland, April-May
1984.
Sampling
period
Larvae Larvae
Eyed liberating liberated
(%) (%) (%) N
24-27 April
7-11 May
22-25 May
92 0 8 128
9 32 59 81
53 8 39 87
Table 2.— Summary
cefes opilio collected i
of internal observations on female Chionoe-
n Bonne Bay, Newfoundland, April-May 1984.
Ripe
Sampling ovaries
period (%)
Spermatophores (%)
Old only Old and new New only N
24-27 April 100
22-25 May 100
45.7 48.6 5.7 35
7.1 92.9 0 42
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
707
55-59 65-69 75-79 85-89 95-99 105-109 115-119 125-129 135-139
60-64 70-74 80-84 90-94 100-104 110-114 120-124 130-134 140-144
CARAPACE WIDTH (5 mm GROUPS)
Figure 1.— Size-frequency distributions of male and female Chionoecetes opilio collected as pairs in
Bonne Bay, Newfoundland, during April-May 1984.
of new eggs were found over the entire sampling
period.
Females were observed with spermathecae con-
taining both old and new spermatophores. In these,
spermathecae were engorged with a very white
glutinous material containing new spermatophores
for three-fourths of their length, while the remain-
ing one-fourth at the dorsal end of the organ was
shrunken and contained a yellowish brown
substance of a "waxy" consistency. Females which
did not have new spermatophores had very small
spermathecae which were entirely yellowish brown
in color. This is very similar to that described for
Chionoecetes bairdi by Paul (1982). While 97% of all
females examined contained old spermatophores,
those containing new spermatophores as well in-
creased to 92.9% from 48.6% between 24 April and
25 May (Table 2). Two specimens contained new
spermatophores only and all had old epizooite-
encrusted shells. Thirty-six percent of the females
with new spermatophores carried full clutches of
eyed eggs.
Diving during 28-31 May revealed that all crabs
had left the sampling area.
Discussion
Small numbers of grasping, male/female pairs of
C. opilio and C. bairdi have been observed in shallow
water elsewhere. Ennis (Unpubl. data) found five
pairs and Hooper (Unpubl. data) found three pairs
of C. opilio in Bonavista Bay and Placentia Bay,
Newfoundland, respectively. Donaldson (1975)
reported two pairs of C. bairdi in Alaska. However,
nothing comparable with the magnitude of the
breeding migration of C. opilio, observed in Bonne
Bay, Newfoundland, has been reported for other
areas. There is considerable scope for speculation
on the ecological significance of this migration.
Although about half the females examined just prior
708
to their departure from the shallow (<35 m) sam-
pling depths in 1984 still had full clutches of eyed
eggs, liberation of a large proportion of larvae in
shallow water may enhance chances for larval sur-
vival overall. At the time of the migration, bottom
temperatures in Bonne Bay at depths beyond 35 m
are probably 0°C or lower [deep water temperatures
are not available for Bonne Bay but Squires et al.
(1971) reported temperatures <0°C at depths
beyond 30 m in early June in North Arm, Bay of
Islands, about 40 km to the south]. Release of lar-
vae in shallow, warmer water (temperature was 3°C
at 30 m during 7-11 May) would considerably reduce
the degree of thermal shock associated with larvae
swimming to the surface. The rate of embryonic
development would likely be increased also, result-
ing in earlier larval release.
In the development of a management strategy for
C. opilio stocks on the Atlantic coast of Canada, a
key assumption has been that, despite high levels
of exploitation, reproductive potential in a stock re-
mains at prefishery levels. The basis for the assump-
tion is that females are protected from exploitation
by the 95 mm CW minimum legal size because they
do not grow to that size and also that males mature
at sizes much smaller than 95 mm CW. In a recent
review, following more than 15 yr of heavy fishing
in some areas, there was no evidence to indicate that
the assumption was invalid (Elner and Robichaud
1983). However, the observations presented here
suggest that a large size differential between the
male and female of a pair is an important element
of behavioral interactions during breeding activity.
It is possible that males smaller than 89 mm CW
(the smallest male observed paired with a female),
even though physiologically mature, may be less like-
ly to mate successfully in competition with large
males.
Males and females appear to be segregated over
most of the year (Hooper in press). Observations on
the east coast of Newfoundland indicate that large
males occur mainly on muddy bottom in deep water
whereas females and small males occur on sand-
gravel or rocky bottom somewhat shallower (Miller
and O'Keefe 1981). In the breeding migration which
occurs in Bonne Bay, Hooper (in press) suggested
that males leave the deeper water area after select-
ing a mature female which is carried to the shallow
water breeding area. Males retain possession of in-
dividual females for extended periods (Hooper in
86
84
82
80
1 78
=: 76
t—
o
» 74
2 72
4
CC
S 70
UJ
^ 68
UJ
u.
66
64
62
60
58
_l ' 1 ' 1 ' 1
. 1 1 1 1
1 ' 1
' 1
•
■Ml
' 1
' 1 '
1 '
•
I ' 1 ' 1 '
•
1 ' 1 ' 1 '
1 < 1
MM
' l_
'_ Y = 00919
X +59-3021
^
J
- R^= 0018?
- N ■- 303
•
•
•
•
•
•
•
• •
•
•
•
•
• •
• •
-
-
.2
•
. •
•
-
—
• •
•
—
-
•
•
.2 .
•
•
-
—
•
•
•
.2.
-
-
•
•
.2
. .
-
—
•
•
•
. . .
.
-
- • • •
•
.2.
•
•
.2
• •
• •
• •
.3 Ji.
•
•
. .2.
.2.3
•
•
.2.
... .2
... .2
j2j_j2_j3_j__^
• . . .4 . .
. .2
.2
. . .2
•
•
■
•—
- • •
• -
•
• •
• •
•
•
•2
•
.2.
—72 T
^^. .
.2
. . .2.
.2
.2
•
• • •
•
• • •
.2
.2.
• •
.2
•
.3 .2 .2
• •3 •& • •
.3.
.3. .
.2
• • •
•
•
•
-
•
•
•
.2 .
•
.2
.2
•
•
•
.3 .2 .2
.2
—
— •
•
•
•
•
•
—
-
•
•
•
•
...
-
" 1 , 1 , 1 , 1
1 1 1 1 1
1 I 1
, 1
•
ill!
•
•
1 1
•
1 1 1
1 ,
•
.2
1 1 1 1 1 1
1 1 1 1 1 .
1 . 1
1 1 .
, 1 '
92 94 96 98 100 102 104 106 108 110 112 114 116 118 120 122 124 126 128 130 132 134 136 138 140
MALE CARAPACE WIDTH (mm)
Figure 2— Recession of female carapace width on male carapace width for pairs of Chionoecetes opilio collected in Bonne Bay, New-
foundland, during April-May 1984. Numbers adjacent to points indicate more than one observation. Slope of the regression is not signifi-
cant (P = 0.017).
709
press) (possibly up to 2 mo) during which time the
female is held by and dependent on the male. In
laboratory studies on C. bairdi, Paul and Adams
(1984) demonstrated that muciparous females are
receptive to mating for periods ranging from <1 to
7 d after all their eggs have hatched. In fact, they
reported that only one ovigerous female mated suc-
cessfully during their study.
In the Gulf of St. Lawrence, male snow crabs
mature within the 50-65 mm CW size range (Powles
1968; Watson 1970); however, in the sampling
reported here, only 3 males from the 303 pairs ex-
amined were smaller than the 95 mm CW minimum
legal size, the smallest being 89 mm. Except for
these, even solitary males of this size and smaller
were absent from the area indicating that competi-
tion for females had occurred in deeper water. This
snow crab population appears to be small and is
isolated from populations elsewhere in the Gulf of
St Lawrence by the 35 m deep sill at the mouth of
Bonne Bay. This area has not been fished commer-
cially and at present the population is considered to
be in the virgin state. Hooper's (in press) observa-
tions indicated there is keen competition between
single males and males already paired with a female
for possession of the female. Under prefishery con-
ditions this competition can be expected to eliminate
small males from participating in breeding activi-
ty. Adams (1982) demonstrated that muciparous
female C. bairdi resisted mating attempts by small
males, and when males of significantly different
sizes competed for the same female, the larger male
was invariably successful. Small numbers of the
largest of the sublegal (<95 mm CW) male C. opilio
appear to be capable of competing and mating suc-
cessfully. However, it is presently unknown whether
males smaller than those observed are capable of
successful mating with multiparous females in the
absence of competition from large males and, if they
are not, whether there are sufficient numbers of
large sublegal males to maintain full reproductive
potential in a heavily fished population.
Acknowledgments
We are indebted to P. O'Keefe, G. Badcock, and
D. Keats for assistance with field work, particular-
ly diving, and to P. Collins, as well as P. O'Keefe
and H. Mullett for assistance with data analysis and
drafting.
Literature Cited
Adams, A. E.
1982. The mating behavior of Chionoecetes bairdi. In B.
Melteff (editor), Proceedings of the International Symposium
on the genus Chionoecetes. Lowell Wakefield Fisheries Sym-
posia Series, p. 273-281. Univ. Alaska, Fairbanks, Sea Grant
Rep. 82-10.
Donaldson, W. E.
1975. Kodiak Tanner Crab Research. Technical Report for
period July 1, 1974 to June 30, 1975. NOAA, NMFS, 69 p.
Elner, R. W., and D. a. Robichaud.
1983. Observations on the efficacy of the minimum legal size
for Atlantic snow crab, Chionoecetes opilio. CAFSAC Res.
Doc. 83/63, 26 p.
Hooper, R. G.
In press. A spring breeding migration of the snow crab
(Chionoecetes opilio) into shallow water in Newfoundland.
Crustaceana.
ITO, K.
1967. Ecological studies on the edible crab, Chionoecetes
opilio 0. Fabricius in the Japan Sea. I. When do female crabs
first spawn and how do they advance into the following
reproductive stage? Bull. Jpn. Sea Reg. Fish Res. Lab.
17:67-84. [Engl, transl. from Jpn. by Fish Res. Board Can.
Trans. Ser. No. 1103.]
