^°fcOA
Fishery Bulletin
SrATES & h
r
Vol. 84, No. 1
January 1986
THEILACKER, GAIL H. Starvation-induced mortality of young sea-caught jack
mackerel, Trachurus symmetricus, determined with histological and morphological
methods 1
RENAUD, MAURICE L. Hypoxia in Louisiana coastal waters during 1983: impli-
cations for fisheries 19
LO, N. C. H., and T. D. SMITH. Incidental mortality of dolphins in the eastern tropical
Pacific, 1959-72 27
MIDDLETON, ROBERT W., and JOHN A. MUSICK. The abundance and distribution
of the family Macrouridae (Pisces: Gadiformes) in the Norfolk Canyon area 35
KEIRANS, WALTER J, SIDNEY S. HERMAN, and R. G. MALSBERGER. Differen-
tiation of Prionotus carolinus and Prionotus evolans eggs in the Hereford Inlet estuary,
southern New Jersey, using immunodiffusion 63
HUNT, JOHN H., WILLIAM C. LYONS, and FRANK S. KENNEDY, JR. Effects of
exposure and confinement on spiny lobsters, Panulirus argus, used as attractants
in the Florida fishery 69
BE ACHAM, TERRY D Type, quantity, and size of food of Pacific salmon (Oncorhyn-
chus) in the Strait of Juan de Fuca, British Columbia 77
JONES, CYNTHIA. Determining age of larval fish with the otolith increment tech-
nique 91
MOYLE, PETER B., ROBERT A. DANIELS, BRUCE HERBOLD, and DONALD M.
BALTZ. Patterns in distribution and abundance of a noncoevolved assemblage of
estuarine fishes in California 105
KRYGIER, E. E., and W G. PE ARCY The role of estuarine and offshore nursery areas
for young English sole, Parophrys vetulus Girard, of Oregon 119
STEIMLE, FRANK W, PAUL D. BOEHM, VINCENT S. ZDANOWICZ, and RALPH
A. BRUNO. Organic and trace metal levels in ocean quahog, A rctica islandica Linne,
from the northwestern Atlantic 133
RALSTON, STEPHEN, REGINALD M. GOODING, and GERALD M. LUDWIG.
An ecological survey and comparison of bottom fish resource assessments (submers-
ible versus handline fishing) at Johnston Atoll 141
WILLASON, STEWART W, JOHN FAVUZZI, and JAMES L. COX. Patchiness and
nutritional condition of zooplankton in the California Current 157
JOHNSON, P. T, R. A. MacINTOSH, and D A. SOMERTON. Rhizocephalan infec-
tion in blue king crabs, Paralithodes platypus, from Olga Bay,-Kodiak Island,
Alaska 177
(Continued on back cover)
V
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Fishery Bulletin
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National Marine Fisheries Service, NOAA
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Dr. Edward D. Houde
Chesapeake Biological Laboratory
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Dr. Reuben Lasker
National Marine Fisheries Service
Dr. Donald C. Malins
National Marine Fisheries Service
Dr. Jerome J. Pella
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Fishery BulletirC^
CONTENTS L^22dlHole^Mass.
Vol. 84, No. 1 January 1986
THE IL ACKER, GAIL H. Starvation-induced mortality of young sea-caught jack
mackerel, Trachurus symmetricus, determined with histological and morphological
methods 1
RENAUD, MAURICE L. Hypoxia in Louisiana coastal waters during 1983: impli-
cations for fisheries 19
LO, N. C. H., and T. D. SMITH. Incidental mortality of dolphins in the eastern tropical
Pacific, 1959-72 27
MIDDLETON, ROBERT W., and JOHN A. MUSICK. The abundance and distribution
of the family Macrouridae (Pisces: Gadiformes) in the Norfolk Canyon area 35
KEIRANS, WALTER J., SIDNEY S. HERMAN, and R. G. MALSBERGER. Differen-
tiation of Prionotus carolinus and Prionotus evolans eggs in the Hereford Inlet estuary,
southern New Jersey, using immunodiffusion 63
HUNT, JOHN H., WILLIAM C. LYONS, and FRANK S. KENNEDY, JR. Effects of
exposure and confinement on spiny lobsters, Panulirus argus, used as attractants
in the Florida fishery 69
BEACH AM, TERRY D. Type, quantity, and size of food of Pacific salmon (Oncorhyn-
chus) in the Strait of Juan de Fuca, British Columbia 77
JONES, CYNTHIA. Determining age of larval fish with the otolith increment tech-
nique 91
MOYLE, PETER B., ROBERT A. DANIELS, BRUCE HERBOLD, and DONALD M.
BALTZ. Patterns in distribution and abundance of a noncoevolved assemblage of
estuarine fishes in California 105
KRYGIER, E. E., and W G. PE ARCY The role of estuarine and offshore nursery areas
for young English sole, Parophrys vetulus Girard, of Oregon 119
STEIMLE, FRANK W, PAUL D BOEHM, VINCENT S. ZDANOWICZ, and RALPH
A. BRUNO. Organic and trace metal levels in ocean quahog, Arctica islandica Linne,
from the northwestern Atlantic 133
RALSTON, STEPHEN, REGINALD M. GOODING, and GERALD M. LUDWIG.
An ecological survey and comparison of bottom fish resource assessments (submers-
ible versus handline fishing) at Johnston Atoll 141
WILLASON, STEWART W, JOHN FAVUZZI, and JAMES L. COX. Patchiness and
nutritional condition of zooplankton in the California Current 157
JOHNSON, P. T, R. A. MacINTOSH, and D A. SOMERTON. Rhizocephalan infec-
tion in blue king crabs, Paralithodes platypus, from Olga Bay, Kodiak Island,
Alaska 177
(Continued on next page)
Seattle, Washington
1986
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
WEBER, EARL C, and STEPHEN R. GOLDBERG. The sex ratio and gonad indices
of swordfish, Xiphias gladius, caught off the coast of southern California in
1978 185
UCHIYAMA, JAMES H., RAYMOND K. BURCH, and SYD A. KRAUL, JR. Growth
of dolphins, Coryphaena hippurus and C. equiselis, in Hawaiian waters as determined
by daily increments on otoliths 186
FROST, KATHRYN J., and LLOYD F. LOWRY Sizes of walleye pollock, Theragra
chalcogramma, consumed by marine mammals in the Bering Sea 192
VAN ENGEL, W. A., R. E. HARRIS, JR., and D. E. ZWERNER. Occurrence of some
parasites and a commensal in the American lobster, Homarus americanus, from the
Mid- Atlantic Bight 197
COLLETTE, BRUCE B. Resilience of the fish assemblage in New England tide-
pools 200
JOHNSON, PHYLLIS T Parasites of benthid amphipods: ciliates 204
MASON, J. C. Fecundity of the Pacific hake, Merluccius productus, spawning in
Canadian waters 209
SELZER, LAWRENCE A., GREG EARLY, PATRICIA M. FIORELLI, P. MICHAEL
PAYNE, and ROBERT PRESCOTT Stranded animals as indicators of prey utiliza-
tion by harbor seals, Phoca vitulina concolor, in southern New England 217
WARNER, JOHN, and BOYD KYNARD. Scavenger feeding by subadult striped bass,
Morone saxatilis, below a low-head hydroelectric dam 220
RANCK, CAROL L., FRED M. UTTER, GEORGE B. MILNE R, and GARY B. SMITH.
Genetic confirmation of specific distinction of arrowtooth flounder, Atheresthes stomias,
and Kamchatka flounder, A. evermanni 222
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 ap-
proves, recommends or endorses any proprietary product or proprietary material
mentioned herein, or which has as its purpose an intent to cause directly or indirect-
ly the advertised product to be used or purchased because of this NMFS publication.
Best NMFS Publications for
The Publications Advisory Committee of the
National Marine Fisheries Service has an-
nounced the best publications authored by
the NMFS scientists and published in the
Fishery Bulletin and the Marine Fisheries
Review for 1983. Only effective and inter-
pretive articles which significantly contrib-
ute to the understanding and knowledge
of NMFS mission-related studies are eligible,
and the following papers were judged as the
best in meeting this requirement:
"Seasonal variation in survival of larval
northern anchovy, Engraulis mordax,
estimated from the age distribution of
juveniles" by Richard D. Methot, Jr. appears
in Fishery Bulletin 81:741-750.' Richard D.
Methot, Jr., fishery biologist is from the
Southwest Fisheries Center's La Jolla Labo-
ratory, National Marine Fisheries Service,
NOAA, 8604 La Jolla Shores Drive, La Jolla,
California 92038.
"To increase oyster production in the north-
eastern United States" by Clyde L.
MacKenzie, Jr. appears in Marine Fisheries
Review 45(3): 1-22. Clyde L. Mackenzie, Jr.,
fishery biologist is from the Northeast
Fisheries Center's Sandy Hook Laboratory,
National Marine Fisheries Service, NOAA,
Highlands, New Jersey 07732.
AWAR
STARVATION-INDUCED MORTALITY OF YOUNG
SEA-CAUGHT JACK MACKEREL, TRACHURUS SYMMETRICUS,
DETERMINED WITH HISTOLOGICAL AND MORPHOLOGICAL METHODS
Gail H. Theilacker1
ABSTRACT
Young jack mackerel, Trachurxis symmetricus, living offshore are starving while those living nearshore
are healthy. These results for sea-caught jack mackerel were determined by using histological and mor-
phological criteria that reliably diagnosed the viability of laboratory-raised jack mackerel. Both the
histological and morphological indices indicated that 350 km offshore about 70% of the first-feeding jack i
mackerel were starving. In contrast, 12% of the fish collected near islands and banks were starving. In
both habitats, mortality rates decreased to zero for jack mackerel at 2 weeks of age The accuracy of
the techniques for prediction of the nutritional state of wild larvae is discussed and evaluated.
Jack mackerel, Trachurus symmetricus, hatch with
yolk reserves that last for 5dat 15°-15.5°C. After
the yolk is absorbed, they must eat within 3 d or die
of starvation. In addition, growth is retarded in lar-
vae that have experienced only 1 d of starvation, and
resumption of normal growth does not occur until
2-3 d after the starvation period (Theilacker 1978,
1981). Thus, in the laboratory, availability of food at
the time of first feeding affects growth and survival
of young jack mackerel. In the field, the relative im-
portance of starvation as a source of mortality of
jack mackerel is unknown. It was first suggested by
Hjort (1914) (reviewed by May 1974) that the
strength of the year class is determined early in life
by the availability of food for larvae at the time of
first feeding (the critical period hypothesis). But only
recently (O'Connell 1980) has the presence of
starving ocean-caught larvae been documented. In
this study I give evidence that starvation may be a
major cause of natural mortality of young jack
mackerel at sea. I use two techniques, developed in
the laboratory, to determine the incidence of starva-
tion (Theilacker 1978). The potential use of these
techniques to monitor sea samples for larval survival
is discussed.
METHODS
Collection
In May 1980 a concentration of jack mackerel eggs
and larvae was located 350 km off the coast of
'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA 92038.
Manuscript accepted February 1985.
-mr""1"" ",TT 1 cmm t™ aj Ufl i mag
California (lat. 31°00'N and long. 120°30'W). A 400
mi2 grid was established which contained 41 sta-
tions, 4 mi apart; it took 4 d to sample all stations
(Fig. 1). At each station, a standard oblique bongo
net tow (Smith and Richardson 1977) and aim net
sample were taken. The bongo samples will be used
in another study to estimate growth and mortality
of jack mackerel larvae (Hewitt et al. in press). The
1 m net (505 /urn mesh) was used to sample larvae
qualitatively from the upper 50 m of water. Ahlstrom
(1959) found that 88% of the larval jack mackerel
collected off California were in the upper 50 m, and
all the jack mackerel collected by Devonald (1983)
were above 42 m. A special collection procedure was
used for the samples taken for histological and mor-
phological analyses. Immediately after the net tow,
the sample was preserved in Bouin's solution to avoid
autolysis of larval tissues (elapsed time was usually
8 min) (Theilacker 1978). The collecting net was not
washed down (a procedure required for quantitative
samples), and the cod end containing the sample was
placed directly into Bouin's solution. The preserved
sample was removed from the cod end within an
hour. After 2 d, Bouin's solution was replaced by 70%
alcohol.
In addition to jack mackerel collections taken in
the open ocean 350 km offshore, a few special tows
(n = 24) for assessment of starvation were made dur-
ing routine cruises in 1978, 1979, and 1980 near the
Channel Islands (Anacapa, Santa Barbara, and San
Clemente) and Tanner Bank.
Preparation of Fish
More than 2,000 jack mackerel were collected in
1
FISHERY BULLETIN: VOL. 84. NO. 1
Los Angeles
Anacapa
Santa Barbara-
San Clemente
Tanner Bank— o
San Diego _
31* N —
Figure 1— Location of jack mackerel, Trachurus symmetricus, col-
lections off the coast of California. Nearshore stations were at
Anacapa, Santa Barbara, and San Clemente Islands and at Tan-
ner Bank. The grid of open-ocean stations was 350 km offshore;
stations were 4 mi apart.
samples taken offshore; from 0 to 262 fish were
caught per sample (Table 1). Larvae sorted from the
samples (n = 445) were counted and five body
measurements taken: standard length (SL, tip of up-
per jaw to perpendicular at end of notochord); head
length (HL, tip of upper jaw to cleithrum); eye
diameter (ED); body depth at the pectoral (BD-1);
and body depth at the anus (BD-2). After measure-
ment, some larvae (n = 369) were prepared for
histological examination. When samples contained
fewer than 50 jack mackerel, most larvae were ex-
amined, but when samples contained more than 100
jack mackerel, about 25% of the fish were examined
histologically. Jack mackerel size distribution in the
offshore study area (determined for 400 fish taken
from stations 16, 23, 34, and 35) was similar among
stations and ranged between 2.6 and 4.7 mm SL. lb
ensure analysis of all ages in the larger samples, fish
were taken equally from each of four length classes:
<3.0; 3.0-<3.5; 3.5-<4.0; 4.0-<5.0 mm. These larvae
were imbedded in paraffin, sectioned at 6 pm, and
stained with Harris hematoxylin and eosinphloxine
B (Theilacker 1978). In my analysis of histological
data I combined the first two size classes because
the size at first feeding was 3.2 mm.
The prevalence of starvation was assessed for 371
jack mackerel selected from 20 of the 32 positive sta-
tions (Table 1). In addition, I analyzed 41 jack
mackerel taken in 14 hauls from the inshore stations
near the Channel Islands and Tanner Bank.
Histological Analysis
The histological assessment of nutritional state is
based on distinct cellular changes that occur in
tissues when larval jack mackerel were deprived of
food; these changes are well documented by Umeda
and Ochiai (1975), O'Connell (1976), and Theilacker
(1978). Tb determine the condition of individual
ocean-caught jack mackerel, I used the histological
criteria I developed in the laboratory by starving jack
mackerel except I did not grade the pancreas. Grades
were assigned to 11 histological characteristics of
the brain, digestive tract, liver, and musculature
(Theilacker 1978, 1981). Fish identities were
unknown during this examination. I classified jack
mackerel larvae into four categories (healthy,
recovering, starving, and dying) according to their
histological scores (the summation of the grades for
each of the 11 histological characteristics).
Tissues of jack mackerel from the sea which had
tissues similar in appearance to the tissues of
feeding, laboratory-raised fish were classified as
healthy; sea-caught jack mackerel which resembled
laboratory fish that had fasted before eating were
classified as recovering (these fish showed signs of
feeding and digestion, but also showed signs of star-
vation); sea-caught larvae which were classified as
starving resembled larvae that had been starved in
the laboratory for 1-3 d (Theilacker 1978, 1981). I
did not observe the dying category in laboratory-
starved larvae; this category is described in Results.
Morphological Analysis
Tb detect starvation I used a set of morphological
THEILACKER: MORTALITY OF SEA-CAUGHT JACK MACKEREL
Table 1.— Number of jack mackerel collected and the condition of those that were ana-
lyzed histologically.
tation
Number of fish
s
Starv-
Recover-
No.
Sampled
Analyzed
Dying
ing
ing
Healthy
Offshore
1
0
0
2
2
1
0
0
1
0
3
0
0
4
2
0
5
0
0
6
0
0
7
2
1
0
1
0
0
8
2
2
0
0
2
0
9
1
1
1
0
0
0
10
0
0
11
3
3
3
0
0
0
12
0
0
13
1
0
14
1
0
15
>200
0
16
>200
0
17
20
13
0
8
5
0
18
>125
0
19
43
35
7
0
1
27
20
242
64
8
19
13
24
21
>250
0
22
>175
0
23
150
32
1
0
4
27
24
1
0
25
23
0
26
4
3
3
0
0
0
27
0
0
28
262
58
3
36
14
5
29
11
11
1
4
4
2
30
250
57
4
13
18
22
31
32
9
7
1
0
1
32
109
25
0
2
20
3
33
31
23
1
3
10
9
34
38
0
35
43
0
36
31
24
3
4
1
16
37
7
5
2
1
2
0
38
2
2
1
0
0
1
39
0
0
40
1
0
41
0
0
Total (Offshore)
>2,264
369
45
92
95
137
Around Islands
Anacapa
12
12
0
1
0
11
Santa Barbara
3
3
0
0
2
1
San Clemente
17
17
0
1
5
11
Tanner
Bank
9
9
0
1
0
8
Total
(Nearshore)
41
41
0
3
7
31
characteristics that successfully diagnosed the ex-
tent of starvation in 85% of the laboratory-reared
jack mackerel (Theilacker 1978). The technique is
based on a stepwise discriminant analysis (SWDA)
using 11 body part measurements. The analysis
allowed me to distinguish between individuals
belonging to fed and starved treatments, given a set
of morphological measurements that describe the
characteristics of the individuals in each feeding
treatment. The 11 body part measurements used to
distinguish between groups of fed and starved jack
mackerel were 1) head length, 2) eye diameter, 3)
body depth at the pectoral, 4) body depth at the
anus, 5) head length/standard length, 6) eye
diameter/standard length, 7) body depth at the pec-
toral/standard length, 8) body depth at the anus/
standard length, 9) eye diameter/head length, 10)
body depth at pectoral/head length, and 11) body
depth at anus/head length. Standard length was used
in the ratios but not as a unit to allow discrimina-
tion between feeding and starving fish of the same
length.