Miller, R. J., and P. G. O'Keefe.
1981. Seasonal and depth distribution, size, and molt cycle
of the spider crabs, Chionoecetes opilio, Hyas araneus and
Hyas coarctatus in a Newfoundland bay. Can. Tech. Rep.
Fish. Aquat. Sci. 1003, 18 p.
Paul. A. J.
1982. Mating frequency and sperm storage as factors affect-
ing egg production in multiparous Chionoecetes bairdi. In
B. Melteff (editor). Proceedings of the International Sym-
posium on the genus Chionoecetes. Lowell Wakefield Fish-
eries Symposia Series, p. 273-281. Univ. Alaska, Fairbanks,
Sea Grant Rep. 82-10.
Paul, A. J., and A. E. Adams.
1984. Breeding and fertile period for female Chionoecetes
bairdi (Decapoda, Majidae). J. Crustacean Biol. 4:589-594.
Powles, H. W.
1968. Distribution and biology of the spider crab Chionoecetes
opilio in the Magdalen Shallows, Gulf of St. Lawrence.
Fish. Res. Board Can. MS Rep. 997, 106 p.
Squires, H. J., G. E. Tucker, and G. P. Ennis.
1971. Lobsters (Homarus americanus) in Bay of Islands,
Newfoundland, 1963-65. Manuscr. Rep. Ser. (Biol.) No.
1151, 58 p.
Taylor, D. M.
1 982. A recent development in tagging studies on snow crab,
Chionoecetes opilio in Newfoundland - Retention of tags
through ecdysis. In B. Melteff (editor). Proceedings of the
International Symposium on the genus Chionoecetes. Lowell
Wakefield Fisheries Symposia Series, p. 405-417. Univ.
Alaska, Fairbanks, Sea Grant Rep. 82-10.
Takeshita, K., and S. Matsuura.
1980. Mating and egg-laying in Tanner crabs. Bull. Far Seas
Fish. Res. Lab.
Watson, J.
1970. Maturity, mating and egg-laying in the spider crab,
Chionoecetes opilio. J. Fish. Res. Board Can. 27:1607-
1616.
1972. Mating behavior in the spider crab, Chionoecetes opilio,
J. Fish. Res. Board Can. 29:447-449.
D. M. Taylor
Fisheries Research Branch
Department of Fisheries and Oceans
710
P.O. Box 5667
St. John's, Newfoundland AlC 5X1, Canada
NICOS/Biology Department
Memorial University of Newfoundland
St. John's, Newfoundland A IB 3X9, Canada
Fisheries Research Branch
Department of Fisheries and Oceans
P.O. Box 5667
St. John's, Newfoundland, AlC 5X1, Canada
R. G. Hooper
G. P. Ennis
FEEDING, DIET, AND REPEAT SPAWNING
OF BLUEBACK HERRING, ALOSA
AESTIVALIS, FROM THE CHOWAN RIVER,
NORTH CAROLINA
Current knowledge of the frequency of feeding
among spawning blueback herring, Alosa aestivalis
Mitchill, is limited. Other aspects of the blueback
herring's life history have been more extensively
studied: feeding of juveniles (Davis and Cheek 1966;
Nichols 1966; Burbidge 1974; Domermuth and Reed
1980; Crecco and Blake 1983), distribution at sea
(Hildebrand 1963; Holland and Yelverton 1973^;
Neves 1981), and spawning range (Bigelow and
Schroeder 1953; Hildebrand 1963; Scott and Cross-
man 1973). However, determination of the occur-
rence of feeding by adults in freshwater has received
little attention despite the fact that spawning
bluebacks are common in rivers from southern New
England (Bigelow and Schroeder 1953) to the St.
Johns River, FL (Hildebrand 1963). Throughout this
extensive range only Frankensteen (1976) has
studied feeding among adult bluebacks in fresh-
water. Furthermore, no attempt has been made to
correlate feeding with length, weight, and sex of in-
dividual fish, distance upstream, or the number of
seasons a blueback has spawned.
The objective of this study is to enhance our
knowledge of the freshwater feeding of blueback
herring. In this paper I describe the occurrence of
feeding, diet, and percentage of repeat spawning
among adults collected in the Chowan River, NC. I
also examined, by multiple regression analysis, the
relation between feeding activity in freshwater and
length, weight, sex, the number of repeat spawnings,
and the distance travelled upstream.
Materials and Methods
Collection of Data
Bluebacks were collected at two sites in the lower
Chowan River system during April 1980 and 1981.
Williams' Fishery, where five collections were made
in 1980, is located on the lower Meherrin River near
its junction with the Chowan River, 90 km upstream
from the Chowan River's mouth. Rocky Hock Creek,
where bluebacks were sampled twice in 1980 and
once in 1981, is roughly 20 km from the mouth of
the Chowan River. Bluebacks at Williams' Fishery
were still migrating upstream while those at Rocky
Hock Creek, a known spawning ground,^ were
preparing to spawn.
Bluebacks were caught in chicken-wire dip nets
and fixed gill nets with 58 mm stretched mesh at
Rocky Hock Creek. A drift gill net of similar
mesh size and a haul seine were used at Williams'
Fishery. None of the fish collected had spawned
yet.
Bluebacks were measured, weighed, and sexed,
and scales were removed for aging. The foregut and
midgut regions of the stomach anterior to the pyloric
caeca were removed and placed in 15% Formalin^
within 10-15 min of capture
Stomach contents were examined in the laboratory
under a dissecting scopa First, fullness of the
foregut and midgut, which are separate sections, was
estimated visually following Hynes (1950) and
Yoshiyama (1980). Five levels of fullness were
used: half full (1/2), full (1), and distended with food
(2) (as in Yoshiyama 1980), plus one quarter full (1/4),
and empty or with traces of food (0). Contents of
each section were then placed in a petri dish, iden-
tified, and counted. Also, the presence or absence
of prey items was noted.
Scales were viewed at 50 x through an EPO LP-2
Profile Projector and marks were interpreted follow-
ing Marcy (1969).
iRolland, B. F., Jr., and G. F. Yelverton. 1973. Offshore
anadromous fish exploratory fishing program. Completion report,
Project AFC-5, 123 p. North Carolina Department of Natural and
Economic Resources, Division of Commercial and Sports Fisheries,
Raleigh, NC 27611.
^S. Winslow, North Carolina Division of Marine Fisheries,
Elizabeth City, NC 27909, pers. commun. February 1980. S.
Winslow had determined the previous year (1979) that blueback
herring collected at this site on Rocky Hock Creek were spawn-
ing. Also, a dam upstream prevented blueback herring from moving
any further than 150 m above my collection sita
^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
FISHERY BULLETIN: VOL. 83, NO. 4, 1985.
711
Statistical Analysis
lb obtain a single index of stomach fullness, values
for the foreguts and midguts were combined by
using a weighted average In calculating mean
volumes each gut section was assumed to be approx-
imately cylindrical. The foregut to midgut volume
ratio, determined from five randomly chosen
stomachs, was 3.16:1. The following equation was
used to calculate the overall gut fullness:
F X 3.16 + M
4.16
with F and M representing the foregut and midgut
values, respectively.
A multiple regression (General Linear Model-
Statistical Analysis Systems) was initially employed
to determine which of the variables collected for each
fish (i.e, distance upstream, length, weight, sex, and
number of repeat spawnings) was most strongly cor-
related with stomach fullness, the dependent
variable Significant variables identified through
multiple regression analysis were further analyzed
with chi-square and F-tests.
Results
Presence of Food
Nearly all (91 of 103 or 88%) fish sampled in April
1980 contained food (Tkble 1) as did all 15 fish col-
lected in April 1981. High percentages of the fish
collected on each date in 1980 had food in their
stomachs (Tkble 1). About 53% (48 of 91) of the blue-
backs in 1980 (Tkble 1) and 73% (11 of 15) of the blue-
backs in 1981 had either foregut and/or midgut
fullnesses of 1/4 or greater. Approximately half of
the fish from each date in 1980, with the exception
of 13 April, had either foregut and/or midgut full-
nesses of 1/4 or greater (Tkble 1).
Diet
The diet of the bluebacks collected in 1980 at both
sites was composed of zooplankters, benthos, and
terrestrial insects (Tkble 2). Chydorid cladocerans
were the only zooplankters consumed in large
numbers at either location (Figs. 1, 2). Insects, which
accounted for 8.1% of the organisms consumed, oc-
curred in about half of the fish. Ephemeroptera
(Baetis), Coleoptera (Dytiscidae), and Heleidae lar-
vae, as well as chironomid larvae and pupae, were
the most conspicuous of the identifiable benthic in-
sects. Most insects, benthic and terrestial, were
unidentifiable. Chironomids occurred more frequent-
ly than other insect groups, but they accounted for
only 2.7% of the total prey items. Several terrestrial
insects were found in stomachs of bluebacks, par-
ticularly at Williams' Fishery. Insects, both benthic
and terrestrial, increased in importance with time
at Williams' Fishery, reaching about 22% during
later collections (Fig. 1). Insects represented a
smaller proportion of the diet at Rocky Hock Creek
(Fig. 2). Fish eggs (probably from alewives or blue-
backs), which occurred in the stomachs of several
bluebacks in 1980 (Figs. 1, 2), were the most abun-
dant food item in that year although their impor-
tance decreased with time Varying amounts of sand
and detritus occurred in many stomachs.
In 1981 the diet of bluebacks from Rocky Hock
Creek was much less diverse (Tkble 3). Cladocerans,
the predominant prey items, comprised 84.1% of the
diet. Almost half of the prey items were daphnid
Table 1.— Incidence of feeding and stomach fullness in male and female blueback herring collected at Williams' Fishery
(WF) and Rocky Hock Creek (RH) during April 1980.