FISHERY BULLETIN: VOL. 84, NO. 1
Adjustment for Shrinkage
® In order to use morphological measurements to
diagnose starvation of jack mackerel, it is essential
to adjust for shrinkage of body measurements. Both
handling and preservation cause shrinkage of lar-
val fishes, and the amount of shrinkage varies among
body parts. Final fish size is dependent not only on
initial size but also on the handling time (which is
different for the laboratory and the field) and the
type of preservative used (Blaxter 1971; Theilacker
1980a; Hay 1981). The shrinkage of laboratory speci-
mens of jack mackerel preserved in Bouin's solution
is known (Theilacker 1980a), but for field-collected
specimens the shrinkage caused by the net tow and
the subsequent effect of Bouin's preservative must
be evaluated.
I conducted laboratory experiments to estimate
the amount of shrinkage caused by handling (net
retention) and by preservation. Live jack mackerel
were pipetted individually (time = 0) onto a slide,
and four body measurements were taken before
placing the fish into a net container through which
15°C seawater circulated. Standard length, head
length, eye diameter, and body depth at the anus
were measured. Body depth at the pectoral fin was
not measured because it was difficult to measure
quickly on live jack mackerel. During net treatments,
I usually remeasured each fish four more times at
5-7 min intervals, replacing the fish in the net be-
tween each set of measurements. After 25-30 min,
the fish were preserved in either Bouin's fixative
(used for histological analyses) or 5% buffered
Formalin2 (as per shipboard procedures; Smith and
Richardson 1977). Remeasurements after preserva-
tion were taken in 3-4 wk.
(a\ Shrinkage of net-captured larval fish has been
shown to decrease with increasing fish size For ex-
ample, shrinkage of northern anchovy decreased
from 19% at 4 mm SL to 8% at 18 mm SL
(Theilacker 1980a). The jack mackerel tested in this
study ranged between 3.35 and 4.10 mm SL, and
within this restricted length group shrinkage was
proportional to size Thus for the shrinkage analy-
ses, all jack mackerel were combined into one
group.
For the combined size group, length of the jack
mackerel body (Fig. 2) and the head continued to
shrink for the duration of the net treatment. Width
of the body (Fig. 3) and the eye shrank initially, and
then remained relatively constant during additional
treatment. To account for positive correlation be-
tween body parts, a multivariate analysis (Table 2)
was used to relate the ratio of net-treated size to live
size (for each body part) with treatment time In-
dividual shrinkage was highly variable; for example,
shrinkage of body depth varied between 0 and 23%
for treatment times between 5 and 20 min (Fig. 3).
However, since these were the best estimates of
average shrinkage for body parts, the regressions
(Table 2) were used to calculate the adjustment fac-
tors needed for this study. Factors for each body part
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0.0
6.0
12.0 18.0
TIME (MIN)
24.0
30.0
Figure 2— Shrinkage of standard length, shown as the ratio of net-
treated size to live size, of individual Trachurus symmetricus lar-
vae as a function of net-treatment time; estimated parameters are
in Table 4.
1.0
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TIME (MIN)
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2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Figure 3— Shrinkage of body depth, shown as the ratio of net-
treated size to live size, of individual Trachurus symmetricus lar-
vae as a function of net-treatment time; estimated parameters are
in Thble 4.
THEILACKER: MORTALITY OF SEA-CAUGHT JACK MACKEREL
$
Table 2.— Shrinkage of jack mackerel larvae. Parameters estimated from multi-
variate linear equations relating the ratio of the net-treated size of a mackerel body
part to its live size (y) with the net-treatment time (x).
Net-treated size/
live size1
(SE)
(SE)
pz
Standard length (SL)
Head length (HL)
Eye diameter (ED)
Body depth (BD-2)
1.0109 (0.0117)
0.9281 (0.0157)
0.9360 (0.0168)
0.8980 (0.0177)
-0.0105 (0.0008)
-0.0038 (0.0011)
-0.0027 (0.0012)
-0.0014 (0.0013)
<0.001 0.66
0.001 0.12
0.031 0.06
0.280 0.02
1n = 89.
Probability that slopes differ from zero.
were calculated by 1) combining the shrinkage ratio
at 8 min (average elapsed time for field collections,
see Methods) with 2) the average shrinkage in
Bouin's preservative after the net treatment, and 3)
comparing the combined shrinkage with results from
shrinkage determined in the laboratory study
(Theilacker 1980a; Table 3). Also given in Table 3 are
average shrinkage ratios calculated for specified time
intervals.
Adjustment factors for standard length, head
length, and eye diameter (Table 3) support the view
that shrinkage of field-collected fishes is greater than
shrinkage of fishes preserved in the laboratory.
Shrinkage of BD-2 was an exception to this pattern,
however, as less shrinkage occurred under simulated
field conditions (20-23%) than in the laboratory
(25%). I (Theilacker 1980a) reported a similar
paradox for northern anchovy where simulated-field
net treatments caused 8% shrinkage of BD-2 as com-
pared with 10% shrinkage for standard laboratory
preservation. Jack mackerel shrinkage was greater
in Bouin's solution than in Formalin, results which
are consistent with studies on northern anchovy.
Also, as with northern anchovy, Formalin preserva-
tion caused a slight increase in the size of the jack
mackerel eye (Table 3).
I adjusted the body measurements of the ocean-
caught jack mackerel with the shrinkage factors
(ratio R8, Table 3). Use of these adjustments should
equate the morphology of preserved, ocean-caught
jack mackerel (this study) with the morphology of
preserved, laboratory-raised jack mackerel that were
used to develop the morphological SWDA (see
Methods: Morphological Analysis). It was necessary
to reestimate the SWDA function for this study,
although nearly the same analysis was made
previously (Theilacker 1978). A new estimate was re-
quired because pectoral body depth was not included
in the shrinkage measurements in this study; hence,
an SWDA function that excluded this measurement
was needed. Elimination of pectoral body depth from
the analysis reduced the level of predictability from
85% to 78%. This new function was used here to
classify the condition of ocean-caught jack mackerel
Table 3.— Shrinkage of jack mackerel larvae1. Treatment ratio (R) is treated size
divided by previous size (1.00 = no shrinkage).
Ratios
Treatment
Mean
Standard
Head
Eye
Body
ratio
R
n
time
length
length
diameter
depth
8 min net/live size
2«1
89
8
0.93
0.90
0.91
0.89
5-10 min net/live size
Ro
36
7.3
0.94
0.90
0.92
0.89
11-15 min net/live size
R,
22
12.6
0.87
0.88
0.88
0.86
16-28 min net/live size
a,
27
19.4
0.81
0.86
0.89
0.88
Bouin's fixative/
net-treated size
3fls
15
—
0.91
0.84
0.93
0.91
Formalin fixative/
net-treated size
3««
13
—
0.96
0.93
1.08
0.91
Laboratory-preserved
in Bouin's fixative
live size
4*7
45
—
0.92
0.82
0.90
0.75
Calibration factor
= R7IR,xR5
5*8
—
—
1.09
1.08
1.06
0.93
1Range in standard length 3.35-4.10 mm.
Calculated from regression (Table 2); ocean-caught fish preserved within 8 min; see text.
Shrinkage in fixative after net treatment.
"Data from Theilacker (1980a).
Adjustment factor to equate measurements of field-collected mackerel (this study) with
measurements of laboratory-raised mackerel (Theilacker 1978).
FISHERY BULLETIN: VOL. 84, NO. 1
after the size of their body parts was adjusted for
shrinkage.
RESULTS
Habitat Conditions
A larval-density gradient was apparent in the open
ocean study area. High densities of jack mackerel
larvae (100-<300/sample) were found in the central
stations and in stations near the western boundary
of the grid; lower densities (20-50) were found to the
north and east, and densities of larvae approached
zero at the southern stations that were occupied at
the beginning and again at the end of the 4-d obser-
vation period (Fig. 4). Larval densities in the south
did not change during this period.
The study area was chosen because temperature,
viewed on satellite thermal image of the sea surface,
corresponded to the temperature range (15°-16°C)
associated with jack mackerel spawning (Farris
1961). Surface temperature in the study area in-
creased from 15.2°C in the north to 16.8°C at the
southern stations, with the majority of jack mackerel
found in water temperatures of 16.1°-16.6°C.
Water temperatures inshore of the grid were about
14°C.
A temperature-salinity curve obtained at station
19 (Fig. 1) agreed well with the curves obtained from
inshore stations with the exception of the warm-
water portion of the curve, which appeared to be a
thin, warm lens of open ocean water intruding coast-
ward over deeper coastal water.
Histological Assessment of
Fish Condition
I used the tissue characteristics of laboratory fish
(raised at 15.0° -15.5° C) of known feeding history as
the criteria to determine the nutritional condition
of the sea-caught jack mackerel. Photomicrographs
of the diagnostic tissue characteristics were
documented by Theilacker (1978). Many of these
characteristics are shown also for wild fish (Fig. 5,
see also Figures 6-14). In addition, the wild fish ex-
hibited four tissue conditions that were not observed
in the laboratory: lesions in the brain; luminal
vacuoles in the midgut; total degeneration of the
midgut mucosal cells; and a wavy configuration of
the muscle fibers. Each of these conditions will be
considered in the following section that describes the
tissues of ocean-caught fish. My emphasis will be on
those tissue characteristics that diagnose starvation
in young jack mackerel.
Brain
The brain of an ocean-caught jack mackerel was
considered normal when the neurons were distinct,
round, and closely spaced. In these fish, brain cell
division was common, but it was not graded. One
percent of the jack mackerel examined had brain le-
sions of the type (Fig. 6) induced by ultraviolet light
in larval northern anchovy, Engraulis mordax, and
Pacific mackerel, Scomber japonicus (Hunter et al.
1979). The grading system classified these jack
mackerel (n = 3) into the healthy category. In a
^Pt. Conception
'O^s? ~"*a*fcl_os Angeles
'San Diego
31» N • —
120.5* W
NUMBER OF LARVAE
0-5
20-50
100-<300
Figure \.—Trachurus symmetricus larval density gradient shown
as number of larvae collected per sample (not quantitative). Sta-
tion grid located 350 km off the coast of California.
THEILACKER: MORTALITY OF SEA-CAUGHT JACK MACKEREL
single specimen, lesions were present not only in the
brain but throughout the spinal cord (Fig. 7) as well.
In addition, the gut and associated glands had
deteriorated to the extent that this fish was con-
sidered starving.
An abnormal central nervous system of a jack
mackerel larva consisted of vacuolar degeneration
and shrinkage of neurons. The degenerating neurons
exhibited increased staining (Fig. 8).
Digestive Track and Associated Glands
The midgut mucosa of young jack mackerel is com-
posed of a single layer of columnar epithelial cells.
Older fish (3.7-4.0 mm) showed increased mitotic ac-
tivity in the basal layer. Microvilli bordered the
midgut lumen only in fish that appeared healthy.
Mucosal cells were closely united in the fish con-
sidered to be normal (Figs. 9, 10). Basal separations
between these cells were common, not only in fish
that appeared to be starving but also in fish that
showed signs of feeding and digestion (Fig. 11).
O'Connell (1980) also reported that sea-caught north-
ern anchovy exhibited basal separations between
mucosal cells while the apical portions were well
joined.
All wild jack mackerel categorized as recovering
had basal separations between midgut mucosal cells.
Laboratory fish that were artificially starved for 1-2
d before feeding showed these separations for several
days after feeding resumed. In the laboratory, lar-
vae did not grow while their tissues were regen-
erating (Theilacker 1981).
Many sea-caught jack mackerel of all ages had
intracytoplasmic vacuoles in the midgut epithelium.
Basal and membrane lined, these vacuoles resem-
bled the vacuolar condition found in some recover-
ing, laboratory fish (Theilacker 1981). In addition,
many sea-caught larvae had smaller, luminal
vacuoles that were found in the laboratory fish (Fig.
12). These luminal vacuoles may indicate a degen-
erative condition. In higher vertebrates a metabolic
imbalance can cause vacuolar degeneration. Vacuola-
tion appears first as numerous small, clear vacuoles
dispersed throughout the cytoplasm. As the condi-
tion becomes more severe, these minute vacuoles
coalesce to form large (sometimes single) clear
spaces that displace the nucleus (Anderson 1971).
On the other hand, the numerous luminal vacuoles
can secrete mucous into the lumen or store fat. Use
of a routine mucicarmine staining was negative for
the presence of mucous cells. Unfortunately, the
presence of fat in the vacuoles could not be tested
because fat is removed during tissue preparation by
clearing agents. Neither vacuolar condition was
graded.
Another unusual condition of the midgut occurred
in many of the smaller wild jack mackerel. In these
fish, the margin of the lumen had lost its integrity,
microvilli were absent, and the sloughing of the
mucosal cells into the lumen (a condition common
in starved laboratory jack mackerel) appeared to
have progressed until the lumen contained masses
of undefinable, cellular material (Fig. 13). O'Connell
(1980) described a comparable condition which he
found in the midgut of a single, northern anchovy
specimen, the smallest examined. All jack mackerel
exhibiting this condition were smaller than the size
attained at first feeding, indicating shrinkage had
occurred. The hindgut also contained necrotic debris,
and other diagnostic tissues were in poor condition.
These jack mackerel were classified as dying.
Hindgut mucosal cells of wild jack mackerel
typically showed eosin-staining inclusions that are
reported to be sites of intracellular digestion (Iwai
1968, 1969; Iwai and Tanaka 1968; Watanabe 1981).
Inclusions in the wild jack mackerel varied in inten-
sity; in healthy specimens the intensity appeared to
be related to time of day (feeding period), increasing
during daylight hours and decreasing during the
night. Although the presence and intensity of hind-
gut inclusions were noted, they were not graded.
Inclusions were not present in larval teleosts de-
prived of food in the laboratory (Theilacker 1978;
Umeda and Ochiai 1975; O'Connell 1976). However,
in many wild jack mackerel showing signs of starva-
tion the presence of pale inclusions indicated that
the fish had eaten at some time in the past.
The key diagnostic characteristics of the pancreas
were obscure in ocean-caught jack mackerel because
of the intensity of staining. In laboratory fish, the
pancreas was very sensitive to food deprivation. For
example, a breakdown in the symmetry of the acinar
secretory unit was detectable after 1 d of food
deprivation (Theilacker 1978). In the wild fish, the
intensity of the staining of the pancreas was difficult
to control (see Fig. 12), and I was not able to obtain
consistent results, hence the condition of the pan-
creas was not evaluated.
The jack mackerel liver was considered normal
when hepatocytes had clear, distinct nuclei (Fig. 9).
The appearance of the cytoplasm was quite variable;
in some larvae very few intracellular spaces existed
in the cytoplasm of the hepatocytes whereas in
others extensive intracellular spaces existed.
Presumably these spaces are areas where glycogen
and fat are stored within the cell. This presumed in-
corporation of stores was most marked in healthy
FISHERY BULLETIN: VOL. 84, NO. 1
mitotic
notochord
swim brain
muscle bladder
Figure b— Trachurus symmetricus larva, 3.75 mm SL. All 11 histological criteria graded as healthy. Bar = 281 ^m.
Figure 6— Head of Trachurus symmetricus larva graded healthy. Mitotic activity and the location of brain lesions are indicated. Bar
= 47 \im. B = brain.
Figure 1— Trachurus symmetricus larva graded as starving. Lesions present throughout brain and spinal cord. Bar = 47 ^m. B =
brain, N = notochord.
Figure 8— Pectoral area of a dying Trachurus symmetricus larva showing darkly stained primitive nerve cells, wavy muscle fibers, necrotic
and atrophied liver, and loss of integrity of midgut mucosal cells. Bar = 47 ^m. FG = foregut, L = liver, m = muscle, MG = midgut,
N = notochord, SB = swim bladder, SP = spinal cord.
Figure 9— Pectoral area of healthy Trachurus symmetricus larva collected offshore showing parallel muscle fibers and abundant inter-
muscular tissue, distinct nuclei in liver and midgut, and good cellular integrity. Note deflating swim bladder. Bar = 47 ^m. FG = foregut,
IM = intermuscular tissue, L = liver, M = muscle, MG = midgut, N = notochord, P = pancreas, SB = swim bladder.
Figure 10— Pectoral area of healthy Trachurus symmetricus larva collected near San Clemente Island showing abundant glycogen reserves
in the liver. Bar = 47 y.m. FG = foregut, L = liver, M = muscle, MG = midgut, N = notochord, P = pancreas, SB = swim bladder.
8
THEILACKER: MORTALITY OF SEA-CAUGHT JACK MACKEREL
jack mackerel collected near islands and banks (Fig.
10) whereas healthy jack mackerel collected offshore
showed moderate to little storage (Fig. 9).
At the other end of the grading scale, the shrunken
livers of jack mackerel considered to be starving con-
tained darkly stained hepatocytes composed of even-
ly stained cytoplasm with indistinct, irregular nu-
clei.
Musculature
Healthy muscle tissue in jack mackerel had the
following characteristics: few spaces between the
muscle fibers; distinct and parallel, striated myo-
fibrils; and abundant, basophilic and nucleated intra-
muscular tissue (Fig. 9). Nourishment was con-
sidered inadequate in fish exhibiting separated (Figs.
11, 14) and hyaline muscle fibers (Fig. 13) and a
reduction (Figs. 11, 14) or absence (Fig. 13) of intra-
muscular tissua In some sea-caught jack mackerel,
muscle fibers were wavy (Fig. 8). Presence of wavy
muscle fibers in wild fish was considered abnormal
because it was always associated with the poor con-
dition in the other diagnostic tissues, but this charac-
teristic was not used in classification. In starved
laboratory fish, nonparallel fibers were reported
(Theilacker 1978, 1981), but the wavy pattern was
unusual. There were fish with intermediate spaces
between muscle fibers that, according to the scores
of the other diagnostic tissues, appeared healthy. The
Figure 11.— Trachurus symmetricus larva graded recovering. Prominent separations between midgut and hindgut epithelial cells, slight
muscle fiber separation and intermediate intermuscular tissue containing distinct nuclei. Bar = 47 \im. HG = hindgut, IM = inter-
muscular tissue, M = muscle, MG = midgut, N = notochord.
Figure 12— Healthy Trachurus symmetricus larva showing luminal vacuoles in the midgut. This histological characteristic was not
graded. Bar = 47 ^m. M = muscle, MG = midgut.
Figure 13.— -Trachurus symmetricus larva graded dying. No intermuscular tissue; hyaline muscle fibers; total degeneration of midgut
mucosa. Bar = 34 ^m. HG = hindgut, M = muscle, MG = midgut.