No. fish
collected
per station
N
No. males
(M) and
females (F)
M F
No. fish (n)
with animal
matter In
stomach
n % F
No. of fish with >1/4 fullness
for the foregut, midgut or both
Station
and
date of
collection
Males
Females
Male
Fem
Total
JS +
ales
Fore
Mid
Both
Fore
Mid i
3oth
% N
WF-4-5-80
16
8
8
12
75.0
0
1
0
1
2
3
7
43.6
RH -4-6-80
9
3
6
9
100.0
0
0
0
2
1
2
5
55.6
WF-4-7-80
17
8
9
15
88.2
1
3
0
0
2
3
9
52.9
WF-4-11-80
17
10
7
15
88.2
2
2
0
1
2
1
8
47.1
RH -4-1 2-80
7
6
1
7
100.0
1
1
0
0
0
1
3
42.9
WF-4-13-80
23
9
14
20
87.0
2
1
0
0
4
1
8
34.8
WF-4-19-80
14
10
4
13
92.9
0
5
0
0
2
1
8
57.1
Total
103
54
49
91
88.4
6
13
0
4
13
12
48
712
cladocerans (Ikble 3). Few copepods were consum-
ed, although they occurred in about half the fish.
Ostracods were important numerically and in occur-
Table 2.— Diets of 103 blueback herring collected at Williams'
Fishery and Rocky Hock Creek during April 1980.
Frequencv
'Of
Proportions of
occurrence
prey items in diet
No. of fish
Prey taxon
observed in
%
No. of prey %
Copepoda
Calanoida
1
1.0
1 V)
Harpacticoida
5
4.9
12 0.4
Cyclopoida
35
33.9
80 2.8
Unidentifiable
7
6.8
21 0.7
Cladocera
Chydoridae
61
59.2
839 29.6
Other families
14
13.6
26 0.9
Ostracoda
15
14.6
58 2.0
Insecta
Miscellaneous
54
52.4
133 4.7
Diptera
Chironomidae
larvae
25
24.3
67 2.4
Chironomidae
pupae
5
4.9
7 0.3
Other families
12
11.7
20 0.7
Oligochaeta
1
1.0
1 V)
Mollusca
Sphaerildae
7
6.8
21 0.7
Fish eggs
43
41.8
1 ,273 44.9
Bryozoan statoblasts
20
19.4
178 6.3
Colonial hydrozoan
pieces
16
15.5
96 3.4
Hydracarina
5
4.9
5 0.2
Total
2,838 100.0
'<0.1%.
Table 3.— Diets of 15 blueback herring collected at Rocky Hock
Creek on 18 April 1981.
Frequency of
Proportions of
occurrence
prey items in diet
No. of fish
Prey taxon
observed in
%
No. of prey
%
Copepoda
Calanoida
5
33.3
8
0.1
Harpacticoida
7
46.6
7
0.1
Cyclopoida
7
46.6
23
0.4
Cladocera
Daphnidae
15
100.0
3,191
48.7
Daphnidae ephippia
12
80.0
1,825
27.9
Chydoridae
13
86.6
493
7.5
Bosminidae
2
13.3
5
V)
Ostracoda
13
86.6
929
14.2
Insecta
Miscellaneous
5
33.3
6
0.1
Diptera
Chironomidae
larvae
5
33.3
8
0.1
Fish eggs
1
6.6
7
0.1
Bryozoan statoblasts
11
73.3
42
0.6
Hydracarina
3
20.0
3
D
Fish larvae
1
6.6
1
V)
Total
6,548
99.8
rence, as were daphnid ephippia. Benthic prey, ter-
restrial insects, fish eggs, detritus, and sand were
rare
Number of Repeat Spawnings
About 85% (87 of 103) of the fish in 1980 and 71%
(10 of 14) in 1981 had spawned before (Ikble 4).
Although some bluebacks in 1980 had spawned as
many as six times, most (72%) had spawned only
once or twice before (Tkble 4). Almost equal numbers
of males (44) and females (43) were repeat spawners
in 1980.
Table 4.— Number of previous years that 103
blueback herring collected at Williams' Fishery
and Rocky Hock Creek during April 1980 had
spawned.
No. of years spawned
1 (first time) 2 3 4 5
6
Male
Female
Total
10 25 14 3 1
6 22 13 6 2
16 47 27 9 3
1
0
1
Relation Between Feeding Activity and
Length, Weight, Sex, Number of
Repeat Spawnings, and Distance Upstream
Sex was the only independent variable that con-
tributed significantly to variance in feeding rate
(Tkble 5). Female bluebacks fed more actively than
males. The full model explained only 21% of the
variance in gut fullness but this was significant {F
= 2.87, P>F = 0.005, 102 df). The near significant
contributions of length and weight to the reduction
of variance in the model is believed to have resulted
primarily from sex related differences in mean size
(x length females = 305.1 mm, x length males =
289.4 mm; x weight females = 258.0 g, x weight
males = 212.5 g). F^irther analysis of the feeding
activity of male and female bluebacks with a chi-
Table 5.— Summary of the contribution of each of
the independent variables to the multiple regression
model for data from 103 blueback herring collected
in 1980. Type IV F values and probability levels are
shown. P < 0.05 significance level used.
KO.1%.
Independent variable
F value
Probability
Site
2.64
0.1078
Sex
7.14
0.0089
No. of repeat spawnings
1.65
0.1818
Length
3.85
0.0527
Weight
3.81
0.0540
718
100
UJ
Q
90-
INSECTS
CHYCXDRIDS
80-
70-
^ 60-]
m
u
Ll
O 40H
y 3o^
on
u
^ 20
10-
0
12/16
OTHERS
HYDRO-
ZOANS
FISH EGGS
4/5
15/17
OTHERS
(OSTRAQODS
STATO-
BLASTS
HYDRO -
ZOANS
CHIRON-
OMIDS
CYCLO-
POIDS
INSECTS
CHYDORIDS
Fl SH EGGS
15/17
OTHERS
STATO-
B LASTS
HYDRO-
20ANS
CHIRON -
OMIDS
CYCLO-
POIDS
INSECTS
CHYDORIDS
FISH EGGS
20/23
OTHERS
HYDRO-
ZOANS
CHIRON-
OMIDS
■Y
CYCLO-
POIDS
INSECTS
CHYDORIDS
FISH EGGS
13/14
OTHERS
STATO-
B LASTS
CHIRON-
OMIDS
■Y
CYCLO-
POIDS
INSECTS
ICHYDORIDS
^
FISH EGGS
^
4/7 4/11 4/13
COLLECTION DATES (1980)
4/19
Figure 1— Changes in the composition of the combined diet (both males and females) over the five collection dates
at Williams' Fishery in April 1980. Numbers above each bar graph indicate number of stomachs with food/total number
of stomachs examined.
square 2x2 contingency table also found signif-
icantly greater levels of feeding activity among
females (x^ value = 5.86, P < 0.025). The difference
in 1980, however, may depend on site. More females
had stomach fullnesses >l/4 than males at Rocky
Hock (x^ value 6.349, P < 0.025), but the difference
was not significant at Williams' Fishery.
For the three most abundant food items females
consumed significantly greater numbers of chydorid
cladocerans (F = 6.02, P>F = 0.0001), insects (F
= 7.64, P>F = 0.0001), and fish eggs (F = 90.15,
P>F= 0.0001) than males in 1980.
Discussion
Blueback herring spawning in the Chowan River
do not stop feeding during their freshwater migra-
tions. Williams' Fishery and Rocky Hock Creek are
714
100
90
9/9
7/7
UJ
Q
Q
LlI
CD
§50
O
40
OSTR/COCS
80-
70-
CHYDORiDS
60-
LlI
Q_
20 H
10-
0
OTHERS
CHIRON-
CYCLO-
POIDS
INSECTS
FISH EGGS
OSTRACOCE
CHYDORIDS
OTHERS
FISH EGGS
4/6 4/12
COLLECTION DATES (1980)
Figure 2.— Changes in the composition of the combined diet (both
males and females) over the two collection dates at Rocky Hock
Creek in April 1980. Numbers above each bar graph indicate
number of stomachs with food/total number of stomachs examined.
too far from the estuary for bluebacks to travel to
saltwater for daily feeding. It is important to note,
also, that the interface between freshwater and salt-
water often extends far out into Albemarle Sound
due to the spring discharge of both the Chowan and
Roanoke Rivers. This was the case in the spring of
1980.'* Moreover, the prey were exclusively of fresh-
water origin. There is, therefore, little doubt that
these bluebacks were feeding in freshwater.
The wide diversity of food items consumed was
unexpected since bluebacks have previously been
reported to be primarily planktivorous (Bigelow and
Schroeder 1953; Hildebrand 1963). The limited 1981
data suggest that prey other than zooplankters are
consumed infrequently if sufficient zooplankters (or
large zooplankters such as Daphnia) are present.
However bluebacks are also capable, as the 1980 data
demonstrate, of foraging opportunistically on other
riverine fauna and terrestrial insects, which could
also explain Frankensteen's (1976) unusual finding
that chironomids were the dominant prey of blueback
herring in the Ikr River. Consumption of benthic
prey probably accounts for the presence of detritus
and sand in the guts.
My data show a difference between male and
female feeding activity. There are two possible ex-
planations for this difference First, females may re-
quire more energy than males during the spawning
migration thus they consume more prey. Neither this
study nor other studies of bluebacks have produced
data to either support or refute this idea. However,
moderate to severe weight loss is common among
other spawning anadromous fishes (eg., Atlantic
salmon, American shad) with females suffering
greater weight loss than males (Belding 1934; Chit-
tenden 1976; Glebe and Leggett 1981). Glebe and
Leggett (1981) found that development of ovaries in
female shad required more energy and time than the
male shads' testes. Consequently, female shad enter-
ing freshwater, particularly southern rivers, often
do not have fully developed ovaries. Thus, not only
must females expend energy for swimming but for
gonad development as well. The same difference in
gonad development may exist between male and
female bluebacks and could explain the different
levels of feeding activity observed in this study.
The second explanation for the difference in
feeding activity is that all bluebacks, regardless of
sex, stop feeding while spawning. However, males
might remain on the spawning grounds longer than
females. Thus, if females leave the area immediate-
ly after they spawn and are replaced by newly ar-
rived females with relatively full guts, this could
cause the gut samples to be biased. This explana-
tion appears to be ruled out by the 1981 data,
however, since half the fish with stomachs >1/A full
collected at Rocky Hock were males.
While previous researchers have found food in
bluebacks' stomachs (Williams et al. 1975 as cited
■•R. Holmes, Department of Natural Resources and Community
Development, Division of Environmental Management, Raleigh, NC
27611, pers. commun. March 1984.
715
in Rulifson et al. 1982; Frankensteen 1976), my find-
ing of a regular occurrence of significant volunnes
of food in blueback stomachs is unprecedented. Fur-
ther research is needed to determine the extent to
which feeding in freshwater is common among
spawning bluebacks in other river systems, and
possibly other anadromous species, and to determine
if a relationship exists between freshwater feeding
and spawning energetics.
Acknowledgments
I am grateful to Seth Reice and Edward Kuenzler
for providing assistance, materials, and workspace
for this study. I also wish to thank Jerry Diamond,
Seth Reice, William Leggett, Angela Arthington,
Rob Edwards, Brad Foster, and three anonymous
reviewers for their careful readings of the manu-
script. Assistance from Mr. and Mrs. Williams and
the staff of Williams' Fishery, Sara Winslow, Bar-
rel Johnson, and Michael Street of the North
Carolina Division of Marine Fisheries, David Ham-
mer, Chris Nations, Ernie Patterson, and Diana
Hyland, as well as thought-provoking discussions
with many other people, is greatly appreciated.
Literature Cited
Belding, D. L.
1934. The cause of the high mortahty in the Atlantic salmon
after spawning. Trans. Am. Fish. Soc 64:219-224.
BiGELOW, H. B., AND W. C. SCHROEDER.
1953. Fishes of the Gulf of Maine U.S. Fish Wildl. Serv.,
Fish. Bull. 53, 577 p.
BURBIDGE, R. G.
1974. Distribution, growth, selective feeding, and energy
transformations of young-of-the-year blueback herring, Alosa
aestivalis (Mitchill), in the James River, Virginia. TVans. Am.
Fish. Soc 103:297-311.
Chittenden, M. E., Jr.
1976. Weight loss, mortality, feeding, and duration of
residence of adult American shad, Alosa sapidissima, in fresh
water. Fish. Bull., U.S. 74:151-157.
Crecco, V. A., AND M. M. Blake.
1983. Feeding ecology of coexisting larvae of American shad
and blueback herring in the Connecticut River. Trans. Am.
Fish. Soc 112:498-507.
Davis, J. R., and R. R Cheek.
1966. Distribution, food habits, and growth of young clupeids,
Cape Fear River system. North Carolina. Proc 20th Annu.
Conf., SE Assoc Game Fish. Comm., p. 250-259.
DOMERMUTH, R. B., AND R. J. REED.
1980. Food of juvenile American shad, Alosa sapidissima,
juvenile blueback herring, Alosa aestivalis, and pumpkinseed,
Lepomis gihhosus, in the Connecticut River below Holyoke
Dam, Massachusetts. Estuaries 3:65-68.
Frankensteen, E. D.
1976. Genus Alosa in a channelized and an unchannelized
creek of the Tkr River basin. North Carolina. M.A. Thesis,
East Carolina University, Greenville, NC, 123 p.
Glebe, B. D., and W. C. Leggett.
1981. Latitudinal differences in energy allocation and use dur-
ing the freshwater migrations of American shad (Alosa
sapidissima) and their life history consequences. Can. J.
Fish. Aquat. Sci. 38:806-820.
Hildebrand, S. F.
1963. Family Clupeidae In H. B. Bigelow (editor). Fishes of
the Western North Atlantic, Part 3, p. 257-454. Sears Found.
Mar. Res., Yale University, New Haven, CT.
Hynes, H. B. N.
1950. The food of fresh-vrater sticklebacks (Gasterostevs
aculeat-us and Pygosteus pungitivs), with a review of methods
used in the studies of the food of fishes. J. Anim. Ecol.
19:36-58.
Marcy, B. C, Jr.
1969. Age determinations from scales of Alosa pseudoharen-
giis (Wilson) and Alosa aestivalis (Mitchill) in Connecticut
waters. Trans. Am. Fish. Soc 98:622-630.
Neves, R. J.
1981. Offshore distribution of alewif e, A losa pseudoharengus,
and blueback herring, Alosa aestivalis, along the Atlantic
coast. Fish. Bull, U.S. 79:473-485.
Nichols, P. R.
1966. Anadromous Fishes Program. In Annual Report of the
Bureau of Commercial Fisheries Biological Laboratory, Beau-
fort, N.C., for the fiscal year ending June 30, 1966, p. 4-8.
U.S. Fish Wildl. Serv. Circ 264.
Rulifson, R. A., M. T. Huish, and R. W. Thoesen.
1982. Anadromous fish in the southeastern United States and
recommendations for development of a management plan.
U.S. Fish Wildl. Serv., Fish. Res., Reg. 4, Atlanta, GA, 525 p.
Scott, W. B., and E. J. Grossman.
1973. Freshwater fishes of Canada. Fish. Res. Board Can.
Bull. 184, 966 p.
Yoshiyama, R. M.
1980. Food habits of three species of rocky intertidal sculpins
(Cottidae) in central California. Copeia 1980:515-525.
Robert P. Creed, Jr.
Department of Biology
University of North Carolina
Chapel Hill, NC 275U
Present address:
Department of Zoology
Michigan State University
East Lansing, MI Jt882jlt
716
INDEX
Fishery Bulletin Vol. 83, Nos. 1-4
Age-composition
anchovy, northern 483
Age determination
alewife 696
fishes 103
multiple regression models 108
scale and otolith methods 696
"Age growth and distribution of larval spot Leiostomus
xanthurus" by Stanley M. Warlen and Alexander J.
Chester 587
ALBERS, W. D, and P. J. ANDERSON, "Diet of Pacific
cod, Gadvs macrocephalus, and predation on the northern
pink shrimp, Pandalus horealis, in Pavlof Bay, Alaska". . . 601
ALLEN, LARRY G.-see DeMARTINI et al.
Alosa aestivalis— see Herring, blueback
Alosa pseudoharengus—see Alewife
Ampelisca agassizi—see Amphipods, benthic
Amphipods, benthic
parasites of 497
Anchovy, northern
egg production and mortality rate 137
growth and age composition 483
rates of ovarian atresia 119
schooling behavior 235
ANDERSON, P J.-see ALBERS and ANDERSON
ANKENBRANDT, LISA, "Food habits of bait-caught skip-
jack tuna, Katsuwomis pelamis, from the southwestern
Atlantic Ocean" 379
"Annual band deposition within the shells of the hard clam,
Mercenaria mercenaria: consistency across habitat near
Cape Lookout, North Carolina," by Charles H. Peterson,
P. Bruce Duncan, Henry C. Summerson, and Brian F.
Beal 671
Anoplopoma fimbria— see Sablefish
"An approach to estimating an ecosystem box model," by
Jeffrey J. Polovina and Mark D. Ow 457
"Aspects of the life history of the fluffy sculpin, Oligocot-
tu£ snyderi" by Mary C. Freeman, Nate Neally, and Gary
D. Grossman 645
AU, DAVID W. K., and WAYNE L. PERRYMAN, "Dolphin
habitats in the eastern tropical Pacific" 623
Balaena misticetvs—see Whales, bowhead
BARLOW, JAY-see GERRODETTE et al.
BARLOW, JAY, "Variability, trends, and biases in reproduc-
tive rates of spotted dolphins, Stenella attenuata" 657
BARNES, A.-see LESTER et al.
BEAL, BRIAN F.-see PETERSON et al.
"Behavior of bowhead whales, Balaena mysticetus, sum-
mering in the Beaufort Sea: a description," by Bernd Wiir-
sig, Eleanor M. Dorsey, Mark A. Fraker, Roger S. Payne,
and W John Richardson 357
Behavior studies
anchovy, northern 235
dolphins 187
whales, bowhead 357
BERMINGHAM, E. L.-see McFARLAND et al.
"Biological aspects of the spring breeding migration of
snow crab, Chionoecetes opilio, in Bonne Bay, Newfound-
land (Canada)," by D. M. Ikylor, R. G. Hooper, and G P
Ennis 707
Bocaccio
seasonal changes in fat and gonad volume 299
BOEHLERT, GEORGE W, "Using objective criteria
and multiple regression models for age determination in
fishes" 103
BOEHLERT, GEORGE W, and MARY M. YOKLAVICH,
"Larval and juvenile growth of sablefish, Anoplopoma fim-
bria, as determined from otolith increments 475
BOEHLERT GEORGE W, DENA M. GADOMSKI, and
BRUCE C. MUNDY, "Vertical distribution of ichthyo-
plankton off the Oregon coast in spring and summer
months" 611
BROOKS, E. R.-see MULLIN et al.
BROTHERS, E. B.-see McFARLAND et al.
BROWN, R. S., and N. CAPUTI, "Factors affecting the
growth of undersize western rock lobster, Panulirvs cygnus
George, returned by fishermen to the sea" 567
CAMPBELL, A.-see JAMIESON and CAMPBELL
Cancer magister—see Crab, Dungeness
717
CAPUTI, N.-see BROWN and CAPUTI
Carcharhinus plumbevs—see Sharks, sandbar
CASEY, JOHN J.-see MEDVED et al.
Catshark
life history notes 695
CHAN. BRIAN-see NEILSON et al.
CHESTER, ALEXANDER J.-see WARLEN and
CHESTER
Chilipepper
seasonal changes in fat and gonad volume 299
Chionoecetes opilio—see Crab, snow
Clam, hard
growth band deposition 671
Clam, soft-shell
spawning cycle in San Francisco Bay 403
Clupea harengus harengus— see Herring, Atlantic
Cod, Pacific
diet and predation in Pavlof Bay, Alaska 601
COLLINS, ROBSON A.-see LOVE et al.