Figure 14— Recovering Trachurus symmetricus larva showing slight muscle fiber separation and slight reduction of intermuscular
tissue Bar = 47 \im. HG = hindgut, IM = intermuscular tissue, M = muscle, MG = midgut, N = notochord.
FISHERY BULLETIN: VOL. 84, NO. 1
grading system usually classified these fish into the
recovering category.
General Histological Observations
In jack mackerel that were considered healthy,
swim bladder inflation was first noted at 3.4 mm.
Swim bladders were inflated in larvae taken at night
whereas they were deflated in those taken in the day.
The swim bladders of 72% of the fish were deflated
by 0700 (n = 81) except for fish scored in the
starving category where inflation was common at
any time of day, which was possibly a symptom of
starvation or an additional energy-sparing func-
tion of the swim bladder (Hunter and Sanchez
1976).
Theilacker (1978) pointed out that the gallbladder
was always enlarged in jack mackerel that were
deprived of food in the laboratory, and this condi-
tion occurred in sea samples of starved larvae taken
in the day. On the other hand, gallbladder enlarge-
ment was also found in the healthy fish as well as
starved fish collected at night. According to Love
(1970), the gallbladder discharges its contents when
stimulated by food. Jack mackerel do not eat at
night, so the gallbladder of healthy fish may remain
distended during the night. Thus enlargement of the
gallbladder was not used to diagnose starvation.
Theilacker's (1978) samples of fed and unfed fish
were taken only during the day, when feeding oc-
curs.
Mitotic figures in the brain of jack mackerel oc-
curred in fish collected at all times of day and night.
On the other hand, mitosis of mucosal cells in the
midgut was restricted to the night. It seems that
mucosal cells of northern anchovy also divide late
at night, when the digestive tracts are empty (O'Con-
nell 1981).
- Evidence for Starvation in the Sea
s
Results of the histological analysis showed that
starvation was a major source of mortality for the
smallest jack mackerel larvae (<3.5 mm) as 59% ap-
peared to be dying of starvation, 23% were eating
but had fasted previously, and only 19% were class-
ed as healthy. The incidence of starving larvae
decreased to 16% in the 3.5-4.0 mm size class and
was 3% in the older larvae (Table 4). The numbers
of fish used for the histological assessment of star-
vation was adequate for the smallest (<3.5 mm SL)
larval size class (coefficient of variation ranged be-
tween 0.09 and 0.15 for the four condition
categories), but larger samples would be needed to
give a reliable estimate of the fraction starving for
the older larvae (>3.5 mm SL) because of the low
incidence of starvation.
Despite the fact that jack mackerel abundance
decreased from west to east and north to south (Fig.
4), I found no consistent differences in the incidence
of starvation between fish taken from areas of high
larval density and those taken from areas of low lar-
val density (Fig. 15). Therefore, to estimate mortality
due to starvation, I combined all samples collected
in the offshore area. To estimate mortality rates on
a daily basis, the observed number of fish belong-
Table 4. — Histological condition of jack mackerel collected 350 km off the coast
of California.
<fi
<r
^
&1
£? 4? ^
^
'Number dying/d + starving/d
Total
2Number dying/d
Total
Daily percent
Starving1 Dying2
Yolk sac
—
—
—
15
15
0
0
<3.5 mm
Number
43
74
45
38
200
Duration (d)
1
3
2
6
Number/d
43
24.7
22.5
6.3
96.5
70
45
3.5<4.0 mm
Number
2
16
38
54
110
Duration (d)
1
3
2
3.3
Number/d
2
5.3
19
16.4
42.7
17
5
4.0-<4.5 mm
Number
0
2
12
45
59
Duration (d)
—
3
2
3.3
Number/d
—
0.7
6
13.6
20.3
3
0
10
THEILACKER: MORTALITY OF SEA-CAUGHT JACK MACKEREL
ing to each size and health category was divided by
the duration— the number of days jack mackerel are
expected to remain in each category (Table 4). Dura-
tions spanned 1 to 6 d depending on age and condi-
tion. For healthy fish, duration is simply the size-class
interval divided by the growth rate Healthy fish
belonging to the smallest size group (<3.5 mm) grow
at 0.05 mm/d (Theilacker 1978) and begin to eat at
3.2 mm SL. Thus duration for this size interval (0.3
mm) was 6 d. Growth rate for older fish was 0.15
mm/d; the rate was determined for this study by
counting daily growth increments in otoliths (Hewitt
et al. in press). The duration that a larva remains
in one of the starvation states is a function of the
persistence of the histological criteria. Young jack
mackerel deprived of food in the laboratory show
signs of starvation for 3 d before dying, and larvae
recovering from a period of starvation show these
signs for 2 d (Theilacker 1978, 1981). Older fish may
be more resistant to starvation, but as I had no in-
formation for older jack mackerel, I used the dura-
tions for younger larvae
For the smallest jack mackerel living 350 km off-
shore, 45% were dying of starvation per day. Daily
mortality dropped rapidly to 5% to zero for older
larvae (Table 4). Increasing the durations for the
older larvae in the starving and recovering
categories (Table 4) decreases this estimate of daily
mortality.
Results of the histological examination of jack
mackerel collected near islands and banks allow a
preliminary assessment of the effects of different
100 r
o
z
>
cc
<
</)
»-
z
UJ
o
DC
1U
a
80 -
60
40 -
20
• 31
"37
• 28
► 38
^•29
• 36
• 20
• 30
- »33
I
• 19
•32 23
I 1 1
I l 1
0 50 100 150 200 250 300 350
NUMBER OF JACK MACKEREL COLLECTED
Figure 15— Percentage of starving Trachurus symmetricus lar-
vae (number starving/number analyzed) related to the number of
larvae collected at each offshore station; station number is
indicated.
habitats on starvation (Table 5; Fig. 16). A large dif-
ference existed in the daily larval mortality caused
by starvation between the open ocean and island and
bank habitats. In areas near the islands, none of the
lying of starvation whereas
first-feeding larvae were
45% from the open ocean were dying of starvation.
/&7 In addition, healthy larvae taken near islands were
\s apparently more fit than healthy larvae captured in
the open ocean, as the larvae from the island habitats
had abundant quantities of glycogen in the liver (Fig.
10), whereas livers of larvae from the open ocean
rarely contained glycogen stores (Fig. 9). This in-
dicates that food must have been much more abun-
dant in the island habitat because not only were
fewer fish starving but the healthy fish were able
to store glycogen. The healthy fish from the open
sea may have been just able to meet their daily
metabolic requirements.
The morphological data gave essentially the same
results as did the histological method. On the basis
of morphometric evidence, 70% of the first-feeding
jack mackerel (<3.5 mm SL) were starving and the
number decreased to zero for older jack mackerel
(Table 6). Although the results were similar, the mor-
phological categories used to classify the fish were
different from the histological ones. In particular,
there was no morphological category for dying fish.
For the morphometric SWDA, larvae were grouped
by feeding treatment (Table 6), and the histological
categories (Table 4) were based on the dominant lar-
val tissue conditions determined to characterize a
nutritional state. Thus the morphometric SWDA
cannot be used to estimate the number of larvae
dying per day due to starvation.
DISCUSSION
Larval Starvation and Recruitment
Both histological and morphological criteria in-
dicate that starvation is probably a major source of
larval jack mackerel mortality at the time of first-
feeding but that the survivors of this 6-d period are
much less vulnerable to starvation. Prey (mainly
young stages of copepods) are more abundant at the
nearshore islands and banks off the coast of Califor-
nia than offshore (Beers and Stewart 1967, 1970; Ar-
thur 1976, 1977; Devonald 1983), and survival of
first-feeding jack mackerel was higher in the near-
shore habitats than offshore Thus selection of
spawning sites may have a great effect on survival.
Eggs and larvae of jack mackerel are very widely
distributed; they occur from Baja California to
British Columbia and up to 400 mi off the coast of
©
ii
FISHERY BULLETIN: VOL. 84, NO. 1
Table 5. — Histological condition of jack mackerel collected near islands and banks
off the coast of California.
<fi
<&
* / & *
^ J? 4? jr <*
*w «P~
Daily percent
Starving1 Dying2
Yolk sac
—
—
—
—
0
<3.5 mm
Number
0
2
6
12
20
Duration (d)
1
3
2
6
Number/d
—
0.7
3
2
5.7
12
0
3.5-<4.0 mm
Number
0
1
1
12
14
Duration (d)
1
3
2
3.3
Number/d
—
0.3
0.5
3.6
4.4
7
0
4.0-<4.5 mm
Number
0
0
0
7
7
Duration (d)
1
3
2
3.3
Number/d
—
—
—
2
2
0
0
'Number dying/d + starving/d
Total
2Number dying/d
Total
Table 6.-
-Predicted condition of field-collected jack mackerel larvae determined
with the morphometric technique.
<3V
^
Daily percent
<b
\
<£■
Starving1
<3.5 mm
Number
48
66
150
264
Duration (d)
22
2
6
Number/d
24
33
25
82
70
3.5-<4.0 mm
Number
0
1
121
122
Duration (d)
2
2
3.3
Number/d
—
0.5
36.7
37.2
1.3
4.0-<4.5 mm
Number
0
0
59
59
Duration (d)
2
2
3.3
Number/d
—
—
17.9
17.9
0
2Number starved/d
Total
2Unfed jack mackerel larvae die in 4 d.
California and up to 1,000 mi off Oregon and Wash-
ington (reviewed by MacCall and Stauffer 1983). In
addition, jack mackerel have a protracted spawning
season which extends from March through
September. The bank and island habitat must be a
very small fraction of the total spawning habitat;
thus despite the higher survival in inshore areas, the
offshore zone may be the most important. In addi-
tion, better feeding conditions around islands may
be offset by a greater abundance of predators.
Whether the large concentration of starving larval
jack mackerel found offshore was an isolated case
or a general condition in offshore areas is unknown.
Given that relative recruitment strength of jack
mackerel year classes varies greatly and is rarely
"average" (Fig. 17; MacCall and Stauffer 1983), the
daily mortality rate of about 45% found in this study
is not unrealistic Considering the relatively long life-
time (i.e, 30+ yr) and high fecundity of jack
mackerel, one can deduce that the overall mortality
may be very high. This study certainly indicates that
starvation at the onset of feeding may be an impor-
tant factor influencing recruitment variation in jack
mackerel.
O'Connell's (1980) study of northern anchovy is the
only other study in which starvation in the sea has
12
THEILACKER: MORTALITY OF SEA-CAUGHT JACK MACKEREL
<
Q
OC
LU
LU
O
OC
LU
CL
OFFSHORE
100 r- r
AROUND ISLANDS
50
0
100
YOLK-SAC
< 3.2mm
N=15
FIRST FEEDING
< 3.5mm
N=200
FIRST FEEDING
< 3.5mm
N=20
50
3.5- < 4.0mm
N=112
3.5-<4.0mm
N=14
w
"•»
100 i-
^ 4.0mm
N=59
Figure 16.— Comparison of the nutritional condition of young Trachurus symmetricus collected from offshore and
nearshore habitats. Daily percents taken from Tables 2 and 3.
been assessed using histological criteria. O'Connell
examined 318 northern anchovy larvae from 64 sta-
tions that extended over a large area, 20-350 km off
the coast of California. lb compare the mortality of
northern anchovy with the daily rates I found for
jack mackerel, I calculated size-specific daily mor-
tality of northern anchovy by using 1) O'Connell's
(1980) histological evaluation, 2) information on time
to irreversible starvation to determine durations
(Lasker et al. 1970; Hunter 1981; Theilacker and
Dorsey 1981), 3) information on shrinkage of ocean-
caught northern anchovy to determine size at first
13
FISHERY BULLETIN: VOL. 84, NO. 1
250% r-
200%
x
UJ
<£
H
£ 150%
<
o
£ 100%
<
UJ
>-
<
50%
0%
1950 I960
YEAR CLASS
1970
Figure 17— Relative recruitment strengths of jack mackerel year
classes in southern California. Virtual year-class strength is
measured by the sum of percentage contributions to seasonal land-
ings over the lifetime of the year class. The dashed line indicates
average strength (from MacCall and Stauffer 1983; Fig. 4).
feeding (Theilacker 1980a), and 4) a growth rate of
0.37 mm/d for healthy sea-caught northern anchovy
(Methot and Kramer 1979). Although the number
of first-feeding larvae was low in O'Connell's data
(n = 23), I calculated a starvation-induced mortal-
ity rate of between 35 and 46%/d. Thus my calcula-
tions indicate that substantial numbers of northern
anchovy larvae as well as jack mackerel larvae are
dying at the time of first feeding. This loss rate for
northern anchovy is similar to estimated total mor-
tality rate at this stage, 39%/d (Lo in press; 1978
data), which suggests that starvation is the major
source of mortality at first feeding. This conclusion
for northern anchovy could not be drawn at the time
that O'Connell did his work because the data on net
shrinkage were not known. The average rates
estimated by O'Connell were much lower because he
combined larval size classes.
Attempts to assess larval starvation in the sea
using morphological criteria are more common
(Shelbourne 1957; Honjo et al. 1959; Nakai et al.
1969; reviewed by May 1974; Ehrlich et al. 1976), but
they have seldom been successful, probably because
of the biases introduced by failure to correct ade-
quately for shrinkage (see next section). Recently
Devonald (1983) used a morphometric index with
shrinkage adjustments to assess jack mackerel
feeding regimes off California. She found good
correspondence between jack mackerel condition
and prey availability and concluded that feeding con-
ditions were better near islands than in the area
between islands. Several of her samples and my
samples were taken concurrently (San Clemente and
Tanner Bank; Table 1), and I found that 92% of the
jack mackerel from the island habitat were healthy.
Thus, my results obtained using histological criteria
confirm Devonald's conclusion.
Other techniques used in the past to assess food
availability include RNA/DNA (Buckley 1980), food
in gut (Rojas de Mendiola 1974; Ciechomski and
Weiss 1974; Arthur 1976; Ellertsen et al. 1981), and
otoliths. Of course otolith work is critical because
estimates of growth rates are essential for assess-
ment of mortality, but it is of no value for assessing
growth at the onset of feeding (Methot 1981).
Arthur (1976) conducted the only other study on
the feeding of jack mackerel off the coast of Califor-
nia. He found, after examining the stomach contents
of 750 specimens from 65 offshore samples, that 60%
of the first-feeding jack mackerel and 10% of the
older larvae (7 mm) had empty stomachs. This obser-
vation lends additional credence to my histological
evaluation of jack mackerel collected offshore that
shows 59% of the first-feeding fish and 3% of the
older fish (>4 mm) were starving.
I believe my estimates of jack mackerel mortality
due to starvation are conservative The assumptions
I made about the persistence of starvation and the
duration of growth were based on extensive
laboratory studies (Theilacker 1978, 1981). Because
the majority of jack mackerel were collected at sites
warmer (16.1°-16.6°C) than the culture temperature
(15°-15.5°C), the durations for growth and starvation
may be altered, but the final estimate of mortality
due to starvation is higher after the appropriate
changes to the durations are made Furthermore, if
net retention of robust fish is greater than reten-
tion of thin fish of the same length, starvation may
be underestimated. In addition, the selection of
unhealthy larvae by predators would also increase
the starvation estimate
Previous evidence supporting the occurrence of
starving fish larvae in the ocean has been mainly cir-
cumstantial (reviewed by May 1974; Jones and Hall
1974; Lasker 1975). Evidence from this study and
O'Connell's (1980) study shows that starvation does
occur and that the young stages of jack mackerel and
northern anchovy are highly vulnerable
Comparison of Morphological and
Histological Criteria for
Starvation Diagnosis
The incidence of starvation based on mor-
14
THEILACKER: MORTALITY OF SEA-CAUGHT JACK MACKEREL
phological criteria was essentially the same as that
based on histological criteria. Owing to the relative
ease, and low cost of measuring fish compared with
a histological examination, the morphological
analysis is an attractive approach. On the other hand,
histological analysis defines a cause and effect rela-
tion between structure and starvation whereas gross
morphological measurements provide an index of
starvation which is highly vulnerable to errors and
biases in calibration and interpretations. Because of
the importance of these measurements in recruit-
ment studies, it is appropriate to consider the merits
of and potential errors in these techniques in some
detail.
(2/ The morphometric approach relies on measure-
ments of fish to compare reared and wild animals
at the same developmental stage Thus shrinkage ad-
justments are needed to intercalibrate laboratory
measurements and field measurements. Fish shrink
when collected in a net and preserved, and shrinkage
of the size of all body parts is dependent on the time
in the net, size of fish, and type of preservative used
(Blaxter 1971; Theilacker 1980a; Hay 1981). In this
study, tow time was controlled at 5 min and samples
were preserved within 8 min. Thus damage to the
fish and shrinkage were minimal, but the samples
were not quantitative It is doubtful that the morpho-
metric technique will work with jack mackerel taken
in standard, quantitative collections. Quantitative net
tows are 20 min, and they include an additional
hosing down of the nets before sample preservation
(Smith and Richardson 1977). The procedure
damages the larvae, causing extensive shrinkage
which makes accurate measuring difficult. Further,
a long tow time decreases confidence in time-specific
shrinkage estimates because fish can be collected at
any time during the towing period. Increasing the
tow time also causes both the magnitude of the
shrinkage correction factor and the standard error
of its estimate to increase For example, in this study,
standard length of jack mackerel shrank by an
average of 6.0 ± 0.6% in 8 min and 19.0 ± 1.0% in
20 min.
While laboratory calibration is absolutely essen-
tial for the morphometric analysis, no shrinkage
calibration is needed for the histological analysis, and
it might be possible to use the histological observa-
tions on other fishes. Diagnostic criteria for the
starving condition of jack mackerel (Theilacker
1978), northern anchovy (O'Connell 1976), and
yellowtail, Seriola quinqueradiata, (Umida and
Ochiai 1975) were similar. In addition, important
biological information is gained while using the
histological approach whereas gross morphological
indices provide no such information. For example,
histological analysis of jack mackerel has revealed
a pattern of diel swim bladder inflation and a disrup-
tion of this rhythm, accumulation of glycogen
reserves, and brain lesions presumably produced by
UV radiation (Hunter et al. 1979). There is just no
substitute for this extensive biological information.
On the other hand, population work requires large
samples, and morphological indices are probably the
only practical means for working with very large
samples. Thus, the optimal experimental design for
population work on starvation is probably the use
of morphological criteria (calibrated for shrinkage)
combined with a smaller subsample of fish which are
graded histologically. All work requires special net
tows, preservation, procedures, and laboratory
calibration.