"A comparison of scale and otolith aging methods for the
alewife, Alosa pseudoharengus" by David A. Libby .... 696
"Confidence limits for population projections when vital
rates vary randomly" by Tim Gerrodette, Daniel Goodman,
and Jay Barlow 207
CONOVER, DAVID 0., "Field and laboratory assessment
of patterns in the fecundity of a multiple spawning fish:
the Atlantic silverside" 331
Crab, Dungeness
salmonid predation 683
Crab, snow
spring breeding migration 707
Crangonidae— see Shrimp
CREED, ROBERT R, Jr., "Feeding, diet, and repeat spawn-
ing of blueback herring, Alosa aestivalis, from the Chowan
River, North Carolina" 711
CROSS, JEFFREY N., "Fin erosion among fishes collected
near a southern California municipal wastewater outfall
(1971-1982)" 195
Delphinus delphis—see Dolphins, common
DeMARTINI, EDWARD E., LARRY G. ALLEN, ROBERT
K. FOUNTAIN, and DALE ROBERTS, "Diel and depth
variations in the sex-specific abundance, size composi-
tion, and food habits of queenfish, Seriphus politus
(Sciaenidae)" 171
"The development and occurrence of larvae of the longfin
Irish lord, Hemilepidotiis zapus (Cottidae)," by Ann C.
Matarese and Beverly M. Vinter 447
Dichelopandalus leptocems—see Shrimp
"Diel and depth variations in the sex-specific abundance,
size composition, and food habits of queenfish, Seriphus
politiis (Sciaenidae)" by Edward E. DeMartini, Larry G.
Allen, Robert K. Fountain, and Dale Roberts 171
Diet— see Food habits
"Diet of Pacific cod, Gadiis macrocephalus, and predation
on the northern pink shrimp, Pandalus borealis, in Pavlof
Bay, Alaska," by W. D. Albers and P. J. Anderson 601
"Distributional patterns of fishes captured aboard commer-
cial passenger fishing vessels along the northern Channel
Islands," by Milton S. Love, William Westphal, and Robson
A. Collins 243
"Dolphin habitats in the eastern tropical Pacific," by David
W. K. Au and Wayne L. Perryman 623
Dolphins
habitats in the eastern tropical Pacific 623
incidental mortality 521
reactions to population survey vessels 187
Dolphins, common
undersea topography and distribution 472
Dolphins, spotted
growth rates 553
reproductive rates 657
DORSEY, ELEANOR-see WURSIG et al.
DUNCAN, BRUCE P.-see PETERSON et al.
"Early postnatal growth of the spotted dolphin, Stenella
attenuata" by Aleta A. Hohn and P. S. Hammond 553
Economic studies
rock shrimp 1
Ecosystems
the ECOPATH model 457
estimating a box model 457
"Effects of feeding regimes and diel temperature cycles on
otolith increment formation in juvenile chinook salmon, On-
corhynchvs tshawytscha" by John D. Neilson and Glen H.
Geen 91
"The effects of net entanglement on the drag and power
output of a California sea lion, Zalophus califomianus" by
Steven D. Feldkamp 692
"Egg production of the central stock of northern anchovy,
Engraulis mordax" by Nancy C. H. Lo 137
718
Eggs— see also Embryos
Embryos
salmonid 81
Engraulis mordax—see Anchovy, northern
ENNIS, G. P.-see TAYLOR et al.
Environmental effects
anchovy, northern 483
dolphin habitats 623
food web 151
grunts, French 413
larval fish 313
mummichog 467
porpoise, harbor 427
tilefish 443
"Factors affecting the growth of undersize western rock
lobster, PanuliTus cygnus George, returned by fishermen
to the sea," by R. S. Brown and N. Caputi 567
"Feeding, diet, and repeat spawning of blueback herring,
Alosa aestivalis, from the Chowan River, North Carolina,"
by Robert R Creed, Jr. 711
FELDKAMP, STEVEN D, "The effects of net entangle-
ment on the drag and power output of a California sea lion,
Zalophus califomianus" 692
"Field and laboratory assessment of patterns in fecundity
of a multiple spawning fish: the Atlantic silverside," by
David 0. Conover 331
"Fin erosion among fishes collected near a southern Califor-
nia municipal wastewater outfall," by Jeffrey N. Cross. . . 195
Fish
distributional patterns in the Channel Islands 243
Fish assemblages, demersal
estimates of marine populations 508
temporal and spatial patterns 507
Fish, larval
distribution and abundance in the northeastern U.S. ... 313
Fishery, eastern Pacific
shrimp 1
Fishery, Gulf of Mexico
juvenile brown shrimp as abundance predictors 677
Fishery, tima
parasite use for stock management 343
Fishery, western Australian
lobster, western rock 567
FLIERL, G. R., and J. S. WROBLEWSKI, "The possible
influence of warm core Gulf Stream rings upon shelf water
larval fish distribution" 313
"Food and feeding of the tomtate, Haemulon aurolineatum
(Pisces, Haemulidae) in the South Atlantic Bight," by
George R. Sedberry 461
"Food habits of bait-caught skipjack tuna, Katsuwonus
pelamis, from the southwestern Atlantic Ocean," by Lisa
Ankenbrandt 379
"Food habits of juvenile rockfishes (Sebastes) in a central
California kelp forest," by Michael M. Singer 531
Food habits
queenfish 171
rockfish 531
sharks, sandbar 395
tomtate 461
tuna, skipjack 379
FOUNTAIN, ROBERT K.-see DeMARTINI et al.
FRAKER, MARK A.-see WURSIG et al.
FREEMAN, MARY C, NATE NEALLY, and GARY D.
GROSSMAN, "Aspects of the life history of the fluffy
scizlpin Oligocottus snyderi 645
Fundulus heteroclittis—see Mummichog
GADOMSKI, DENA M.-see BOEHLERT et al.
Gadus mojcrocephalus—see Cod, Pacific
GASKIN, DAVID E.-see READ and GASKIN
GASKIN, DAVID E., and ALAN P WATSON, "The
harbor porpoise, Phocoena phocoena, in Fish Harbour, New
Brunswick, Canada: occupancy, distribution, and move-
ments" 427
GERRODETTE, TIM, DANIEL GOODMAN, and JAY
BARLOW, "Confidence limits for population projections
when vital rates vary randomly" 207
GEEN, GLEN H.-see NEILSON and GEEN
GEEN, GLEN H.-see NEILSON et al.
Globicephala macrorhynchus—see Whales, Pacific pilot
GOODMAN, DANIEL-see GERRODETTE et al.
GROSSMAN, GARY D.-see FREEMAN et al.
GROSSMAN, GARY D., MICHAEL J. HARRIS, and
JOSEPH E. HIGHTOWER, "The relationship between
tilefish, Lopholatilus chamaeleonticeps, abundance and sedi-
ment composition off Georgia" 443
Growth rates
dolphin, spotted 553
herring, Atlantic 289
lobster, rock 567
Grunts, French
recruitment patterns in Hague Bay, Virgin Islands ... 413
719
GUILLEMOT, PATRICK J., RALPH J. LARSON, and
WILLIAM H. LENARZ, "Seasonal cycles of fat and gonad
volume in five species of northern California rockfish". . .
299
HABIB, G.-see LESTER et al.
Haemulon aurolineatum—see Ibmtate
Haemulon Jlavolineatum—see Grunts, French
HAMMOND, R S.-see HOHN and HAMMOND
"The harbor porpoise^ Phocoena phocoena, in Fish Harbour,
New Brunswick, Canada: occupancy, distribution, and move-
ments," by David E. Gaskin and Alan P. Watson 427
HARRIS, MICHAEL J.-see GROSSMAN et al.
HAYNES, EVAN B., "Morphological development, iden-
tification, and biology of larvae of Pandalidae; Hippolytidaei
and Crangonidae (Crustacea, Decapoda) of the northern
North Pacific Ocean" 253
Hemilepidotus zapus—see Lord, longfin Irish
Herring, Atlantic
growth comparison studies 289
Herring, blueback
diet and spawning in the Chowan River, North Caro-
lina 711
HEWITT, ROGER R, "Reactions of dolphins to a survey
vessel: effects on census data 187
HIGHTOWER, JOSEPH E.-see GROSSMAN et al.
HINES, ANSON H., KENRIC E. OSGOOD, and JOSEPH
J. MIKLAS, "Semilunar reproductive cycles in Fundulus
heteroclitus (Pisces: Cyprinodontidae) in an area without
lunar tidal cycles" 467
Hippolytidae— see Shrimp
HOHN, ALETA A, and R S. HAMMOND, "Early postnatal
growth of the spotted dolphin, Stenella attenuata, in the
offshore eastern tropical Pacific" 553
Homarus americanvs—see Lobster, American
HOOPER, R. G.-see TAYLOR et al.
HORTON, HOWARD F.-see MAULE and HORTON
HUI, CLIFFORD A., "Undersea topography and com-
parative distributions of two pelagic cetaceans 472
HUNTER, J. ROE, and BEVERLY J. MACEWICZ, "Rates
of atresia in the ovary of captive and wild northern anchovy,
Engraulis mordax" 119
HUNTER, JOHN, and RAGAN NICHOLL, "Visual
threshold for schooling in northern anchovy, Engraulis
mordax" 235
720
Ichthyoplankton
vertical distribution off the Oregon coast 611
JAMIESON, G. S., and A. CAMPBELL, "Sea scallop
fishing impact on American lobsters in the Gulf of St.
Lawrence" 575
JOHNSON, PHYLLIS T, "Parasites of benthic amphipods:
microsporidans of Ampelisca agassizi (Judd) and some
other gammarideans" 497
JONES, CYNTHIA, "Within-season differences in growth
of larval Atlantic herring, Clupea harengiis harengus . . . 289
Katsuwonits pelamis—see Tbna, skipjack
KOTCHIAN-PRENTISS, N. M.-see McFARLAND et al.
LARSON, RALPH J.-see GUILLEMOT et al.
Larvae
fish, environmental effects 313
food web off southern California coast 151
herring, Atlantic, growth studies 289
lord, longfin Irish, development in Bering Sea 447
sable fish grovrth 475
shrimp 253
spot 587
"Larval and juvenile growth of sablefish, Anoplopoma fim-
bria, as determined from otolith increments," by George
W Boehlert and Mary M. Yoklavich 475
Leiostomus xanthurvs—see Spot
LENARZ, WILLIAM H.-see GUILLEMOT et al.