Caution needs to be exercised when transferring
information obtained in the laboratory to the field.
Raising larval jack mackerel in small containers is
known to affect growth, nutritive condition, and
possibly activity (Theilacker 1980b). Additionally,
there is evidence that wild fish tend to be thinner
than their laboratory counterparts (larval herring,
Blaxter 1971; juvenile herring, Balbontin et al. 1973;
larval northern anchovy, Arthur 1976). My use of the
morphometric SWDA assumes that the morpho-
metric criteria I developed in the laboratory for lar-
val jack mackerel raised in large tanks are applicable
to ocean-caught jack mackerel.
ACKNOWLEDGMENTS
Many thanks to Brian Rothschild who suggested
research on the nutritive condition of larval fish and
to William T (Tosh) Yasutake who offered me a per-
sonalized course in teleost histology. The offshore
collections were made possible by Roger Hewitt's ef-
fective planning, the crew of the RV David Starr
Jordan, and the assistance of Jack Metoyer and
Carol Kimbrell. Miguel Carrillo sorted the mackerel,
Richard Kiy measured them, and Jack Metoyer
prepared them for histological analyses. Metoyer also
helped with the shrinkage study. Nancy Lo assisted
with all statistical applications. I appreciate John
Hunter's and Martin Newman's constructive reviews
of the manuscript. Many thanks to the Technical Sup-
port Group for typing services.
LITERATURE CITED
Ahlstrom, E. H.
1959. Vertical distribution of pelagic fish eggs and larvae off
California and Baja California. U.S. Wildl. Serv., Fish.
15
FISHERY BULLETIN: VOL. 84, NO. 1
Bull. 60:107-146.
Anderson, W. A. D.
1971. Degenerative changes and disturbances of metabolism.
In W. A. D. Anderson (editor), Pathology, p. 68-95. The C.
V. Mosby Co., St. Louis, 6th ed.
Arthur, D. K.
1976. Food and feeding of larvae of three fishes occurring in
the California Current, Sardinops sagax, Engraulis mordax,
and Trachurus symmetricus. Fish. Bull., U.S. 74:517-530.
1977. Distribution, size, and abundance of microcopepods in
the California Current system and their possible influence
on survival of marine teleost larvae Fish. Bull., U.S. 75:
601-611.
Balbontin, F, S. S. de Silva, and K. S. Ehrlich.
1973. A comparative study of anatomical and chemical charac-
teristics of reared and wild herring. Aquaculture 2:217-
240.
Beers, J. R., and G. L. Stewart.
1967. Micro-zooplankton in the Euphotic zone at five locations
across the California Current. J. Fish. Res. Board Can. 24:
2053-2068.
1970. Numerical abundance and estimated biomass of micro-
zooplankton. In J. D. H. Strickland (editor), The ecology of
the plankton off La Jolla, California, in the period April
through September, 1967. Vol. 17 (Part VI), p. 67-87. Bull.
Scripps Inst. Oceanogr.
Blaxter, J. H. S.
1971. Feeding and condition of Clyde herring larvae Rapp.
P.-v. Reun. Cons. int. Explor. Mer 160:128-136.
Buckley, L. J.
1980. Changes in the ribonucleic acid, deoxyribonucleic acid,
and protein content during ontogenesis in winter flounder,
Pseudopleuronectes americanus, and effect of starvation.
Fish. Bull., U.S. 77:703-708.
ClECHOMSKI, J. D, DE, AND G. WEISS.
1974. Estudios sobre la Alimentacion de larvas de la merluza,
Merluccius merluccius Hubbsi de la anchoita, Engraulis an-
choita, en la mar. Physis. Seer. A Buenos Aires 33:199-208.
Devonald, K. F.
1983. Evaluation of the feeding success of first-feeding jack
mackerel larvae off southern California, and some con-
tributing factors. Ph.D. Thesis, Univ. California, Scripps
Inst. Oceanogr., 227 p.
Ehrlich, K. F, J. H. S. Blaxter, and R. Pemberton.
1976. Morphological and histological changes during growth
and starvation of herring and plaice larvae Mar. Biol. (Berl.)
35:105-118.
Ellertsen, B., E. Moksness, P. Solendal, T. Str0mme, S.
TlLSETH, T WESTGARD, AND V. 0IESTAD.
1981. Some biological aspects of cod larvae (Gadus morhua
L.). ICES Symposium on Early Life History of Fish, Woods
Hole Mass., April 1979. Rapp. R.-v. Reun. Cons. int. Explor.
Mer 178:317-319.
Farris, D. A.
1961. Abundance and distribution of eggs and larvae and sur-
vival of larvae of jack mackerel (Trachurus symmetricus).
U.S. Fish Wildl. Serv., Fish. Bull. 61:247-279.
Hay, D. E.
1981. Effects of capture and fixation on gut contents and body
size of Pacific herring larvae Rapp. P.-v. Reun. Cons. int.
Explor. Mer 178:395-400.
Hewitt, R., G. H. Theilacker, and N. C. H. Lo.
In press. Causes of mortality in young jack mackerel. Mar.
Ecol. Prog. Ser.
Hjort, J.
1914. Fluctuations in the great fisheries of northern Europe
viewed in the light of biological research. Rapp. P.-v. Reun.
Cons. Perm. int. Explor. Mer. 20:1-228.
HONJO, K., T KlTACHI, AND H. SUZUKI.
1959. On the food distribution and survival of post larval
iwashi-1-Distribution of food organisms, the food of the an-
chovy and ecologically related species along the southwest-
ern Pacific coast of Honshu, Sept.-Nov. 1958. Reports on the
major coastal fish investigations, and the investigations for
forecasting of oceanographic conditions and fisheries
(preliminary report), February 1959. (Engl. Transl. by S.
Hayaski.)
Hunter, J. R.
1981. Feeding ecology and predation of marine fish larvae
In R. Lasker (editor), Marine fish larvae morphology, ecology
and relation to fisheries, p. 33-77. Wash. Sea Grant Pro-
gram, Univ. Wash. Press, Seattle
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.
Hunter, J. R, J. H. Taylor, and H. G Moser.
1979. Effects of ultraviolet irradiation on eggs and larvae of
the northern anchovy, Engraulis mordax, and the Pacific
mackerel, Scomber japonicus, during the embryonic stage
Photochem. Photobiol. 29:325-338.
Iwai, T.
1968. The comparative study of the digestive tract of teleost
larvae— V. Fat. absorption in the gut epithelium of goldfish
larvae Bull. Jpn. Soc. Sci. Fish. 34:973-978.
1969. Fine structure of gut epithelial cells of larval and
juvenile carp during absorption of fat and protein. Arch.
Hist. Jpn. 30:183-199.
Iwai, T, and M. Tanaka.
1968. The comparative study of the digestive tract of teleost
larvae— III. Epithelial cells in the posterior gut of halfbeak
larvae Bull. Jpn. Soe Sci. Fish. 34:44-48.
Jones, R., and W B. Hall.
1974. Some observations on the population dynamics of the
larval stage in common gadoids. In J. H. S. Blaxter (editor),
Early life history of fish, p. 87-102. Springer-Verlag. Berl.
Lasker, R.
1975. Field criteria for survival of anchovy larvae: the rela-
tion between inshore chlorophyll maximum layers and suc-
cessful first feeding. Fish. Bull., U.S. 73:453-462.
Lasker, R., H. M. Feder, G H. Theilacker, and R. C. May.
1970. Feeding, growth, and survival of Engraulis mordax lar-
vae reared in the laboratory. Mar. Biol. (Berl.) 5:345-353.
Lo, N. C. H.
In press. Egg production of the central stock of northern an-
chovy, 1951-1982. Fish. Bull., U.S. 83.
Love, R. M.
1970. The chemical biology of fishes. Acad. Press (Lond.), p.
222-257.
MacCall, A. D, and G. D Stauffer.
1983. Biology and fishery potential of jack mackerel
(Trachurus symmetricus). Calif. Coop. Oceanic Fish. Invest.
Rep. 24:46-56.
May, R. C.
1974. Larval mortality in marine fishes and the critical period
concept. In J. H. S. Blaxter (editor), The early life history
of fish, p. 3-19. Springer-Verlag, N.Y.
Methot, R. D, Jr.
1981. Growth rates and age distributions of larval and juvenile
northern anchovy,, Engraulis mordax, with inferences on
larval survival. Ph.D. Thesis, Univ. California, San Diego,
328 p.
16
THEILACKER: MORTALITY OF SEA-CAUGHT JACK MACKEREL
Methot, R. D., Jr., and D. Kramer.
1979. Growth of northern anchovy, Engraulis mordax, larvae
in the sea. Fish. Bull., U.S. 77:413-423.
Nakai, Z., M. Kosaka, M. Ogura, G. Hayashida, and H.
Shimozono.
1969. Feeding habit, and depth of body and diameter of
digestive tract of Shirasu, in relation with nutritious condi-
tions. J. Coll. Mar. Sci. Technol, Tbkai Univ. 3:23-34.
O'CONNELL, C. P.
1976. Histological criteria for diagnosing the starving condi-
tion in early post yolk sac larvae of the northern anchovy,
Engraulis mordax Girard. J. Exp. Mar. Biol. Ecol. 25:285-
312.
1980. Percentage of starving northern anchovy, Engraulis
mordax, larvae in the sea as estimated by histological
methods. Fish. Bull., U.S. 78:475-489.
Rajos de Mendiola, B. R.
1974. Food of the larval anchoveta, Engraulis ringens J. In
J. H. S. Blaxter (editor), The early life history of fish, p.
277-285. Springer-Verlag, N.Y.
Shelbourne, J. E.
1957. The feeding and condition of plaice larvae in good and
bad plankton catches. J. Mar. Biol. Assoc U.K. 36:539-552.
Smith, P. E., and S. L. Richardson.
1977. Standard techniques for pelagic fish egg and larva
surveys. F.A.O. Fish. Tech. Pap. 175, 100 p.
The i lacker, G. H.
1978. Effect of starvation on the histological and morpho-
logical characteristics of jack mackerel, Trachurus sym-
metrica, larvae Fish. Bull., U.S. 76:403-414.
1980a. Changes in body measurements of larval northern an-
chovy, Engraulis mordax, and other fishes due to handling
and preservation. Fish. Bull., U.S. 78:685-692.
1980b. Rearing container size affects morphology and nutri-
tional condition of larval jack mackerel, Trachurus sym-
metricus. Fish. Bull., U.S. 78:789-791.
1981. Effect of feeding history and egg size on the mor-
phology of jack mackerel, Trachurus symmetricus, larvae.
ICES Symposium on Early Life History of Fish, Woods Hole,
Mass., April 1979. Rapp. P.-v. Reun. Cons. int. Explor. Mer
178:432-440.
Theilacker, G. H., and K. Dorsey.
1980. Larval fish diversity. In Workshop on the effects of en-
vironmental variation on the survival of larval pelagic fishes.
Intergov. Oceanogr. Comm. Rep. 28:105-142. UNESCO,
Paris.
Umeda, S., and A. Ochiai.
1975. On the histological structure and function of digestive
organs of the fed and starved larvae of the yellowtail, Seriola
quinqueradiata. [In Jpn., Engl, summ.] Jpn. J. Ichthyol.
21:213-219.
Watanabe, Y.
1981. Ingestion of horseradish peroxidase by the intestinal
cells in larvae or juveniles of some teleosts. Bull. Jpn. Soc.
Sci. Fish. 47:1299-1307.
17
HYPOXIA IN LOUISIANA COASTAL WATERS DURING 1983:
IMPLICATIONS FOR FISHERIES
Maurice L. Renaud1
ABSTRACT
Hypoxic bottom water (<2.0 ppm dissolved oxygen) was present in shallow (9-15 m) waters south of cen-
tral Louisiana in June and July 1983. It was patchy in distribution from south of Barataria Pass to south
and west of Marsh Island. Data suggested that bottom water hypoxia did affect the abundance and distribu-
tion of shrimp and bottomfish. Offshore bottom water dissolved oxygen was significantly correlated with
1) combined catches of brown and white shrimp (r = 0.56, P < 0.002), 2) fish biomass (r = 0.56, P <
0.001), and 3) vertical density gradient (r = -0.73, P < 0.001). Several hypoxic stations were in regions
designated as potentially hypoxic through a posteriori analysis of satellite data. Micrapogonius undulatus
was the dominant fish species nearshore and offshore Penaeus aztecus and P. setiferus were sparsely
distributed throughout the study area.
The presence of bottom water hypoxia (<2.0 ppm
dissolved oxygen) in the nearshore Gulf of Mexico
is a common, recurring, and mostly seasonal (June-
August) event. It is generally thought to be associ-
ated with temperature and salinity stratification ini-
tiated by freshwater runoff and with phytoplankton
blooms during hot, calm weather (Fotheringham and
Weissberg 1979; Bedinger et al. 1981; Comiskey and
Farmer 1981; Turner and Allen 1982a, b; Boesch
1983; Leming and Stuntz 1984). Phytoplankton
respiration and decomposition of sinking organic
matter are major oxygen consuming processes. High
oxygen demand of the organic load in freshwater
runoff (Gallaway 1981) and lack of a direct oxygen
replenishing mechanism (strong winds) in the pres-
ence of vertical stratification contribute to hypoxia
formation (Harris et al. 1976; Ragan et al. 1978;
Swanson and Sindermann 1979; Harper et al. 1981).
Christmas (1973) and Boesch (1983) discussed possi-
ble nitrate pollution in rivers and coastal hypoxia.
Boesch (1983) presented a brief history of hypoxia
in the Gulf of Mexico and evaluated its causes and
consequences. The extent to which any factor is in-
volved with hypoxia formation is unknown.
Hypoxia in the Gulf of Mexico has been most
noticeable in shallow (<20 m) Louisiana waters. It
has been reported infrequently on the Texas shelf
(Harper et al. 1981; Gallaway and Reitsema 1981).
Low oxygen levels have also been measured east of
the Mississippi River Delta inshore of barrier islands
'Southeast Fisheries Center Galveston Laboratory, National
Marine Fisheries Service, NOAA, 4700 Avenue U, Galveston, TX
77550.
and in inland bays (May 1973; Christmas 1973) and
offshore of Mobile Bay, AL (Turner and Allen 1982b).
Abnormally high concentrations of moribund fish
and crustaceans near the shoreline ("jubilees") in
Alabama have also been linked to hypoxia (May
1973).
Considerable interest in hypoxia has been renewed
by a less than average shrimp harvest in 1982 (Klima
et al. 1983) and 19832. In this paper I report the loca-
tions and extent of Louisiana coastal hypoxia in 1983
and discuss the interrelationships of fish and shrimp
abundance and distribution with environmental
parameters.
METHODS
Nearshore data were collected in a 7.3 m Aqua-
Sport at a total of 56 stations from nine transects
west of the Mississippi River Delta (long. 89°33'W
to 90°14'W) from 1 to 16 June 1983 (Fig. 1). The
transects, perpendicular to shore, ranged from 5 to
8 km in length and 1 to 16 m in depth. The six east-
ernmost transects were sampled twice, with a sam-
pling interval of 14 d. Shrimp and bottomfish were
collected at 23 of 56 stations in 15-min tows with
a 3.0 m box trawl. Towing speed was about 3 kn.
Before each tow, water temperature, salinity, and
dissolved oxygen concentration were recorded at 1
m depth intervals with a Hydrolab 8000. Hydro-
graphic profiles were made at the remaining 33
stations.
An offshore study area extending from long.
21983 Gulf Coast Shrimp Data, NOAA, NMFS.
Manuscript accepted January 1985.
FTSHFRV RT1I T FTTN- VOT 84 MO 1 1 Q«fi
19
FISHERY BULLETIN: VOL. 84, NO. 1
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20
RENAUD: HYPOXIA IN LOUISIANA WATERS
90°47'W to 93°02'W was sampled with a 24.4 m
steel-hull commercial shrimp trawler from 30 June
to 6 July 1983 (Fig. 1). Depth varied from 4 to 20
m and distance from shore ranged from 8 to 54 km.
Shrimp and bottomfish were collected at 34 of 65
stations in 20-min tows with a 12.2 m semiballoon
trawl. The same trawl was used as a midwater
shrimp sampler above previously identified hypoxic
water. Surface and bottom measurements of water
temperature, salinity, and dissolved oxygen concen-
tration were recorded before each tow. Water
samples were collected with a Kemmerer bottle
Salinities were measured with a refractometer.
Temperature and dissolved oxygen concentration
were measured with a YSI Model 51-B. Surface and
bottom hydrographic data were collected at the re-
maining 31 stations. The Southeast Area Monitor-
ing and Assessment Program (SEAMAP)3 person-
nel collected similar data off Louisiana in June 1983.
SEAMAP dissolved oxygen data were included in
the contour analyses.
The Harvard SYMAP program (Dougenik and
Sheehan 1975), a Northwest Alaska Fisheries Center
Contour Subroutine, and the Galveston Laboratory
Generalized Mapping system were utilized to pro-
duce a map of dissolved oxygen contours off Loui-
siana. Koi4 presents an indepth explanation of these
contour mapping programs. Vertical density gra-
dient of the water column, shrimp catch, and fish
catch were regressed with bottom water dissolved
oxygen concentration. A "best fit" line through the
data was determined using the least squares concept.
Surface water temperature (°C) and chlorophyll
content (mg/m3) were measured off Louisiana by
the Coastal Zone Color Scanner (CZCS) aboard the
Nimbus-7 satellite Personnel from the Mississippi
Laboratories of the Southeast Fisheries Center,
working at the National Space Technology Labora-
tories, Mississippi, used CZCS and "ground truth"
field data to predict potentially hypoxic areas in
coastal Louisiana waters.
RESULTS AND DISCUSSION
Regions of hypoxic bottom water have been
detected along portions of the Texas-Louisiana
coastline every summer from 1972 to 1983 (Harris
3Southeast Area Monitoring and Assessment Program: a State-
Federal cooperative research effort organized to assess the distribu-
tion and abundance of shrimp and bottomfish in the Gulf of Mexico.
4Koi, D. 1985. Generalized geographic mapping system. Un-
publ. manuscr., 47 p. Southeast Fisheries Center Galveston
Laboratory, National Marine Fisheries Service, NOAA, 4700
Avenue U, Galveston, TX 77550.
et al. 1976; Ragan et al. 1978; Bedinger et al. 1981;
Harper et al. 1981; Reitsema et al. 1982; Boesch
1983). Hypoxia was noted from 16 June to 6 July
1983. It was patchy in distribution and found main-
ly in 9 to 15 m depths from south of Barataria Pass
to south and west of Marsh Island (Fig. 1).
A total of 34 fish and 11 invertebrate species were
collected offshore The Atlantic croaker, Micropo-
gonius undulatus, and the Atlantic threadfin, Poly-
dactylies octonemus, were the dominant bottomfish
at 58% and 30% of the stations, respectively; Atlantic
bumper, Chloroscombrus chrysurus, was the com-
mon pelagic. Brown shrimp, Penaeus aztecus; white
shrimp, P. setiferus; mantis shrimp, Squilla empusa;
and broken-back shrimp, Trachypenaeus sp., were the
most common invertebrates collected, but in small
quantities. Total crustacean catch was always <5.0
kg/h.
Bottom water dissolved oxygen concentration was
significantly correlated with 1) fish biomass (r =
0.56, P < 0.001) (Fig. 2) and the number of brown
and white shrimp present (r = 0.56, P < 0.002) (Fig.
3). Shrimp and bottomfish were generally absent
from hypoxic stations. Atlantic croaker were not at
stations with hypoxic bottomwater, and shrimp
catches never exceeded 2 kg/h in the areas. Sea cat-
fish, Arisus felis; butterfish, Peprilus paru; and
Atlantic bumper were common in trawls at hypoxic
sites. These were also the most abundant fish in mid-
4.0r-
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2.0 4.0
BOTTOM WATER DISSOLVED OXYGEN
CONCENTRATION (PPM)
6.0
FIGURE 2— Offshore fish biomass in relation to bottom water
dissolved oxygen concentration.
21
FISHERY BULLETIN: VOL. 84, NO. 1
2.0r-
a
P
oc
fflS
I
U-CJ
°«
oc t-
uj >>
m q.
2S
= 5
OX
1.0
0.0
2.0 4.0
BOTTOM WATER DISSOLVED OXYGEN
CONCENTRATION (PPM)
6.0
Figure 3.— Offshore shrimp abundance in relation to bottom water
dissolved oxygen concentration.
water trawls above previously identified hypoxic
areas. Therefore, it was concluded that they were
captured from the upper water column as the trawl
passed through it. Four brown shrimp, three lesser
blue crabs, Callinectes similus, and one mantis
shrimp were the only crustaceans captured in five
midwater trawls. The relationship between shrimp
and bottomfish abundance and distribution indicates
that they do not pass through or over hypoxic water
masses. Actual avoidance behavior in the field has
not been documented.
Nearshore, a total of 20 fish and 5 invertebrate
species were collected. Atlantic croaker was the
dominant species. Brown shrimp were present in low
numbers at most stations. White shrimp; blue crabs,
Callinectes sapidus; lesser blue crabs; and sea bobs,
Xiphopenaeus sp., were the only other crustaceans
collected. A high variability in fish and shrimp abun-
dance was probably due to the low fishing efficiency
of the small net at the deeper nearshore stations.
As a result, no significant correlation was present
at nearshore stations between bottom water dis-
solved oxygen concentration and fish or shrimp
abundance
Vertical density stratification was present at both
nearshore and offshore stations. Dissolved oxygen
concentration and vertical density gradient were
negatively correlated (r = -0.73, P < 0.001) (Fig.
4). This agrees with Leming and Stuntz (1984) who
found a high correlation between bottom dissolved
oxygen content and surface to bottom density gra-
dients off Louisiana in 1982 (r = -0.74, P < 0.001).
Offshore, the mean difference between surface and
bottom dissolved oxygen was 6.4 ppm (standard er-
ror = 0.40) in hypoxic areas and 1.6 ppm (standard
error = 0.08) in nonhypoxic areas. Temperature
generally did not vary more than 2°C between the
surface and bottom regardless of the area.
During the first week of July, 92% of the hypoxic
stations were in areas predicted as potentially hypox-
ic through a posteriori analyses of remote sensing
data. Hypoxic areas were characterized by surface
water temperatures near 30 °C, which agrees with
Leming and Stuntz (1984). They discussed satellite
data acquisition, its value in identifying and
forecasting hypoxic regions in the Gulf of Mexico,
z
III
a
>
x
o ^
> |
W O
Q <
« s
e z
t m
*2
2 °
I-
H
o
m
8. Or*
6.0 -'
4.0 -
2.0 -
0.0
Figure 4.— Bottom water dissolved oxygen concentration in
relation to vertical density gradient of the water column. Den-
sity gradient is expressed as (bottom sigma-t minus surface
sigma-t)/depth.
0.5 1.0 1.5
DENSITY GRADIENT
22
RENAUD: HYPOXIA IN LOUISIANA WATERS
and its implications regarding shrimp management.
The effect of hypoxia on shrimp is not completely
understood. It is possible that an extensive area of
hypoxic bottom water can act as a physical barrier
to juvenile shrimp migration offshore and to post-
larval migration into nursery grounds. Limited in-
direct evidence supports this hypothesis. Gazey et
al. (1982) described a shrimp mark-release study in
Louisiana. Extensive longshore and offshore move-
ment occurred before the recapture of the shrimp
during 1979, when hypoxia was not reported off
Louisiana (Fig. 5). In 1978, when hypoxia was wide-
spread along the Louisiana coastline (Fig. 6), shrimp
did not move comparable distances. It was possible
that hypoxia reduced shrimp movement into offshore
waters.
The most extensive occurrence of hypoxic bottom
water recorded in Louisiana coastal waters occurred
from May 1973 to May 1974 (Flowers et al. 1975;
Ragan et al. 1978). It was widespread between
Barataria and Timbalier Passes and extended up to
30 km offshore in some regions. Ragan et al. (1978)
reported several areas to be anoxic The duration and
severity of this hypoxic condition may have had an
impact on the offshore brown shrimp fishery in 1973.
Total brown shrimp catch and CPUE (catch per unit
effort) in 1973 were significantly lower (paired £-test,
P < 0.05) than in 1972 (fn. 2). Catch declined 36%
(2.8 million kg) and the mean CPUE was reduced
by 120 kg/vessel per d. Movement of juvenile brown
shrimp to the offshore fishery occurs from May to
August (Cook and Lindner 1970). Monthly catch and
CPUE of brown shrimp from January through April
1973 did not differ from the same time period in
1972; however, catch and CPUE from May through
December were significantly lower (paired £-test, P
< 0.01) in 1973. Postlarval recruitment of brown
shrimp occurs from January to May (Baxter and
Renfro 1966). An interaction between hypoxia and
postlarval recruitment in 1974 might have been
responsible for the continued poor harvest of brown
shrimp that year. Catch and CPUE were still sig-
nificantly lower than in 1972 (paired i-test, P < 0.05).
It was not until 1976 that brown shrimp catch sur-
passed the 1972 levels (Table 1). A decline in total
shrimp catch of Louisiana in 1982 may have been
related to a large region of hypoxic bottom water
reported by Stuntz et al. (1982).
Although hypoxia has not been directly linked to
declines in annual catch, its presence during critical
LOUISIANA
C~-30 ^ f1
Figure 5— Movement of tagged juvenile brown shrimp from Caillou Lake and Barataria Bay expressed as days at
large before recapture (from Gazey et al. 1982). Shrimp were released in July 1979. Hypoxia was not documented
off this coastal area in 1979.
23
FISHERY BULLETIN: VOL. 84, NO. 1
LOUISIANA
Figure 6.— Movement of tagged juvenile brown shrimp from Caillou Lake, expressed as days at large before recap-
ture (from Gazey et al. 1982). Shrimp were released in June 1978. Regions of hypoxic bottom water, noted from June
to August, are overlaid onto this map (Fotheringham and Weissberg 1979; Bedinger et al. 1981; Comiskey and Farmer
1981).
Table 1. — Louisiana brown shrimp catch data.
1972
1973
1974
1975
1976
5-yr
average
Catch per unit effort
(kg/vessel per d)
Jan .-Apr.
May-Aug.
Sept.-Dec.
190
383
376
216
225
233
180
249
328
196
296
346
208
348
268
198
300
310
Annual average
344
1223
'256
288
302
284
Catch
(millions of kg)
Jan. -Apr.
May-Aug.
Sept.-Dec.
Total
0.831
4.529
2.293
7.653
1.478
2.630
0.822
M.930
0.633
2.702
1.578
14.913
0.645
2.112
1.414
4.171
1.020
5.966
2.601
9.587
0.921
3.588
1.742
6.251
Effort
(24-h days fished)
Jan. -Apr.
May-Aug.
Sept.-Dec.
Total
4,379
1 1 ,828
6,361
22,568
6,870
11,722
3,528
22,120
3,509
10,852
4,805
19.166
3,288
7,128
4,083
14,499
4,903
17,127
9,715
31,745
4,590
11,731
5,698
22,020
'CPUE and catch data in 1973 and 1974 were significantly lower than that in 1972 (paired Mest, P < 0.05)
portions of the shrimp life cycle implicate it as a prob-
able source of variation in annual shrimp yield. Sup-
port for this viewpoint has been documented in
laboratory experiments which indicate that brown
and white shrimp detect and avoid water with low
oxygen levels.5 Brown shrimp were the least tolerant
of the two species. They avoided dissolved oxygen
concentrations up to and including 2.0 ppm. White
shrimp did not avoid oxygen levels higher than 1.5
ppm. Variable behavior was exhibited by both species
at higher treatment levels. Total time (TT) spent in
water with 1.5 ppm did not differ between species,
5Renaud, M. 1985. Detection and avoidance of oxygen depleted
water by Penaeus setiferus and Penaeus aztecus. Unpubl. manuscr.,
16 p. Southeast Fisheries Center Galveston Laboratory, National
Marine Fisheries Service, NOAA, 4700 Avenue U, Galveston, TX
77550.
24
RENAUD: HYPOXIA IN LOUISIANA WATERS
nor did their response time (RT), i.e, time taken to
retreat into normal seawater. However, these
measurements were significantly (£-test, P < 0.001)
shorter for brown shrimp (TT = 6.2, RT = 3.8 min)
versus white shrimp (TT = 20.0, RT = 6.2 min) when
tested at 2.0 ppm. Behavioral responses of brown and
white shrimp exposed to hypoxic water included 1)
an initial increase in activity, 2) walking or swim-
ming retreat, and 3) rapid eye movements. White
shrimp also exhibited notable abdominal flexing,
periods of exhaustion, and sometimes death. These
three latter behaviors were not observed with brown
shrimp. Dissolved oxygen levels tested are common
along Louisiana's Gulf Coast during the summer and
early fall. Therefore it is not unreasonable to assume
that similar behavioral responses occur in nature
Hypoxia in the New York Bight (Swanson and
Sindermann 1979) had a severe impact on the com-
mercial fisheries of sedentary species. Surf clam,
Spisula solidissima; ocean quahog, Arctica islan-
dica; and scallop, Placopectin magellanicus,
abundance was reduced by 92%, 25%, and 12%,
respectively, in the affected area. The response of
recreational fish species, summer flounder,
Paralichthys dentatus, and bluefish, Pomatomus
saltatrix, to low oxygen levels was noted by changes
in their distribution patterns during the hypoxic
event. Temperature stratification, phytoplankton
blooms, spoil deposition, and sewage treatment
outflow were alleged major contributors to hypoxia
formation in the New York Bight. It was concluded,
however, that abnormal climatological and
hydrological phenomena were responsible for this
hypoxic event. Swanson and Sindermann (1979)
stated that effective regulation of waste disposal into
riverine and oceanic environments may control or
restrict bottom water hypoxia formation.
Future research on the phenomenon of hypoxia
should be centered on its predictability; remote
sensing has potential in this area. Timely informa-
tion dissemination on the extent and location of
hypoxic areas would help fishermen to avoid areas
where low catches might be anticipated or to harvest
a crop before it dies or migrates.
ACKNOWLEDGMENTS
The author expresses his sincere appreciation to
1) the Lousiana Wildlife and Fisheries Department
for providing NMFS personnel with services at their
Grand Terre Island Marine Laboratory and at their
Field Station in Caillou Lake; 2) the Gulf States
Marine Fisheries Commission for access to the 1983
SEAMAP data; 3) David Trimm for this major con-
tribution to data collection; 4) Dennis Koi for com-
puter services and related software analyses,
especially those relevant to contour mapping; 5)
Frank Patella for acquisition and transformation of
several years of Gulf coast shrimp data; 6) Tom Lem-
ing for satellite data; and 7) Beatrice Richardson for
typing the manuscript.
LITERATURE CITED
Baxter, K. N., and W. C. Renfro.
1966. Seasonal occurrence and size distribution of postlarval
brown and white shrimp near Galveston, Texas, with notes
on species identification. U.S. Fish Wildl. Serv., Fish. Bull.
66:149-158.
Bedinger, C. A., R. E. Childers, J. W. Cooper, K. T. Kimball,
and A. Kwok.
1981. Pollution fate and effect studies. In C. A. Bedinger
(editor), Ecological investigations of petroleum production
platforms in the central Gulf of Mexico, Vol. 1, Part 1, 53
p. Report to the Bureau of Land Management, New
Orleans, LA, Contract No. AS551-CT8-17.
Boesch, D. F.
1983. Implications of oxygen depletion on the continental shelf
of the northern Gulf of Mexico. Coastal Ocean Pollut.
Assess. News 2:25-28.
Christmas, J. Y. (editor).
1973. Cooperative Gulf of Mexico estuarine inventory and
study, Mississippi: Phase I, area description, Phase II,
hydrology, Phase II, sedimentology, Phase IV, biology. Gulf
Coast Research Laboratory, Ocean Springs, MS, 434 p.
Comiskey, C. E., and T. A. Farmer (editors).
1981. Characterization of base-line oceanography for the Tex-
oma region brine disposal sites. Vol. I. Final Report to U.S.
Department of Energy, Strategic Petroleum Reserve Office,
Wash., D.C., Contract No. DEAC01-774508788, 130 p.
Cook, H. L., and M. J. Lindner.
1970. Synopsis of biological data on the brown shrimp Penaeus
aztecus aztecus Ives, 1891. InM. N. Mistakidis (editor), Pro-
ceedings of the World Scientific Conference on the Biology
and Culture of Shrimps and Prawns, p. 1471-1497. FAO
Fish. Rep. 57(4).
DOUGENIK, J. A., AND D. E. SHEEHAN.
1975. SYMAP User's Manual. Camera Stat of Bedford,
Cambridge, MA, 187 p.
Flowers, C. W., W. T. Miller, and J. D. Gann.
1975. Water chemistry. In J. G. Gosselink, R. H. Miller, M.
Hood, and L. M. Bahr (editors), Environmental assessment
of a Louisiana offshore port and appertinent pipeline and
storage facility. Vol. II, App. V, Sect. 1, 86 p. Final Report
to Louisiana Offshore Oil Port, New Orleans, LA.
Fotheringham, N., and G. H. Weissberg.
1979. Some causes, consequences and potential environmen-
tal impacts of oxygen depletion in the northern Gulf of Mex-
ico. Proc. 1 1th Annu. Offshore Tech. Conf ., April 30-May 3,
1979, 3611:2205-2208.
Gallaway, B. J.
1981. An ecosystem analysis of oil and gas development on
the Texas-Louisiana continental shelf. U.S. Fish Wildl. Serv.,
Off. Biol. Serv., Wash., D.C., FWS/OBS-81-27, 88 p.
Gallaway, B. J., and L. A. Reitsema.
1981. Shrimp spawning site survey. In W. B. Jackson and E.
P. Wilkens (editors), Shrimp and redfish studies; Bryan
Mound brine disposal site off Freeport, Texas 1979-1981.
25
FISHERY BULLETIN: VOL. 84, NO. 1
NOAA Tech. Memo. NMFS-SEFC-67, Vol. IV, 84 p. Available
from National Technical Information Service, Springfield, VA
22151.
Gazey, W. J., B. J. Gallaway, R. C. Fechhelm, L. R. Martin, and
L. A. Reitsema.
1982. Shrimp mark release and port interview sampling
survey of shrimp catch and effort with recovery of captured
tagged shrimp. In W. B. Jackson (editor), Shrimp popula-
tion studies: West Hackberry and Big Hill brine disposal sites
off southwest Louisiana and upper Texas coasts, 1980-1982,
Vol. II, 306 p. NOAA/NMFS Final Report to Department
of Energy.
Harper, D. E., L. D. McKinney, R. R. Salzer, and R. J. Case.
1981. The occurrence of hypoxic bottom water off the upper
Texas coast and its effects on the benthic biota. Contrib.
Mar. Sci. 24:53-79.
Harris, A. H., J. G. Ragan, and R. H. Kilgen.
1976. Oxygen depletion on coastal waters. La. State Univ.
Sea Grant Summ. Rep., Proj. No. R/BOD-1, 161 p.
Klima, E. F, K. N. Baxter, F. J. Patella, and G. A. Matthews.
1983. Review of 1982 Texas closure for the shrimp fishery off
Texas and Louisiana. NOAA Tech. Memo. NMFS-SEFC-108,
22 p. Available from National Technical Information Service,
Springfield, VA 22151.
Leming, T. D., and W. E. Stuntz.
1984. Zones of coastal hypoxia revealed by satellite scanning
have implications for strategic fishing. Nature (Lond.) 310:
136-138.
May, E. B.
1973. Extensive oxygen depletion in Mobile Bay, Alabama.
Limnol. Oceanogr. 18:353-366.
Ragan, J. G., A. H. Harris, and J. H. Green.
1978. Temperature, salinity and oxygen measurements of sur-
face and bottom waters on the continental shelf off Louisiana
during portions of 1975 and 1976. Nicholls State Univ., Prof.
Pap. Ser. (Biol.) 3:1-29.
Reitsema, L. A., B. J. Gallaway, and G. S. Lewbel.
1982. Shrimp spawning site survey. In W. B. Jackson (editor),
Shrimp population studies: West Hackberry and Big Hill
brine disposal sites off southwest Louisiana and upper Texas
coasts, 1980-1982, Vol. IV, 88 p. NOAA/NMFS Final Report
to Department of Energy.
Stuntz, W E., N. Sanders, T D. Leming, K. N. Baxter, and
R. M. Barazotto.
1982. Area of hypoxic bottom water found in northern Gulf
of Mexico. Coastal Ocean. Climatol. News 4:37-38.
Swanson, R. L., and C. J. Sindermann (editors).