LESTER, R. J. G., A. BARNES, and G. HABIB, "Para-
sites of skipjack tuna, Katsuwonus pelamis: fishery
implications" 343
LIBBY, DAVID A., "A comparison of scale and otolith aging
methods for the alewife, Alosa pseudoharengus" 696
"Life history characteristics of Pandalus montagui and
Dichelopandalus leptocerus in Penobscot Bay, Maine," by
David K. Stevenson and Fran Pierce 219
LO, NANCY C. H., "Egg production of the central stock
of northern anchovy, Engraulis mordax" 137
Lobster, American
damage from scallop drags 575
Lobster, rock
factors affecting growth 567
"Long-term responses of the demersal fish assemblages
of Georges Bank," by William J. Overholtz and Albert V.
Tyler 507
Lopholatilus chamaeleonticeps—see Tilefish
Lord, longfin Irish
development of larvae
447
LOVE, MILTON S., WILLIAM WESTPHAL, and ROB-
SON A. COLLINS, "Distributional patterns of fishes cap-
tured aboard commercial passenger fishing vessels along
the northern Channel Islands" 243
Lyopsetta exilis—see Ichthyoplankton
plankton off southern California: a storm and a larval fish
food web" 151
Mummichog
semilunar reproductive cycles .
MUNDY, BRUCE C.-see BOEHLERT et al.
Mya arenaria—see Clam, soft-shell
467
MACEWICZ, BEVERLY J.-see HUNTER and
MACEWICZ
MAIS, K. F.-see PARRISH et al.
MALLICOATE, D. L.-see PARRISH et al.
MATARESE, ANN C, and BEVERLY M. VINTER, "The
development and occurrence of larvae of the longfin Irish
lord, Hemilepidotus zajms (Cottidae)" 447
MAULE, ALEC G., and HOWARD F. HORTON, "Prob-
able causes of the rapid growth and high fecundity of
walleye, Stizostedion vitreum vitreum in the mid-Columbia
River" 701
McFARLAND, W. N., E. B. BROTHERS, J. C. OGDEN,
M. J. SHULMAN, E. L. BERMINGHAM, and N. M.
KOTCHIAN-PRENTISS, "Recruitment patterns in young
French grunts, Haemulon flavolineatum (family
Haemulidae) at St. Croix, Virgin Islands" 413
MEDVED, ROBERT J., CHARLES E. STILLWELL, and
JOHN J. CASEY, "Stomach contents of young sandbar
sharks, Carcharhinus plumbeus, in Chincoteague Bay,
Virginia" 395
Menidia menidia—see Silverside, Atlantic
Mercenaria mercenaria—see Clam, hard
Migration
crab, snow 707
ichthyoplankton 611
lobster, American 575
porpoise, harbor 543
queenfish 171
salmon, coho 682
MIKLAS, JOSEPH J.-see HINES et al.
Morphology
lord, longfin Irish, larvae 447
shrimp, larvae 253
shrimp, rock 1
"Morphological development, identification, and biology of
larvae of Pandalidae, Hippolytidae, and Crangonidae
(Crustacea, Decapoda) of the northern North Pacific
Ocean," by Evan B. Haynes 253
Mullin, M. M., E. R. BROOKS, F M. H. RE ID, J. NAPP,
and E. R. STEWART, "Vertical structure of nearshore
NAPP, J.-see MULLIN et al.
NEALLY, NATE-see FREEMAN et al.
NEILSON, JOHN D, GLEN H. GEEN, and BRIAN
CHAN, "Variability in dimensions of salmonid otolith
nuclei: implications for stock identification and microstruc-
ture interpretation" 81
NEILSON, JOHN D., and GLEN H. GEEN, "Effects of
feeding regimes and diel temperature cycles on otolith in-
crement formation in juvenile chinook salmon, Oneorhyn-
chus tshawytscha" 91
NIESEN, THOMAS M.-see ROSENBLUM and NIESEN
"Notes on the life history of the catshark Scyliorhiniis
meadi" by Glenn R. Parsons 695
"Observer effect on incidental dolphin mortality in the
eastern tropical Pacific tuna fishery," by Bruce E. Wahlen
and Tim D. Smith 521
OGDEN, T C.-see McFARLAND et al.
Oligocottus snyderi—see Sculpin, fluffy
Oncorhynchus tshawytscha— see Salmon, chinook
OSGOOD, KENRIC E.-see HINES et al.
Otoliths
alewives 696
herring, Atlantic 289
multiple regression models 103
rockfish 103
sablefish 475
salmon, chinook 81, 91
trout, rainbow 81
OVERHOLTZ, WILLIAM J., and ALBERT V. TYLER,
"Long-term responses of the demersal fish assemblages of
Georges Bank" 507
OW MARK D.-see POLOVINA and OW
Pandalus borealis—see Shrimp, northern pink
Pandalus montagui—see Shrimp
Pandalidae— see Shrimp
721
Panulims q^gnus—see Lobster, rock
"Parasites of benthic amphipods: microsporidans of Am-
pelisca agassizi (Judd) and some other gammarideans," by
Phyllis T. Johnson 497
"Parasites of skipjack tuna, Katsuwonus pelamis: fish-
ery implications," by R. J. G. Lester, A. Barnes, and G.
Habib 343
Parasite studies
amphipods 497
tuna, skipjack 343
PARRISH, R. H., D. L. MALLICOATE, and K. F. MAIS,
"Regional variations in the growth and age composition of
northern anchovy, Engraulis mordax" 483
PARSONS, GLENN R., "Notes on the life history of the
catsharks Scyliorhinus meadi" 695
PAYNE, ROGER S.-see WtJRSIG et al.
Penaeus aztecus—see Shrimp, brown
PEREZ FARFANTE, ISABEL, "The rock shrimp genus
Sicyonia (Crustacea: Decapoda: Penaeoidea) in the eastern
Pacific 1
FERRYMAN, WAYNE L.-see AU and FERRYMAN
PETERSON, CHARLES H., R BRUCE DUNCAN,
HENRY C. SUMMERSON, and BRIAN F BEAL, "Annual
band deposition within shells of the hard clam, Mercenaria
mercenaria: consistency across habitat near Cape Lookout,
North Carolina" 671
Phocoena phocoena—see Porpoises, harbor
Phytoplankton
vertical structure off southern California 151
PIERCE, FRAN-see STEVENSON and PIERCE
Plankton
ichthyoplankton off the Oregon coast 611
vertical structure off southern California 151
POLOVINA, JEFFREY J., and MARK D. OW, "An ap-
proach to estimating an ecosystem box model" 457
Population studies
confidence limits for projections 207
dolphin reactions to survey vessels 187
estimates using juvenile shrimp 677
Porpoises, harbor
distribution and movements in Fish Harbour 427
movements and activities 543
"The possible influence of warm core Gulf Stream rings
upon shelf water larval fish distribution," by G. R. Flierl
and J. S. Wroblewski 313
"A possible link between coho (silver) salmon enhancement
722
and a decline in central California Dungeness crab abun-
dance," by David H. Thomas 682
"Probable causes of the rapid growth and high fecundity
of walleye, Stizostedion vitreum vitreum, in the mid-
Columbia River," by Alec G. Maule and Howard F
Horton 701
Psettichthys melanostictus—see Ichthyoplankton
Queenfish
food habits, migration, and abundance 171
"Radio tracking the movements and activities of harbor por-
poises, Phocoena phocoena (L.), in the Bay of Fundy,
Canada," by Andrew J. Read and David E. Gaskin 543
"Rates of atresia in the ovary of captive and wild northern
anchovy, Engraulis mordax" by J. Roe Hunter and Beverly
J. Macewicz 119
"Reaction of dolphins to a survey vessel: effects on census
data," by Roger R Hewitt 187
READ, ANDREW J., and DAVID E. GASKIN,' "Radio
tracking the movements and activities of harbor porpoises,
Phocoena phocoena (L.), in the Bay of F\indy, Canada". . . 543
"Recruitment patterns in young French grunts, Haemulon
flavolineatum (family Haemulidae), at St. Croix, Virgin
Islands," by W N. McFarland, E. B. Brothers, J. C. Ogden,
M. J. Shulman, E. L. Bermingham, and N. M. Kotchian-
Prentiss 413
"Regional variations in the growth and composition of
northern anchovy, Engraulis mordax" by R. H. Parrish, D.
L. Mallicoate, and K. F. Mais 483
REID, F. M. H.-see MULLIN et al.
"The relationship between tilefish, Lopholatilus chamae-
leonticeps, abundance and sediment composition off
Georgia," by Gary D. Grossman, Michael J. Harris, and
Joseph E. Hightower 443
Reproductive biology
clam, soft-shell 403
dolphins, spotted 657
grunts, French 413
mummichog 467
silverside, Atlantic 331
RICHARDSON, W. JOHN-see WtJRSIG et al.
ROBERTS, DALE-see DeMARTINI et al.