1979. Oxygen depletion and associated benthic mortalities in
New York Bight, 1976. NOAA Prof. Pap. No. 11, 345 p.
Rockville, MD.
Turner, R. E., and R. L. Allen.
1982a. Bottom water oxygen concentration in the Mississippi
River Delta Bight. Contrib. Mar. Sci. 25:161-172.
1982b. Plankton respiration rates in the bottom waters of the
Mississippi River Delta Bight. Contrib. Mar. Sci. 25:173-179.
26
INCIDENTAL MORTALITY OF
DOLPHINS IN THE EASTERN TROPICAL PACIFIC, 1959-72
N. C. H. Lo1 and T. D. Smith2
ABSTRACT
The estimates of the number of dolphins killed annually from the beginning of the U.S. tuna purse seine
fishery in the eastern tropical Pacific are used by the National Marine Fisheries Service in developing
management advice for the U.S. purse seine fleet. We estimated the annual number of dolphins killed
incidentally in the tuna purse seine fishery for 1959-72. Kill data were available for only a few years prior
to 1970. Because no obvious trend was shown with the existing data, kill rates were averaged over those
years and stratified by various categories: large and small vessels, sets with large catch of tuna and small
catch of tuna, sets which used backdown (a dolphin-releasing procedure), and sets which did not use
backdown. These kill rates, combined with estimated number of sets, produced the estimated annual kills.
Because data were available only for some of the years, they had to be pooled to obtain annual estimates.
As a result, the annual estimates were highly correlated. Because the total as well as the annual estimates
are of interest, it is necessary to compute the variance-covariance of the estimated annual kills. The an-
nual kill from 1959 to 1972 varied from 55,000 in 1959 to 534,000 in 1961. There were three distinct
maxima of 534,000, 460,000, and 467,000, corresponding to peaks in number of sets made on dolphins
in 1961, 1965, and 1970. The total kill from 1959 to 1972 was estimated to be about 4.8 million, with
a coefficient of variation of 17%.
The eastern tropical Pacific tuna purse seine fleet
began to develop rapidly in the late 1950's and has
grown to over 100 U.S.-registered vessels and a
substantial number of non-U.S.-registered vessels in
recent years. This fleet fishes primarily for yellow-
fin tuna, Thunnus albacares, and skipjack tuna, Kat-
suwonus pelamis. Majority of the yellowfin tuna are
taken while the tunas are schooling with dolphins
primarily of the species Stenella attenuata and S.
longirostris. Birds and dolphins are frequently used
as cues in finding the tuna. During the capture of
the tuna, some of the dolphins are killed or drown-
ed by becoming tangled in the net webbing (Perrin
1969). The number of dolphins killed has been
estimated to have been greater than one-half million
in some of the years in the 1960's (Smith 1983). Cur-
rently, fewer animals are killed each year due to im-
provements in the fishing gear and in procedures to
release dolphins.
Estimates of the total number of dolphins killed
each year in this fishery are used as a basis for
management advice by the National Marine
Fisheries Service (NMFS). In this paper we describe
in detail the method used in Smith (1983), including
estimation of the variances and covariances of the
annual kill estimates so that the variance of the total
kill for the period can be estimated. Additionally, we
reexamine the data used in previous estimates (Per-
rin 1970; Perrin and Zweifel 19713; Perrin et al. 1982;
Smith 1983; Smith and Lo 1983), and we present
revised estimates of the total numbers of dolphins
killed.
MATERIALS AND METHODS
The model used to estimate the total annual in-
cidental kill of dolphins (Tt) in the eastern tropical
Pacific tuna purse seine fishery is
Tt = RtXt
(1)
where t denotes the year (1959 to 1972), R denotes
the number of dolphins killed per set, and X denotes
the number of sets made involving dolphins. The rate
of kill (R) varies between larger and smaller vessels,
and in dolphin sets where fewer and greater amounts
of yellowfin tuna are caught (Lo et al. 1982). In addi-
tion, the rate of dolphin kills is generally less if
Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, 8604 La Jolla Shores Drive, La
Jolla, CA 92038.
2Northeast Fisheries Center Woods Hole Laboratory, National
Marine Fisheries Service, NOAA, Woods Hole, MA 02543.
Manuscript accepted February 1985.
FISHERY BULLETIN: VOL. 84, NO. 1, 1986.
3Perrin, W. F, and J. R. Zweifel. 1971. Porpoise mortality in
the eastern tropical tuna fishery in 1971. Unpubl. manuscr., 22 p.
Southwest Fisheries Center La Jolla Laboratory, National Marine
Fisheries Service, NOAA, 8604 La Jolla Shores Drive, La Jolla, CA
92038.
27
FISHERY BULLETIN: VOL. 84, NO. 1
backdown, a dolphin-release procedure, is used
(Green et al. 1971; Barham et al. 1977; Smith and
Lo 1983). lb account for these factors affecting rates
of dolphin kill, Equation (1) can be reexpressed with
the rates and numbers of sets stratified by vessel
tuna carrying capacity, catch of fish, and use of back-
down procedure:
ft-ZIZ
1=1 y=i a-=i
Ktijk Xfijk
(2)
where t
i
J
k
year
1 for vessel capacity >600 tons; 2 for
vessel capacity <600 tons
1 for yellowfin tuna catch >lk ton; 2 for
yellowfin tuna catch <lk ton
1 backdown is used; 2 backdown is not
used.
Data on the number of dolphins killed during
fishing trips in the period from 1964 to 1968 are
given in Smith and Lo (1983). Similar but more ex-
tensive data (eg, backdown information) are avail-
able in NMFS records for 1971 and 1972. Estimates
on the number of sets involving dolphins from 1959
to 1972 are given by Punsley (1983). These data
sources have certain limitations which do not allow
for the use of the complete stratification scheme in
Equation (2). Assumptions are made based on sam-
ple sizes and on apparent lack of changes in rates
over time to accommodate these limitations.
The mean numbers of dolphins killed (kill-per-set)
are shown in Table 1 for each year in which data are
available, stratified by vessel size and by catch of fish
(successful, >lk ton of yellowfin tuna; unsuccessful,
<lk ton of yellowfin tuna). The definition of suc-
cessful set follows that of Perrin and Zweifel (fn. 3).
The vessel class stratification was based on the
vessel's fish carrying capacity. The 1964-74 kill data
indicate that kill-per-set was different for vessels
with <600 tons carrying capacity and vessels with
>600 tons for unsuccessful sets. For successful sets
the optimal vessel class stratification was not clear;
either 400, 600, or 800 tons can be used as division
points for stratification. For consistency, we adopted
the same stratification used for unsuccessful sets.
(The results were similar with alternative stratifica-
tion schemes.) Other factors such as the age of the
vessel and the experience of the captain could af-
fect kill rates but were not considered in the
stratification because these factors could not be
isolated for analysis.
The mean number of dolphins killed varied
markedly over the years but without any obvious
trends (Table 1). A two-way analysis of variance with
the data pooled over years showed statistically
significant differences in kill rates in sets made by
small and large vessels (P < 0.01) and in successful
and unsuccessful sets (P < 0.01). Thus Equation (2)
was simplified by eliminating the time stratification
for kill rates, whereas the vessel size and catch strata
were retained.
Few observations are available for sets where
backdown was not used. In successful sets, backdown
was used more than 90% of the time; thus, we have
observations on kill rates in only 20 sets where back-
down was not used. Thirteen of these sets were made
by large vessels and seven by small vessels, and the
mean kill rates within vessel size class are highly
variable and not significantly different. The overall
ratio of the kill rates, pooled over vessel size, when
backdown was not used and when it was used is
significantly greater than unity, and the annual
Table 1. — Average numbers of dolphins killed (M) in purse seine sets in the eastern tropical Pacific by
year, for small and large vessels making successful (>1A ton tuna) and unsuccessful (<1A ton tuna) net
sets. Standard deviation (SD), number of sets (A/), and number of trips are given.
Successful sets
Unsuccessful sets
and
No. of
No. of
year
M
SD
N
trips
M
SD
N
trips
Data source
Small vessels (<600 tons
1964 60 47
1965 26 28
1968 130 114
1971 117 180
carrying capacity)
20 1
35 1
13 1
19 3
60
3
4
13
8
4
10
1
11
2
3
1
1
1
2
Smith and Lo (1983)1
Smith and Lo (1983)
Smith and Lo (1983)
Unpubl. NMFS
1972
57
110
103
6
4
10
16
5
Unpubl. NMFS
Total
62
108
190
12
6
13
33
10
Large vessels (>600 tons
1971 41 56
carrying capacity)
16 2
0
Unpubl. NMFS
1972
37
123
117
6
0.4
1.4
12
5
Unpubl. NMFS
Total
37
119
133
8
0.4
1.4
12
5
'From table 5 of Smith and Lo (1983), omitting incomplete data collected in 1966.
28
LO and SMITH: INCIDENTIAL MORTALITY OF DOLPHINS
ratios vary without a consistent trend over time
(Table 2).
In unsuccessful sets the use of the backdown pro-
cedure was more variable because the conditions of
the set are more diverse For example, only a few
or no dolphins may be captured, and the net may not
be retrieved in the usual manner. Because of this
diversity and because so few observations are avail-
able, we consider one kill rate for all unsuccessful
sets.
Reexpressing Equation (2) to account for a
constant ratio of kill rates for successful sets when
backdown was used and when it was not used, and
for no difference in kill rates for unsuccessful sets,
yields
Mil
i=i y_i k-1
■K'ijk-X-tijk
= 2. l^nll V^till + CXH12) + R.i2.Xtl2.) (3)
1=1
where C = R..l2IR,.n and the subscript . is used
when that stratifying variable is not considered. For
example, R.^ is the kill-per-set not stratified by
year t, and XH2. is the total number of sets not
stratified by use of backdown.
Estimates of the total number of sets involving
dolphins from 1959 to 1972. with approximate
variances, are given by Punsly (1983). He also gives
partial estimates of the numbers of successful and
unsuccessful sets, but does not provide estimates of
the numbers of sets by vessel size Punsly's data did
not indicate the use of the backdown procedure
The coefficients of variation (CV) of Punsly's
estimates are <1% in all years except 1959 and 1960,
when it was 8%. The percentage of unidentified sets
in 1959-61 was higher than subsequent years because
set type was not recorded systematically
(Hammond4). We assume these estimates are in fact
constants, because in most years, and in the absence
of additional information in 1959-61, the CVs are
small compared with the CVs of the kill rates
(0.13-1.0, Table 1).
By applying the proportions of successful and un-
successful dolphin sets from Punsly's partial
estimates to his totals, we obtained numbers of suc-
cessful and unsuccessful dolphin sets. We further
prorate these estimated numbers of successful and
unsuccessful sets to large and small vessels by
multiplying by the estimates of proportions from
NMFS (Anonymous 19765) of sets made by vessels
of each size class (Table 3). The slight differences
between the totals for each year given by Punsly are
due to rounding.
The number of sets during which backdown was
used can be estimated from the estimated total
number of sets involving dolphins (Table 3) and the
observed proportion of successful sets in which back-
down was used (Table 2). The observed proportions
increase from 0.79 in 1964-65 to almost unity (0.96)
by 1972. The backdown procedure was reportedly
4P. S. Hammond, Sea Mammal Research Unit, British Antarctic
Survey, Cambridge, England, pers. commun. 1983.
6Anonymous. 1976. Report of the workshop on stock assess-
ment of porpoises involved in the eastern Pacific yellowfin tuna
fishery (La Jolla, July 27-31, 1976). Southwest Fish. Cent., Ad-
min. Rep. LJ-76-29, 54 p. + app.
Table 2. — Mean number of dolphins killed (R) during purse seine sets in the eastern tropical
Pacific Ocean when the backdown dolphin-release procedure was and was not used. Also
given are the ratio of numbers killed with and without backdown (C), the proportion of suc-
cessful sets where backdown was used (P), the number of sets (A/), number of trips, and stan-
dard error in parentheses.
Backdown used
Yes
No
No. of
No. of
Year
"mi
N
trips
°M2
N
trips
C
P
1964'
44
16
1
128
4
1
3.0
0.79
19651
48
6
1
24
2
1
0.50
19661,2
—
17
1
—
2
1
—
0.89
19681
142
11
1
92
1
1
0.65
19713
81
30
5
111
4
3
1.40
19723
41
193
12
169
9
6
4.10
0.96
Total
50
256
21
131
20
12
2.62
"(0.80)
0.93
1From Smith and Lo (1983).
2Kill rates tor 1966 omitted because incomplete data were collected.
3NMFS records.
<SE(£) = 6 [CV2(rt..12) + C\z2(tf.#11) - 2cor(A..12, 4..11)]1'2; where C = A..12ff).a11.
29
FISHERY BULLETIN: VOL. 84, NO. 1
Table 3. — Numbers of purse seine sets involving dolphins
in the eastern Pacific Ocean, from 1959 to 1972, for small
(<600 tons) and large (>600 tons) vessels, and for successful
(>1/» tons tuna) and unsuccessful (<1/4 tons) sets, modified
from Punsly (1983).
Successful sets
Unsuccessful sets
small
large
small
large
Year
PW
(*m.)
(*f22»)
(*fl2.)
1959
326
0
265
0
1960
3,170
0
2,303
0
1961
3,888
32
3,928
0
1962
1,773
5
1,942
19
1963
2,291
10
2,092
23
1964
4,444
45
3,089
64
1965
5,346
27
2,418
29
1966
4,948
44
1,835
25
1967
3,363
2
841
3
1968
2,956
175
982
41
1969
5,365
1,401
1,402
192
1970
4,936
2,313
957
412
1971
1,871
2,602
652
409
1972
2,704
4,982
855
846
developed on one vessel in 1959-60 (Barham et al.
1977) and used by at least three vessels in 1961
(Anonymous 1962). If 79% of the sets in 1964-65
were made using this procedure, as suggested by the
very limited available data, a rather rapid increase
in usage must have occurred in 1962 and 1963. This
is possible because, if properly used, the procedure
reduces the amount of handling time of dead
dolphins, thus speeding up the fishing operation. As
an approximation, we assume that usage increased
from 0 to 0.79 linearly from 1959 to 1964-65, and
was 0.89 for 1966-71 and 0.96 for 1972.
Denoting the interpolated and extrapolated esti-
mates of the proportion of successful sets using the
backdown dolphin release procedure by Pt gives
Xtill - Pistil,
Xtii2 = (1 - Pt) Xti\»-
Substituting these relationships into Equation (3),
with the assumption that the estimated numbers of
sets given by Punsley (1983) are constants, the
following equations result when the terms are
rearranged:
Tt = X {P'in[xtii*Pt + C(l - PtV^tii'] + P'i2»Xti2»}
i
= Z \R'illXtil»[Pt + C(l - PJ\ + P'i2'Xti2.\.
i
(4)
The time series of estimated annual kill (tt) from
1959 to 1972 was obtained by pooling the available
data over years and strata, resulting in estimates that
are not statistically independent. Thus in order to
estimate the variance of the total kill of dolphins for
the period in addition to the variances it is necessary
to determine the covariances among the annual
estimates.
We denote the estimates of the total kill of dolphins
(ft) for each year from 1959 to 1972 by the vector
f, and denote the estimates of the variances of the
elements of f by the symmetric matrix If. The
estimate of the kill in each year (Equation (4)) can
be expressed in matrix form as the product of a vec-
tor of the numbers of sets in each of the four com-
binations of the vessel size and fishing success
classifications (Xt), and a vector of the four corre-
sponding kill rates (Qf). Each element of T then can
be expressed as a matrix product
Tt = X\ Qt
(5)
where X't = (Xtn„ Xm„ Xnz„ XtZ2.)
Qt =
Qn
Qt2
Qt3
Qa
R.in[Pt(i -Q + C]
R.2n[Pt(l -Q + C]
R»\2»
R. 22.
P'inft
P»21lft
K*\2*
R*22*
and /, = P,(l - 6) + C.
Then the variance-covariance matrix of T is
30
LO and SMITH: INCIDENTAL MORTALITY OF DOLPHINS
Zr =
V(T59)
Cov(T59, f60) V(f 60)
Cov(f 59, f 72) Cov(f60, f72) . . . V(f 72)
V(X'59 Q59)
Cov(Z'59 Q59, X'60 Q60) V(X'60 Q60)
Cov(X'59 Q59, X'12 Q72) Cov(X'60 Q60, X'72 Q72) . . . V(X'72 Q72)
with VCfy = X'flQtXt
as the diagonal elements of If
(6)
where 1qt =
V(R.inft)Cov{R.ulft,R.2nft) 0 0
V&.211 ft) o o
^.21.) 0
V(R.22.)
(7)
The diagonal elements of If can be computed by
noting that R,i2. is uncorrelated with R.in, Pt, or C,
and the covariance of Pt and C is zero because one
C value is used for all years in 1959-72 and Pt can
be different between years.
The off-diagonal elements of If are
Cov(t „ tj = CovPT'A, X'mQm)
4 4
= 11^ Cov(QMJ, Qmj) X„
i=i i=i
(8)
,mj) ■"■my
Expressions for each of the terms in If are given
in the Appendix.
RESULTS AND DISCUSSION
The estimates of the total number of dolphins
killed incidentally in the tuna purse seine fishery
from 1959 to 1972 (Table 4, from Equation (4)) vary
from a low of 55,000 in 1959 to a high of 534,000
in 1961. Three distinct maxima of 534,000, 460,000,
and 467,000 are apparent (Fig. 1), corresponding to
peaks in numbers of sets made on dolphins in 1961,
1965, and 1970 (Table 3). A total of about 4.8 million
dolphins is estimated to have been killed in the whole
period (Table 4).
The CVs of the annual estimates decline rapidly
Table 4.— Estimated number of dolphins
killed by year (Equation (4)), with standard
errors (SE) and coefficient of variations
(CV).
Year
Number killed
SE
CV
1959
55,000
18
0.32
1960
478,000
146
0.31
1961
534,000
149
0.28
1962
216,000
54
0.25
1963
240,000
54
0.22
1964
390,000
77
0.20
1965
460,000
92
0.20
1966
374,000
58
0.15
1967
257,000
39
0.16
1968
229,000
35
0.15
1969
461,000
68
0.15
1970
467,000
70
0.15
1971
254,000
43
0.17
1972
380,000
61
0.16
1959-72
4,790,000
857
0.18
31
FISHERY BULLETIN: VOL. 84, NO. 1
800 r
700 -
600
c
a
M
3
o
£ 500 -
z
400
O
a
"- 300
O
K
Ul
CD
2
z
200
100
J l_
_l_
_l_
JL
_1_
1959 60 61 62 63 64 65 66 67 68 69 70 71 72
YEAR
Figure 1.— Estimated numbers of dolphins killed in the east-
ern tropical Pacific tuna purse seine fishery from 1959 to 1972.
Standard errors of the estimates shown as vertical bars. From Table
4.
from 32% in 1959 to 15% from 1966 to 1970, and
then increase only slightly in 1971 and 1972. The
covariances are large (upper triangular matrix, Table
5). They are all positives, and tend to be smaller for
pairs of estimates widely spaced in time The
covariances can be examined more easily in terms
of correlation coefficients (lower triangular matrix,
Table 5). The correlations range from 0.31 to 0.99.
The CV of the estimated total is 18%. This is
substantially higher than the corresponding value
of 6% obtained when the covariances are ignored.
Because the total is the sum of 14 numbers, an ap-
proximate 95% confidence interval, obtained by add-
ing and subtracting two standard errors, is 3.1-6.5
million dolphins.
The variation in the estimated numbers of dolphins
killed over the period 1959-72 is due to several fac-
tors: 1) The number of sets made involving dolphins
varied from year to year depending on the number
of sets of tuna schooling in the absence of dolphins;
such tuna are apparently preferred when available
2) The use of the backdown dolphin-release pro-
cedure increased rapidly from 1959 to 1964. How-
ever, the development of the backdown dolphin-
release procedure is not well known. The available
data reflect the tendency of captains to use the
technique once it was known. There is little infor-
mation on how rapidly the procedure became known
to other captains and no information on how rapid-
ly they learned to use it effectively. Our assumption
of a linear increase probably overestimates the use
of backdown initially, but may or may not overesti-
mate its subsequent use 3) The proportion of suc-
cessful sets made by small vessels increased from
about 50% from 1959 to 1964, to >75% from 1965
to 1972 (Table 1). The higher dolphin kill rate for suc-
cessful sets results in an increase in estimated
dolphin kills as the proportion of successful sets in-
creased. 4) The increase in the proportion of sets
which were made by large vessels starting in 1968
results in a decrease in estimated dolphin kill rates
due to the lower dolphin kill rate of these vessels.
Several factors which may have affected the
numbers of dolphins killed in this period have not
been accounted for because of the assumptions made
by incomplete data. Chief among these assumptions
were 1) the relatively small samples are represen-
tative of the fleet as a whole 2) the kill rates on un-
successful sets are not affected by the use of back-
down, 3) the ratio of kill-per-set in successful sets
without backdown to that with backdown is constant
Table 5.-
-Covariances (upper triangular matrix, x1010) and correlation coefficients (lower triangular matrix) for the
estimated total dolphins killed by year, from 1959 to 1972.
1959
1960
1961
1962
1963
1964
1965
1966
1967
1968
1969
1970
1971
1972
1959
0.41
0.42
0.14
0.13
0.16
0.15
0.11
0.07
0.06
0.13
0.13
0.06
0.04
1960
0.99
3.49
1.24
1.15
1.37
1.32
0.92
0.62
0.56
1.10
1.08
0.54
0.40
1961
0.99
0.99
1.27
1.19
1.45
1.38
0.95
0.64
0.57
1.13
1.11
0.55
0.42
1962
0.97
0.98
0.99
0.44
0.55
0.52
0.34
0.23
0.21
0.41
0.40
0.19
0.15
1963
0.92
0.94
0.96
0.98
0.58
0.53
0.33
0.22
0.20
0.39
0.38
0.18
0.15
1964
0.76
0.79
0.83
0.88
0.95
0.75
0.43
0.29
0.26
0.50
0.49
0.23
0.20
1965
0.79
0.81
0.84
0.88
0.92
0.93
0.56
0.34
0.27
0.51
0.50
0.23
0.20
1966
0.65
0.66
0.67
0.67
0.67
0.62
0.86
0.30
0.21
0.39
0.38
0.17
0.16
1967
0.75
0.76
0.77
0.78
0.78
0.71
0.89
0.93
0.16
0.30
0.29
0.13
0.10
1968
0.74
0.75
0.76
0.77
0.76
0.70
0.77
0.69
0.90
0.31
0.30
0.14
0.10
1969
0.73
0.74
0.75
0.76
0.75
0.68
0.75
0.66
0.87
0.98
0.63
0.33
0.27
1970
0.71
0.72
0.73
0.73
0.72
0.65
0.70
0.62
0.83
0.94
0.98
0.36
0.38
1971
0.58
0.59
0.59
0.59
0.57
0.50
0.54
0.46
0.63
0.75
0.85
0.92
0.25
1972
0.34
0.35
0.36
0.36
0.36
0.34
0.37
0.34
0.39
0.43
0.55
0.65
0.83
32
LO and SMITH: INCIDENTIAL MORTALITY OF DOLPHINS
for both large and small vessels for all years, and
4) the kill rate itself for sets with backdown did not
change over the years.
Although each of the unaccounted for factors could
have an effect on the estimated numbers of dolphins
killed, the magnitude of such effects is probably
smaller than the magnitude of the effects of vessel
size, set success, and use of backdown described in
this study. For example, although the kill rate data
available are few, there are some additional data
which are not available to us, but which are reported-
ly similar (Smith and Lo 1983). The last three
assumptions noted above deal with the dolphin kill
rates with and without backdown, and would tend
to both increase and decrease the estimates, if they
could be taken into account.
Our estimates of the total number of dolphins
killed (Table 4) are slightly lower than previous esti-
mates made using the same method (Smith 19796,
1983). The previously estimated total number of
dolphins killed from 1959 to 1972 was 5.1 million
(total of Smith's [1983] table 4, divided by 0.96 for
other species and by 1.048 for injured animals). The
difference between the two estimates resulted from
the revision of the estimated number of sets that cap-
ture tuna associated with dolphins (Punsly 1983) and
of the numbers of dolphins killed per set (Smith and
Lo 1983).
There are alternate approaches to estimating the
numbers of dolphin killed. For example, estimates
could be made from data on the numbers of fishing
trips made (kill-per-trip), or the number of tons of
tuna caught (kill-per-ton). These approaches make
different assumptions about the fishing process (Lo
et al. 1982; Hammond and Tsai 1983), and require
data which are not as precise as are data on the total
numbers of sets. For example, fishing trips are dif-
ficult to count consistently because they may not be
completed within the calendar year and may be ex-
6Smith, T. D. (editor). 1979. Report of the Status of Porpoise
Stocks Workshop, August 27-31, 1979, Southwest Fisheries Center,
La Jolla, California Southwest Fish. Cent., Admin. Rep. LJ-79-41,
120 p.
tended by partial unloading of the catch. There are
fewer such problems with the data for kill-per-set
estimators on the number of dolphins killed, and the
problems that exist have already been resolved
(Punsley 1983).
LITERATURE CITED
Anonymous.
1962. How tuna seining paid off for the U.S. fleet in 1961.
Fish Boat, Feb., p. 19-30.
Barham, E. G., W. K. Taguchi, and S. B. Reilly.
1977. Porpoise rescue methods in the yellowfin purse seine
fishery and the importance of Medina panel mesh size Mar.
Fish. Rev. 39(5): 1-10.
Green, R. E., W. F. Perrin, and B. P. Petrich.
1971. The American tuna purse seine fishery. In Hilmar
Kristjonsson (editor), Modern Fishing Gear of the World, Vol.
3, p. 182-194. Fish. News (Books) Ltd., Lond.
Hammond, P. S., and K. T. Tsai.
1983. Dolphin mortality incidental to purse-seining for tunas
in the eastern Pacific Ocean, 1979-81. Rep. Int. Whaling
Comm. 33:589-597.
Lo, N. C. H., J. Powers, and B. E. Wahlen.
1982. Estimating and monitoring incidental dolphin mortality
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.
1969. The problem of porpoise mortality in the U.S. tropical
tuna fishery. Proceedings of the 6th Annual Conference on
Biology, Sonar, and Diving Mammals, p. 45-48. Stanford
Research Institute
Perrin, W. F, T. D Smith, and G. T. Sakagawa.
1982. Status of populations of spotted dolphin, Stenella at-
tenuate/,, and spinner dolphin, S. longirostris, in the eastern
tropical Pacific In FAO, Mammals in the seas, Vol. IV. Small
cetaceans, seals, sirenians, and otters, p. 67-83.
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. Inter-Am. Trop. Tuna Comm. Bull. 18:229-
299.
Smith, T D.
1983. Changes in size of three dolphin (Stenella spp.) popula-
tions in the eastern tropical Pacific Fish. Bull., U.S. 81:1-14.
Smith, T. D, and N. C. H. Lo.
1983. Some data on dolphin mortality in the eastern tropical
Pacific tuna purse seine fishery prior to 1970. U.S. Dep.
Commer., NOAA Tech. Memo. SWFC-TM-NMFS-34, 26 p.
33
FISHERY BULLETIN: VOL. 84, NO. 1
APPENDIX
In Equation (7), the first and second terms on the main diagonal are
V(R.tllft) = V(R.lU)V(f<) + R2.mV(ft) + fMR.m) (A-l)
for i = 1 and 2, noting that Cov(R.!Uft) = 0.
The variance of ft is given by
V(A) = V(Pt) (1 + V(Q) + Pf V(Q (A-2)
+ &V(Pt) + V(C) - 2V(P,)C
- 2V(C)Pf + 2 Cov(Pt, Q.
This last term is assumed to be zero, as noted above. The off-diagonal element in Equation
(7) is
Cov(R.lUft, R.jnft) = R.m R.JU V(ft) (A-3)
for i ¥= j = 1 and 2.
In Equation (8), based upon Equation (5)
Cov(Qm, Qmj) =
CovtR.,!
fui
R.fl
i/J
for i =
and j =
- 1,2
= 1,2
0
i ±j
for i =
= 3,4
VCR.*,.)
i = j
and j =
= 3,4
where Cov(R.m fu, R.ju fm) (A-4)
[R%u + V(R.jU)]Cov(fu, fm) + fufmV(R.m) i = j
R-iuR.ju Cov(/M, /J i # j
assuming Cov(R.ai, R.jn) = 0
and Cov(/M, /J = Cov(PM, Pm) [V(Q + C2] (A-5)
+ V(Q.[1 + AA -Pu ~Pml
34
THE ABUNDANCE AND DISTRIBUTION OF
THE FAMILY MACROURIDAE (PISCES: GADIFORMES)
IN THE NORFOLK CANYON AREA1
Robert W. Middleton2 and John A. Musick3
ABSTRACT
The Norfolk Canyon off Virginia and the adjacent slope areas were sampled with 13.7 m otter trawls
in June 1973, November 1974, September 1975, and January 1976. Trawl depths ranged from 75 to 3,083
m, and 22 species of macrourids were captured during the study. Coryphaenoides rupestris demonstrated
seasonal movement to shallower water (ca. 750 m) during winter. Nezumia bairdii, N. aequalis, and Cory-
phaenoides carapinus exhibited a significant positive correlation between head length and depth (r2 =
0.47, 0.37, and 0.35, respectively). Nezumia bairdii apparently spawns in July or August, and reaches
an age of about 11 years. New size records were established for Nezumia aequalis (64 mm head length
(HL)) and N. bairdii (66 mm HL). New depth records were established for Coelorinchus c. carminatus
and N. aequalis (884 and 1,109 m, respectively). The known geographic ranges for Coelorinchus carib-
beus, C. occa, Nezumia cyrano, Coryphaenoides colon, Hymenocephalus gracilis, H. italicus, Bathygadus
macrops, Macrourus berglax, and Gadomus dispar were extended to the Norfolk Canyon area.
The Macrouridae (Pisces: Gadiformes) includes some
of the most abundant archibenthic deep-sea fish
species (Marshall 1965, 1971; Marshall and Iwamoto
1973; Iwamoto and Stein 1974) and attains greatest
abundance and diversity on the continental slopes
of the world oceans (Marshall and Iwamoto 1973).
Present knowledge of the life history and ecology
of macrourids has been accrued piecemeal from
faunal lists and taxonomic works (Gunnerus 1765;
Gunther 1887; Gilbert and Hubbs 1920; Farron 1924;
Iwamoto 1970; Okamura 1970; Marshall and
Iwamoto 1973; Iwamoto and Stein 1974), or from
studies on physiology, anatomy, and life history
(Kulikova 1957; Marshall 1965; Phleger 1971; Ran-
nou 1975; Rannou and Thiriot-Quiereaux 1975;
Haedrich and Polloni 1976; McLellan 1977; Merrett
1978; Smith et al. 1979). The meager literature on
reproduction and growth of macrourids and other
deep-sea anacanthine fishes has recently been
reviewed by Gordon (1979). With the advent of in-
creasing expertise in deepwater trawling, some
macrourid species, such as Coryphaenoides rwpestris
and Macrourus berglax, have become commercially
•Contribution No. 1226 from the Virginia Institute of Marine
Science.
2Virginia Institute of Marine Science, College of William and
Mary, Gloucester Point, VA 23062; present address: Minerals
Management Service, U.S. Department of the Interior, 1951 Kidwell
Drive, Vienna, VA 22180.
3Virginia Institute of Marine Science, College of William and
Mary, Gloucester Point, VA 23062
important in the western North Atlantic. Experi-
mental commercial trawling was initiated by the
Soviet Union in 1962, and many studies directly
related to the commercial fishing of macrourids have
been subsequently published by Soviet workers
(Podrazhanskaya 1967, 1971; Sawatimskii 1971,
1972; Grigor'ev 1972) and to a lesser extent by Polish
researchers (Stanek 1971; Nodzinski and Zukowski
1971).
The present study examines the seasonal distribu-
tion and abundance of the macrourid species cap-
tured in the Norfolk Canyon area. In addition aspects
of age, growth, and reproduction of selected domi-
nant species are also described.
MATERIALS AND METHODS
Gear
The data presented in this paper were obtained
on four cruises to Norfolk Canyon and the adjacent
open slope to the south (Fig. 1) conducted by the RV
Columbus Iselin (June 1973) and RV James M. Gillis
(November 1974, September 1975, January 1976).
On all cruises a 13.7 m semiballoon otter trawl with
1.3 cm (stretched) mesh in the cod end liner and 5.1
cm (stretched) mesh in the wings and body was
employed. Steel "china V" doors at the end of 22.9
m bridles were used to permit spreading of the net
from a single warp (Musick et al. 1975).
Manuscript accepted March 1985.
FISHERY RIILLETIN: VOL. 84. No. 1. 1986.
35
FISHERY BULLETIN: VOL. 84, NO. 1
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Figure 1— Map of the Norfolk Canyon study area with station
73*30'
locations indicated.
73*00'
Sampling Design
Norfolk Canyon and an adjacent open slope were
divided into five sampling strata: 75-150 m, 151-400
m, 401-1,000 m, 1,001-2,000 m, and 2,001-3,000 m.
Six stations were then randomly assigned in each
depth stratum. The duration of all tows in depths
of <2,000 m was 0.5 h (bottom time). Where the
depth exceeded 2,000 m, the tow times were ex-
tended to 1 h. Station depth was determined from
a sonic precision depth recorder when the net was
set and then every 3 min for the duration of the 0.5
h tows (every 6 min for the 1-h tows). Mean station
depth was then determined by averaging the 11
resultant values.
Data Collection and Analysis
Head lengths instead of total lengths were
measured because macrourids have slender whiplike
tails that are easily damaged during trawling. The
head length (HL) was measured to the closest
millimeter, from the tip of the snout to the posterior
edge of the opercle using Helios4 dial calipers. The
fish were weighed with an Ohaus dial-a-gram scale
Calibration showed the scale to be accurate within
■•Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
1.0-1.5 g under all typical shipboard conditions.
The sex and gonadal conditions of freshly captured
specimens were noted. Gonadal samples for histo-
logical processing were stored in Davidson's preser-
vative and later mounted using standard paraffin
techniques. Sections (5 mm) were stained with
Mayer's hematoxylin and eosin counterstain.
Saccular otoliths and a scale sample were removed
from all Nezumia bairdii and stored dry. Represen-
tative otolith samples were chosen randomly from
individuals over the entire size range of fish
captured.
The length-weight relationships for Nezumia bair-
dii, Coryphaenoides armatus, and C. rupestris were
analyzed using log transformed weights regressed
against head length (Fig. 2).
Regression analysis of head length on depth of cap-
ture was performed for each species to determine
any significant change in head length with change
in depth. Testing of the hypothesis that fi = 0 for
the regression line ascertained whether there was
a significant change of size with changing depth. The
coefficient of determination (r2) was also calculated
to determine what proportion of the variance of head
length could be attributed to change in depth.
The a posteriori Student-Newman-Keuls analysis
of means was used as a second method for inter-
preting the size/depth relationship. This method
calculated the mean depth of capture of each head-
36
MIDDLETON and MUSICK: ABUNDANCE AND DISTRIBUTION OF MACROURIDAE
length interval, combined the head lengths in subsets
whose mean depths did not differ significantly from
each other, and defined the constituents of each
subset.
Due to the large size and thickness of the macrou-
rid otoliths, standard age determination techniques
proved unsuccessful (Christensen 1964; McEachran
and Davis 1970). Therefore, a thin section was re-
moved from each otolith and, using a dissecting
microscope, the number of bands presumed to be an-
nual were counted and recorded.
Gonads of the specimens were classified into repro-
ductive stages for analysis. The criteria for these
stages were as follows:
Stage 1— Undeveloped. The gonads were immature
and no development was evident. The reproduc-
tive organs were difficult to distinguish within the
body cavity.
Stage 2— Early Immature The reproductive organs
had enlarged slightly. The sex could be determined,
but no vascularization of the ovaries was apparent.
The organs of both sexes had a highly translucent
appearance.
Stage 3— Immature The ovaries were enlarged and
vascularization had begun. The testes had become
discernibly "sausage shaped". The organs of both
sexes were opaque.
Stage 4— Late Immature The reproductive organs
of both sexes were full size The ovaries were about
90% vascularized. The testes had become milky
white in color.
Stage 5— Mature The reproductive organs were
developed completely. Ovaries were fully vascular-
ized and had a granular appearance.
Stage 6— Ripe. Advanced spermatogenesis or
oogenesis was evident. The oocytes were fully
developed in the females and the male testes con-
tained milky-white seminal fluid.