"The rock shrimp genus Sicyonia (Crustacea: Deca-
poda: Panaeoidea) in the eastern Pacific," by Isabel P6rez
Farfante 1
Rockfish
age determination 103
food habits 531
Rockfish, calico
fin erosion 195
Rockfish, canary
seasonal changes in fat and gonad volume 299
Rockfish, widow
seasonal changes in fat and gonad volume 299
Rockfish, yellowtail
seasonal changes in fat and gonad volume 299
ROSENBLUM, SHELLY E., and THOMAS M. NIESEN,
"The spawning cycle of soft-shell clam, Mya arenaria, in
the San Francisco Bay" 403
Sablefish
growth 475
Salmo gairdneri—see TVout, rainbow
Salmon, chinook
otoliths 81, 91
Salmon, coho
predation on Dungeness crab 682
Salmon, silver— see Salmon, coho
Scallops, sea
abundance 580
fishery damage to American lobsters 575
Sculpin, fluffy
life history aspects 645
Scyliorhinus meadi—see Catshark
Sea-lion, California
entanglement studies 692
"Sea scallop fishing impact on American lobster in the Gulf
of St. Lawrence," by G. S. Jamieson and A. Campbell. . . 575
"Seasonal cycles of fat and gonad volume in five species of
northern California rockfish," by Patrick J. Guillemot, Ralph
J. Larsen, and William H. Lenarz 299
5e6astes— see Rockfish
Sebastes entomelas—see Rockfish, widow
Sebastes flavidns—see Rockfish, yellowtail
Sebastes goodei—see Chilipepper
Sebastes paucispinis—see Bocaccio
Sebastes pinniger—see Rockfish, canary
SEDBERRY, GEORGE R., "Food and feeding of the tom-
tate, Haemulon aurolineatum (Pisces, Haemulidae) in the
South Atlantic Bight" ■ 461
Seriphiis politiis—see Queenfish
"Semilunar reproductive cycles in Fundulus heteroclitus
(Pisces: Cyprinodontidae) in an area without lunar tidal
cycles," by Anson H. Hines, Kenric E. Osgood, and Joseph
J. Miklas 467
Sharks, sandbar
food habits in Chincoteague Bay, Virginia 395
Shrimp
abundance 223
identification and development 253
length-frequency data 222
life history aspects 219
Pandalidae, Hippolytidae, Crangonidae larvae 253
sex transition 225
Shrimp, brown
population estimates using juveniles 677
Shrimp, northern pink
Pacific cod diet in Pavlof Bay, Alaska 601
Shrimp, rock
description and taxonomy in the eastern Pacific 1
SHULMAN, M. J.-see McFARLAND et al.
Silverside, Atlantic
patterns in fecundity 331
SINGER, MICHAEL M., "Food habits of juvenile rock-
fishes (Sebastes) in a central California kelp forest" .... 531
Size-composition
queenfish 172
SMITH, TIM D.-see WAHLEN and SMITH
Sole, Dover
fin erosion 195
Sole, rex
fin erosion 195
"The spawning cycle of soft-shell clam, Mya arenaria in San
Francisco Bay," by Shelly E. Rosenblum and Thomas M.
Niesen 403
Spawming— see Reproductive biology
Spot
age, growth and distribution of larvae in North Caro-
lina coastal waters 587
"Standing stock of juvenile brown shrimp, Penaeus aztecus,
in Tfexas coastal ponds," by Loretta F Sullivan 677
Stenella attenuata—see Dolphins, spotted
STEVENSON, DAVID K., and FRAN PIERCE, "Life
history characteristics oiPandalus montagui and Dichelo-
pandalus leptocerus in Penobscot Bay, Maine" 219
723
STEWART, E. F.-see MULLIN et al.
STILLWELL, CHARLES E.-see MEDVED et al.
Stizostedion vitreum vitreum—see Walleye
Stock identification
salmonid
"Stomach contents of young sandbar sharks, Carcharhinvs
plumbeics, in Chincoteague Bay, Virginia," by Robert J.
Medved, Charles E. Still well, and John J. Casey
SULLIVAN, LORETTA F, "Standing stock of juvenile
brown shrimp, Penaeus aztecus, in Ttexas coastal ponds". . .
SUMMERSON, C.-see PETERSON et al.
81
395
677
Tkxonomy
shrimp, rock 1
TAYLOR, D. M., R. G. HOOPER, AND G. R ENNIS,
"Biological aspects of the spring breeding migration of
snow crab Chionecetes opilio, in Bonne Bay, Newfoundland
(Canada)" 707
THOMAS, DAVID H., "A possible link between coho (silver)
salmon enhancement and a decline in central California
Dungeness crab abundance" 682
Tilefish
abundance and sediment composition off Georgia .... 443
Tbmtate
feeding habits in the South Atlantic Bight 461
TVout, rainbow
otoliths 81
"Ulna fishery
incidental dolphin mortality 521
"Ulna, skipjack
foot habits in the southwestern Atlantic 379
parasite use and fishery implications 343
Ibna, yellowfin
related to dolphin habitats in the Pacific 623
TYLER, ALBERT V.-see OVERHOLTZ and TYLER
"Undersea topography and comparative distributions of two
pelagic cetaceans," by Clifford A. Hui 472
"Using objective criteria and multiple regression models for
age determination in fishes," by George W. Boehlert .... 103
"Variability in dimensions of salmonid otolith nuclei: im-
plications for stock identification and microstructure inter-
pretation," by John D. Neilson, Glen H. Geen, and Brian
Chan 81
"VariabOity, trends, and biases in reproductive rates of spot-
ted dolphins, Stenella attenuata" by Jay Barlow 657
"Vertical distribution of ichthyoplankton off the Oregon
coast in spring and summer months," by George W Boeh-
lert, Dena M. Gadomski, and Bruce C. Mundy 611
"Vertical structure of nearshore plankton off southern
California: a storm and a larval fish food web," by M. M.
Mullin, E. R. Brooks, F. M. H. Reid, J. Napp, and E. F.
Stewart 151
VINTER, BEVERLY M.-see MATARESE and VINTER
"Visual threshold for schooling in northern anchovy, En-
graulis mordax" by John Hunter and Ragan Nicholl .... 235
WAHLEN, BRUCE E., and TIM D. SMITH, "Observer ef-
fect on incidental dolphin mortality in the eastern tropical
Pacific tuna fishery" 521
Walleye
growth and fecundity in the Columbia River 701
WARLEN, STANLEY M., and ALEXANDER J.
CHESTER, "Age, growth and distribution of larval spot,
Leiostomus xanthurvs, off North Carolina 587
WATSON, ALAN P.-see GASKIN and WATSON
WESTPHAL, WILLIAM-see LOVE et al.
Whales, bowhead
behavior in the Beaufort Sea 357
Whales, Pacific pilot
undersea topography and distribution 472
"Within-season differences in growth of larval Atlantic
herring, Clupea harengus harengus" by Cynthia Jones . . . 289
WROBLEWSKI, J. S.-see FLIERL and WROBLEWSKI
WURSIG, BERND, ELEANOR M. DORSEY, MARK A.
FRAKER, ROGER S. PAYNE, and W JOHN RICHARD-
SON, "Behavior of bowhead whales, Balaena mysticetus,
summering in the Beaufort Sea: a description" 357
YOKLAVICH, MARY M.-see BOEHLERT and
YOKLAVICH
Zalophiis californianus—see Sea-lion, California
Zooplankton
vertical structure off southern California .
151
724
NOTICES
NOAA Tfechnical Reports NMFS published during first 6 months of 1985
Technical Report NMFS
19. Synopsis of biological data on the spottail pinfish, Diplodus holbrooki
(Pisces: Sparidae). By George H. Darcy. January 1985, iv + 1 1 p., 8 figs.
20. Ichthyoplankton of the continental shelf near Kodiak Island, Alaska. By
Arthur W. Kendall, Jr., and Jean R. Dunn. January 1985, iii + 89 p.,
5 figs., 7 tables.
21. Annotated bibliography on hypoxia and its effects on marine life, with
emphasis on the Gulf of Mexico By Maurice L. Renaud. February 1985,
iii + 9 p.
22. Congrid eels of the eastern Pacific and key to their leptocephali. By
Solomon N. Raju. February 1985, iii + 19 p., 12 figs., 2 tables.
23. Synopsis of biological data on the pinfish, Lagodon rhomboides (Pisces:
Sparidae). By George H. Darcy. February 1985, iv + 32 p., 22 figs., 24
tables.
24. Tfemperature conditions on the cold pool 1977-81: A comparison between
Southern New England and New York transects. By Steven K. Cook.
February 1985, iii + 22 p., 5 figs., 5 tables, 14 app. figs.
25. Parasitology and pathology of marine organisms of the world ocean. By
William J. Hargis, Jr. (Editor). March 1985, iv + 135 p. [38 papers.]
26. Synopsis of biological data on the sand perch, Diplectrum formosum
(Pisces: Serranidae). By George H. Darcy. March 1985, iv + 21 p., 20
figs., 7 tables.
27. Proceedings of the Eleventh U.S.-Japan Meeting on Aquaculture, Salmon
Enhancement, Ibkyo, Japan, October 19-20, 1982. By Carl J. Sindermann
(Editor). March 1985, iii -i- 102 p. [15 papers.]
28. Review of geographical stocks of tropical dolphins (Stenella spp. and
Delphinus delphis) in the eastern Pacific By William F. Perrin, Michael
D. Scott, G. Jay Walker, and Virginia L. Cass. March 1985, iv -i- 28 p.,
26 figs., 4 tables.
29. Prevalence, intensity, longevity, and persistence ofAnisakis sp. larvae and
Lacistorhynchus tenuis metacestodes in San Francisco striped bass. By
Mike Moser, Judy A. Sakanari, Carol A. Reilly, and Jeannette Whipple
April 1985, iii -i- 4 p., 6 figs.
30. Synopsis of biological data on the pink shrimp, Pandalus borealis Kr^yer,
1838. By Sandra E. Shumway, Herbert C. Perkins, Daniel F. Schick, and
Alden R Stickney May 1985, iv -i- 57 p., 46 figs., 36 tables.
Some NOAA publications are available by purchase from the Superintendent of Documents, U.S.
Government Printing Office, Washington, DC 20402.
ERRATA
Fishery Bulletin, Vol. 82, No. 2
Epperly, Sheryan P., and Walter R. Nelson, "Arithmetic versus exponential calcula-
tion of mean biomass," p. 446-448.
— R + R
Page 446, left column, equation should read: Bt = -
2
Bt {e^'-^' - 1)
Gt -Z,
Page 446, right column, equation should read: Bi =
AAl, left column, line 1, correct to read:
recruit. In one, Bf was computed arithmetically.
Page 447, right column, line 3, correct to read:
F-multiples and ages of entry, when B^ was cal-
Page 447, Figure 1, second line, correct to read:
when dt = 1.0 and Sj = 1.0, DELTA = J?,(5( ^^ - B( ^^^) = B^ * {0.0061 + 0.0037 (G( - Z^)
Page 448, paragraph 1, line 8, correct to read:
ing a need to minimize the G^ - Zi difference if B^
Page 448, paragraph 1, last line, correct to read:
ommend that 5, be calculated exponentially.
U S Po«»l Ssrvic*
STATEMENT OF OWNERSHIP, MANAGEMENT AND CIRCULATION
Required hy 39 U S C J6S5I
1 A. TITLE OF PUBLICATION
Fishery Bui let in
3 FREQUENCY OF ISSUE
Quarterly
IB. PUBLICATION NO.
3A NO OF ISSUES PUBLISHED
ANNUALLY
2. DATE OF FILING
. su
38 ANNUAL SUBSCRIPTION
PRICE
S21,Q0
4 COMPLETE MAILING ADDRESS OF KNOWN OFFICE OF PUBLICATION fSlreet. Ctrv. Cnuntv. State and Z1P*4 Codei iSot pnnteni
Scientific Publications Office, NMFS
7600 Sand Point Way N.E. BIN C15700 (bldg. 1), Seattle, WA 98II5
5 COMPLETE MAILING ADDRESS OF THE HEADQUARTERS OF GENERAL BUSINESS OFFICES OF THE PUBLISHER iSoi pnnieri
National Marine Fisheries Service, NOAA, DOC
2001 Wisconsin Ave., NW , Washington, DC 20235
6. FULL NAMES AND COMPLETE MAILING ADDRESS OF PUBLISHER, EDITOR, AND MANAGING EDITOR (Tha iiem MUST yOT be blank/
PUBLISHER f.Wameand Complete Mailing Address)
Jack McCormicK, Scientific Publications Office, NMFS
7600 Sand Point Way N.E. BIN C15700, Seattle, WA 98115
iOVrOH iNarie and Compleu yifiiliniAtiiiress) u^r-c
Mary FuKuyama, Scientific Publications Office, NMFS
7600 Sand Point Way N.E. BIN C15700, Seattle, WA 98115
MANAGING EDITOR iName and Complete Mailing Address)
Mary Fukuyama, Scientific Publications Office, NMFS
7600 Sand Point Way N.E. BIN C15700, Seattle, WA 98H5
7 OWNER (If owned by a corporation, its name and address must be stated and also immediately thereunder the names and addresses of stockholders
owning or holding J percent or more of total amount of stock If not owned by a corporation, the names and addresses of the individual owners must
be given If owned by a partnership or other unincorporated firm, its name and address, as well as that of each individual must be given. If the publica-
tion IS published by a nonprofit organization, its name and address must be stated.) {Item must be completed.)
FULL NAME
COMPLETE MAILING ADDRESS
department of Commerce
]kth St., NW. Washington. DC 20230
8 KNOWN BONDHOLDERS. MORTGAGEES, AND OTHER SECURITY HOLDERS OWNING OR HOLDING 1 PERCENT OH MORE OF TOTAL
AMOUNT OF BONDS. MORTGAGES OR OTHER SSCUR\r\£S (If therr are none, so state)
FULL NAME
COMPLETE MAILING ADDRESS
None
9. FOR COMPLETION BY NONPROFIT ORGANIZATIONS AUTHORIZED TO MAIL AT SPECIAL R/^TSS (Section 42J 12 DMMonly)
Th* purpoM, function, and nonprofit status of this organization and the exempt status for Federal income tax purposaa (Check one)
E
(1)
HAS NOT CHANGED DURING
PRECEDING 12 MONTHS
D
(21
HAS CHANGED DURING
PRECEDING 12 MONTHS
(If changed, publisher must submit explanation of
change with this statement i
10.
EXTENT AND NATURE OF CIRCULATION
(See instructions on reverse side)
AVERAGE NO. COPIES EACH
ISSUE DURING PRECEDING
12 MONTHS
ACTUAL NO. COPIES OF SINGLE
ISSUE PUBLISHED NEAREST TO
FILING DATE
A, TOTAL NO. COPIES (Net Press Run)
(handled by U.S.
B. PAID AND/OR REQUESTED CIRCULATION Uash DC
1 Sales through dealers and carriers, street vendors anucountet saTeJ
2.2'«I
2,2i4l
«f»e^
ZOijOZ)
2 Mail Subscription
(Paid and/or requested)
C. TOTAL PAID AND/OR REQUESTED CIRCULATION
(Sum of I OBI and I0B2) printed for sqles 800
800
0. FREE DISTRIBUTION BY MAIL. CARRIER OR OTHER MEANS
SAMPLES, COMPLIMENTARY, AND OTHER FREE COPIES
],kU\
\.hk\
E. TOTAL DISTRIBUTION (Sum of C artd D)
Z.Z'tl
2.2'«1
F. COPIES NOT DISTRIBUTED
1. Office use. left over, unaccounted, spoiled after printing
2. Return from News Agents
G. TOTAL (Sum of E, FI and 2-should equal net press run shown in A)
Z.Z'tl
2.2l4l
11.
I certify that the statements made by
me above are correct and complete
SIGNATURE AND TITLE OF EDITOR, PUBLISHER. BUSINESS MANAGER, OR OWNER
PS Form 3526, Julv 1984
(See instruction on revene)
^
77
INFORMATION FOR CONTRIBUTORS TO THE FISHERY BULLETIN
Manuscripts submitted to the Fishery Bulletin will reach print faster if they conform to the following instructions.
These are not absolute requirements, of course, but desiderata.
CONTENT OF MANUSCRIPT
The title page should give only the title of the paper,
the author's name, his affiliation, and mailing address, in-
cluding ZIP code
The abstract should not exceed one double-spaced page
In the text, Fishery Bulletin style, for the most part,
follows that of the U.S. Government Printing Office Style
Manual. Fish names follow the style of the American
Fisheries Society Special Publication No. 12, A List of Com-
mon and Scientific Names of Fishes from the United States
and Canada, Fourth Edition, 1980.
Text footnotes should be typed separately from the text.
Figures and tables, with their legends and headings,
should be self-explanatory, not requiring reference to the
text. Their placement should be indicated in the right-hand
margin of the manuscript.
Preferably figures should be reduced by photography to
5% inches (for single-column figures, allowing for 50%
reduction in printing), or to 12 inches (for double-column
figures). The maximum height, for either width, is 14
inches. Photographs should be printed on high quality or
glossy paper.
Do not send original drawings to the Scientific Editor;
if they, rather than the photographic reductions, are needed
by the printer, the Scientific Publications Office will request
them.
Each table should start on a separate page Consistency
in headings and format is desirable Vertical rules should
be avoided, as they make the tables more expensive to print.
Footnotes in tables should be numbered sequentially in
arable numerals. Tb avoid confusion with powers, they
should be placed to the left of numerals.
Acknowledgements, if included, are placed at the end of
the text.
Literature is cited in the text as: Lynn and Reid (1968)
or (Lynn and Reid 1968). All papers referred to in the text
should be listed alphabetically by the senior author's sur-
name under the heading "Literature Cited." Only the
author's surname and initials are required in the literature
cited. The accuracy of the literature cited is the respon-
sibility of the author. Abbreviations of names of periodicals
and serials should conform to Serial Sources for the BIOSIS
Data Base. {Chemical Abstracts also uses this system, which
was developed by the American Standards Association.)
Common abbreviations and s3mibols, such as mm, m,
g, ml, mg, °C (for Celsius), %, °Iqq, and so forth, should be
used. Abbreviate units of measure only when used with
numerals. Periods are only rarely used with abbreviations.
We prefer that measurements be given in metric units;
other equivalent units may be given in parentheses.
FORM OF THE MANUSCRIPT
The original of the manuscript should be typed, double-
spaced, on white bond paper. Please triple space above
headings. We would rather receive good duplicated copies
of manuscripts than carbon copies. The sequence of the
material should be:
TITLE PAGE
ABSTRACT
TEXT
LITERATURE CITED
TEXT FOOTNOTES
APPENDIX
TABLES (Each table should be numbered with an
arable numeral and heading provided).
LIST OF FIGURES (Entire figure legends)
FIGURES (Each figure should be numbered with an
arable numeral; legends are desired)
ADDITIONAL INFORMATION
Send the ribbon copy and two duplicated or carbon copies
of the manuscript to:
Dr. William J. Richards, Scientific Editor
Fishery Bulletin
Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service, NOAA
75 Virginia Beach Drive
Miami, FL 33149-1099
Fifty separates will be supplied to an author free of
charge and 50 supplied to his organization. No covers will
be supplied.
Contents— Continued
Notes
PETERSON, CHARLES H, R BRUCE DUNCAN, HENRY C. SUMMERSON, and
BRIAN F. BE AL. Annual band deposition within siiells of the hard clam, Mercenaria
mercenaria: consistency across habitat near Cape Lookout, North Carolina 671
SULLIVAN, LORETTA F, DENNIS A. EMILIANI, and K. NEAL BAXTER. Stand-
ing stock of juvenile brown shrimp, Penaeits aztecus, in Tfexas coastal ponds 677
THOMAS, DAVID H. A possible link between coho (silver) salmon enhancement and
a decline in central California Dungeness crab abundance 682
FELDKAMP, STEVEN D. The effects of net entanglement on the drag and power out-
put of a California sea lion, Zalophus califomianns 692
PARSONS, GLENN R. Notes on the life history of the catshark, Scyliorhinus
meadi 695
LIBBY, DAVID A. A comparison of scale and otolith aging methods for the alewife,
Alosa pseudoharengus 696
MAULE, ALEC G., and HOWARD F HORTON. Probable causes of the rapid growth
and high fecundity of walleye, Stizostedion vitreum vitreum, in the mid-Columbia
River 701
TAYLOR, D. M., R. G. HOOPER, and G. R ENNIS. Biological aspects of the spring
breeding migration of snow crabs, Chionoecetes opilio, in Bonne Bay, Newfoundland
(Canada) 707
CREED, ROBERT P., JR. Feeding, diet, and repeat spawning of blueblack herring, Alosa
aestivalis, from the Chowan River, North Carolina 711
Index 717
Notices
NOAA Ibchnical Reports NMFS published during first 6 months of 1985.
• GPO 593-096
11
MBL WHOI LIBRARY
UH n
UA F