Stage 7— Spent. The testes and ovaries were spent.
The reproductive organs were flaccid and had
recently released sperm or eggs.
RESULTS AND DISCUSSION
Species Accounts
Coelorinchus c. carminatus (Goode 1880)
Coelorinchus c. carminatus is a relatively shallow
water macrourid reported from depths of 89-849 m
(Marshall and Iwamoto 1973). In the study area this
species was captured in depths of 210-884 m (Fig.
3). Marshall and Iwamoto (1973) reported C. c. car-
minatus from northern Brazil to the Grand Banks,
but absent in the Bahama Island chain. The largest
specimen captured in our study had a head length
of 70 mm, while Marshall and Iwamoto (1973)
reported specimens with 73 mm HL.
During our study, a maximum of 188 individuals
and 4 kg of C. c. carminatus were captured in a 0.5-h
trawl. This species also contributed as much as 34.2%
of the number and 27.8% of the biomass of benthic
fishes captured in individual samples.
Figure 4 shows the depth distribution of C. c. car-
minatus incremented by 2 mm size groups. A slight
increase in head length with increase of depth was
apparent. The slopes of the regression lines were
shown to be significantly different from zero. The
coefficient of determination (Table 1) also showed a
correlation between head length and depth. There
was variability among cruises, but this may be at-
_ 2
S
o
o"n = 305
? n = 422
Coryphaenoides armatus
-i 1 1 r
-i r
~r
d*n = 156
$ n = 279
Coryphaenoides rupestns
0 10 20 30 40 SO 60 O 10 20 30 40 SO 60 70 80 90 100 0
HEADLENGTH (mm)
-i — i — i — i — i —
30 50
100
-I
ISO
200
Figure 2.— The log (wt) versus head length regressions for Nezumia bairdii, Coryphaenoides armatus, and Coryphaenoides rupestris.
37
FISHERY BULLETIN: VOL. 84, NO. 1
Figure 3— Minimum and maximum depth
of capture, with minimum, maximum, and
modal temperatures of capture for each
species and each cruise
A Coelonnchus C carminatus
<* A* A*3 Afc
D Nezumia bairdii
fi ,* .o* .
f> j* v5 A«,
SN
Depth M'n
'm > Man
2 52
260
210
226
..Min
Depth
(m.) Moi
270
315
277
310
776
750
828
884
1350
1525
1644
1470
_ Mm
Temp
(°C) Ma,
Mode
47
49
43
45
_ Mm
Temp
t°C) Ma<
Mode
4 1
4 1
37
37
II 3
106
II 1
110
IQO
96
92
7. 1
90
7 4
8 7
7 8
5 1
5.1
4.4
53
w Nezumia aequalis
>° o* o*
<b j> Jo jo'
0s
U Coryphaenoides rupestris
<5 A» J? Jo
Depth
(m) Moi
367
578
330
452
Depth Min
tmj Man
636
578
616
828
986
912
1109
884
1591
1525
1108
1698
Mm
Temp
(°C) Moi
Mode
45
45
43
4 3
Mm
Temp
(°C> Mo.
Mode
4 1
45
37
4 1
57
7.1
78
80
49
57
43
5.0
5 1
62
4 5
49
46
5.3.
4.0
48
t Coryphaenoides carapinus
,-e o" ,o* ,os
f> J* *{3 A«=
i Coryphaenoides armatus
,n° S>* ,o* .
<b y Vs A*
0N
r> ... Min
Depth
(m) Mat
1194
1403
1189
1108
Depth Min
(m) Mai
2100
2257
2250
1876
2642
2767
2679
2642
3083
2920
Mm
Temp
(°C) Ma.
Mode
3.5
2 9
2 5
2 9
Mm
Temp
(°C) Mo.
Mode
2.5
2 3
24
4.1
4 2
4 0
3 9
3.3
2 8
3 2
3 8
3 9
3 7
3 8
29
24
28
Table 1.— The coefficient of determination (r2) for the change in
head length with change in depth regression lines.
Cru
ses
Jan.
June
Sept.
Nov.
Combined
Species
76-01
73-10
75-08
74-04
cruises
Coelorinchus c.
carminatus
0.006
0.23
0.13
0.44
0.23
Nezumia
aequalis
0.45
0.15
0.62
0.14
0.37
Nezumia bairdii
0.12
0.50
0.44
0.49
0.47
Coryphaenoides
rupestris
0.04
0.19
0.08
0.11
0.02
C. carapinus
0.59
0.005
0.30
0.37
0.35
C. armatus
0.000
—
0.05
0.000
0.14
tributed to sampling artifacts and the relatively nar-
row depth range (674 m) of this species.
The analysis of variance showed a significant dif-
ference in mean depths of the head length groups
(F = 35.9, F(table; a . 0.01) = 1.79). The Student-
Newman-Keuls test divided the group into two
significantly different subsets; one 10-50 mm HL and
the other 51-70 mm HL.
Other macrourids (N. bairdii and N. aequalis) had
high biomass but low numerical abundance at the
deep end of their ranges, indicating the presence of
a few large specimens there This was not the case
for C. c. carminatus (Fig. 5). The occurrence of fish
distributing by size can be obscured if the larger
members of the population traverse the entire range
The biomass of the species would be elevated at the
shallower depths so that a consistent biomass level
is present throughout the depth range Comparison
of Figure 4 with Figure 5 shows that although the
mean depth of capture for this species increased with
head length, the larger fish occurred over the en-
tire depth range This pattern is important because
it shows that for some fishes the "bigger-deeper"
phenomenon described by Polloni et al. (1979) may
really be a "smaller-shallower" phenomenon. A plot
of mean fish weight against depth as used by Polloni
38
MIDDLETON and MUSICK: ABUNDANCE AND DISTRIBUTION OF MACROURIDAE
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FISHERY BULLETIN: VOL. 84, NO. 1
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Figure 5— The distribution of log transformed (log (x + 1)) abundance and weight of Coelorinchus c. carminatus at each station, plotted
against depth.
et al. (1979) may have a highly positive slope, but
these data are impossible to interpret without infor-
mation about length-frequency patterns with depth.
The temperatures at which C. c. carminatus were
captured varied from 4.3° to 11.3°C (Fig. 6). The
average temperature of collection was 7.6 °C.
Nezumia aequalis (Gunther 1878)
Nezumia aequalis is a closely related congener of
40
N. bairdii and is found primarily south of the study
area (Marshall and Iwamoto 1973). Nezumia ae-
qualis attains a head length of at least 53 mm and
has a depth distribution of 200-1,000 m. Its
Figure 6— The temperature range for each species, by cruise Th
dot designates the modal temperature, Ccc. - Coelorinchus
carminatus, N.b. - Nezumia bairdii, N.a. - Nezumia aequalis, C.i
- Coryphaenoides rupestris, Gc. - Coryphaenoides carapinus, C.s
- Coryphaenoides armatus.
MIDDLETON and MUSICK: ABUNDANCE AND DISTRIBUTION OF MACROURIDAE
12
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JANUARY 76-01
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SPECIES
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41
FISHERY BULLETIN: VOL. 84, NO. 1
geographic range is listed as from the Faroe bank
to northern Angola in the eastern Atlantic, the
Mediterranean, and from Davis Straits to northern
Brazil in the western Atlantic (Marshall and Iwamoto
1973).
In the Norfolk Canyon area the depth of capture
of N. aequalis was from 330 to 1,109 m. The greatest
number in a trawl was 40 in November of 1974, and
the highest biomass per trawl was 300 g in Septem-
ber 1975. Nezumia aequalis comprised up to 8.9%
of a trawl catch by number and 3.1% by weight. The
analysis of variance of the mean depths of the head
length groups gave a F value of 3.32 (F(table; a =
0.01) = 2.11). The Student-Newman-Keuls analysis
showed only one subset, probably because of the low
sample size Examination of Figure 7 suggests head
length increased with depth, and the slope of the line
was significantly different from zero.
Although its bathymetric range was extensively
sampled, densities were low and few mature speci-
mens were captured (Fig. 8). These findings are in
contrast to the distribution and abundance of its
cogener, N. bairdii, suggesting competitive exclu-
sion. Alternately, Norfolk Canyon populations ofN.
aequalis may represent expatriation from denser
populations in the Gulf of Mexico or on the Blake
Plateau.
The temperature range for N. aequalis captured
in the Norfolk Canyon area was from 4.3° to 8.0 °C
(Fig. 6). The average temperature of collection was
5.3°C.
Nezumia bairdii (Goode and Bean 1877)
Nezumia bairdii is a relatively small macrourid
with a reported head length of up to 60 mm (Mar-
shall and Iwamoto 1973). During our study the head
lengths varied from 12 to 66 mm with the weight
of the largest specimen being 295 g. The geographic
range of N. bairdii extends from the Straits of
Florida north to the Grand Banks (Marshall and
Iwamoto 1973). Nezumia bairdii is captured com-
monly between 90 and 183 m in the northern part
of its range and appears to undergo tropical sub-
mergence because it is found primarily between 548
and 731 m in the southern parts of its range The
inclusive depth range is 90-2,285 m (Goode and Bean
1885; Marshall and Iwamoto 1973). One anomalous
catch at a depth of 16.5 m was recorded in Vineyard
Sound (Bigelow and Schroeder 1953), but this was
most likely a discard from a commercial fishing
vessel.
Within the study area the depth of capture ranged
from 270 to 1,644 m (Fig. 3). The largest catch in
a half hour tow was 76 fish and the greatest biomass
per half hour tow was 5.7 kg. Nezumia bairdii com-
prised up to 30% of the demersal fish catch in
number and up to 15% of the biomass.
In the January plot (Fig. 9), the head length in-
creased slightly with depth. The regression line of
the mean depth of each head length class showed
a positive slope significantly different than zero. By
June (Fig. 9) the regression line showed a highly
significant positive slope and three distinct size
groups separated by depth were evident. The first
group included those fish <30 mm HL, the second
group was from 30 to 42 mm HL, and the third group
was >43 mm HL. The head lengths at the start of
maturity for females (27 mm) and males (32 mm) cor-
respond well with the dividing line between size
groups one and two, as defined by depth distribu-
tion. Also, N. bairdii females and males can be fully
mature at 44 and 45 mm HL, respectively (Fig. 10).
These values are close to the division between the
second and third size groups noted above The three
size groups appear to reflect maturity stages as well
as size differences, and this may contribute to the
bathymetric differences. The first group consisted
of all immature fish that were not found in deep
water in June The second group could be termed
the transitional group because it included fish that
were just starting to mature and those more highly
developed. Since this group included such a diverse
spectrum of maturity, it encompassed portions of the
depth ranges of both immature and mature fish. The
third group consisted of all mature fish and was not
found in water shallower than approximately 600 m
in June In September, the larger fish had reached
their deepest limit, and immature N. bairdii were
virtually absent deeper than 1,000 m. By November
(Fig. 9), the largest fish were returning to shallower
water to complete what appears to be a seasonal
migration cycle
Examination of histological sections of gonads
showed that the only spent N. bairdii were captured
on the September cruise Although no ripe fish were
caught on any cruise, these spent fish suggest that
N. bairdii spawns in July or August, coincident with
the time when the mature fish are inhabiting their
deepest level.
Marshall's (1965) hypothesis concerning reproduc-
tion of certain macrourids states that fertilization
takes place at the bottom. Subsequently the eggs,
which are buoyant, develop and hatch on their way
upward to the seasonal thermocline The larvae then
maintain themselves just below the thermocline, in
order to take advantage of the plankton that tends
to accumulate there in the density gradient. In con-
42
MIDDLETON and MUSICK: ABUNDANCE AND DISTRIBUTION OF MACROURIDAE
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43
Nezumia a equal is
FISHERY BULLETIN: VOL. 84, NO. 1
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* g
X
oa
a
A A
— I 1 1 1 r—
100 200 300 400 500
— I 1 1 1 1 1 1 1 1 1
600 700 800 900 1000 1 100 1200 1300 1400 1500
DEPTH ( m )
Figure 8— The distribution of log transformed (log (x + 1)) abundance and weight of Nezumia aequalis at each station, plotted against depth.
junction with Marshall's hypothesis, the advantages
of the type of seasonal migration suggested by our
data are twofold. First, the migration concentrates
the reproductively mature fish in a limited area
thereby increasing the probability of a sexual en-
counter. Second, it allows additional time for develop-
ment of eggs on their rise to the upper layers, and
concurrently lessens the chance that the egg will
travel through the thermocline and be removed from
the area by the more aqtive surface currents
(although egg density could be such that neutral
buoyancy occurs at the thermocline). If these sug-
gestions hold true, it would be expected that the lar-
vae would benefit from the high productivity and
warmer temperatures of the surface waters and have
enhanced growth. As productivity declines in the late
44
MIDDLETON and MUSICK: ABUNDANCE AND DISTRIBUTION OF MACROURIDAE
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45
FISHERY BULLETIN: VOL. 84, NO. 1
fall and the larvae become larger, they would drop
out of the water column to the bottom. Length fre-
quencies of N. bairdii (Fig. 11) suggested that
Nezumia bairdii
6,
5 ■
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— i 1 1 1 1 1 1
O 10 20 30 40 50 60 70
HEADLENGTH
Figure 10.— The gonadal maturity stages plotted against head
length for Nezumia bairdii.
recruitment of young occurred between the months
of November and January. No small N. bairdii were
captured benthically between the proposed deep-
water spawning time and the shallower January
recruitment spike.
The larger N. bairdii occurred deeper than the
small ones (Figs. 9, 12) demonstrating the "larger-
deeper" phenomenon.
The age and growth analysis of N. bairdii
presented many problems. Due to the thickness of
the sacculus otolith a thin cross section had to be
removed from each. After examination of the thin
sections, two problems became apparent. First, all
of the smaller specimens had two hyaline zones.
Because the specimens were obtained on the winter
(January; 76-01) cruise, all had hyaline zones around
the perimeter as expected. There was, in addition,
a well-defined hyaline zone in the interior of all the
otoliths obtained from the smallest fishes available
(<27 mm HL). Subsequently two hypotheses were
proposed: 1) a period of hyaline zone formation (slow
growth) occurred between June-July (spawning) and
January, and 2) young N. bairdii were not available
to our trawl until the second winter hyaline zone was
forming (age about 1.5 yr).
The first hypothesis was discarded because a
period of slow growth within the first 6 mo would
have no apparent selective advantage It should be
noted, however, that since the larvae of N. bairdii
were probably pelagic, a change from planktonic
feeding to benthic feeding would have occurred dur-
ing that time. Such an ontogenetic change occurs in
related gadid fishes. Musick (1969) described the
70-1
60
50-
40
30
20-
10-
Nezumia bairdii
J ^
H.L. (mm)
Figure 11— Head length frequency distribution for Nezumia bairdii by cruise The number above
each cruise indicates the number of specimens.
46
MIDDLETON and MUSICK: ABUNDANCE AND DISTRIBUTION OF MACROURIDAE
ontogenetic transition for Urophycis chuss and sug-
gested that the transition from pelagic to demersal
adaptations in morphology and behavior occurred
within a period of 12-24 h. This short time span
would be unlikely to be reflected in macroscopic
hyaline band formation. Therefore, the second hy-
pothesis appeared more likely, and led to the con-
clusion that the juvenile N. bairdii remained pelagic
until the second winter and then descended from the
water column to the bottom where they were
captured.
Nezumia bairdii
The second problem was that in the older fish (>4
yr) the outer bands were very difficult to define with
any degree of confidence The percentage of
unreadable otoliths increased from about 5% in fish
<4 yr to about 50% in fish >4 yr. The mean head
length of N. bairdii with four bands was 42.7 mm,
the size at the onset of sexual maturity. Growth may
have slowed down to compensate for the energy
needed for reproduction, and produced spatially
close and obscure hyaline zones. Therefore spawn-
ing checks may have had considerable influence on
co
3 0n
a. ^
co - 2. OH
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£T
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o-
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oo
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loxo
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a
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= 73-10
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= 74-04
A
• 75-08
X
-- 76-01
4.0-1
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® *2.0H
£ o
1.0-
P*h xxX a
«& o
x \ xS°_ 6
a ^
a a
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*$
oo
0 A a
A
x
— I 1 1 1 l 1 1 1 1 1
200 400 600 800 1000 1200 1400 1600 1800 2000
DEPTH (m)
Figure 12— The distribution of log transformed (log (x + 1)) abundance and weight of Nezumia bairdii at each station plotted against depth.
47
the interpretation of the hyaline zones.
Using the length at age data, a Walford growth
transformation graph was plotted (Beverton and
Holt 1957). Instead of calculating the L^, we used
our largest specimen (66 mm HL ). The estimate of
Brady's coefficient (K) obtained from this graph was
0.276. Using the Walford graph, the head lengths
for those presumed ages >4 yr could be iteratively
generated. This method gave a maximum age of ap-
proximately 11 yr. The von Bertalanffy growth equa-
tion for length was
Lt = 66 (L - e
-0.276 (T+0.
16)).
Rannou (1976) studied the age and growth of a
congener (N. sclerorhyncus) that occupies a similar
depth range in the western Mediterranean. He
calculated a K coefficient of 0.16 and an L^ of 42.31
mm HL. Thus, although this species is smaller than
N. bairdii, it has a much slower growth rate, prob-
ably attributable to lower productivity in the western
Mediterranean compared with the slope off the mid-
Atlantic coast of the United States (Koblentz-Mishke
et al. 1970).
The length-weight regression for N. bairdii (Fig.
2) was analyzed. The solution of the line for N. bair-
dii males was log (weight) = 0.038 (head length)
+ 0.083, r2 = 0.810, and for females it was log
(weight) = 0.035 (head length) + 0.216, r2 = 0.760.
These length-weight relationships are not unlike
those summarized by Gordon (1979) for other small
macrourids (Coelorinchus coelorinchus, C. occa, and
Nezumia aequalis).
In summary, larger N. bairdii were captured
deeper and the minimum and maximum depths of
capture off the mid-Atlantic coast were 270 m and
1,644 m. The fish seasonally migrated to deeper
water with the mature fish occurring deeper than
immature fish. The males matured at about 45 mm
HL and the females became mature at 44 mm HL.
Nezumia bairdii probably spawned pelagic eggs in
July and August and the young apparently remained
pelagic until the second winter (January), when they
first appeared in bottom trawls. The maximum age
of N. bairdii was presumed to be 11 yr. The
temperature range for N. bairdii was from 3.7° to
10.0°C, with the average temperature of capture
being 5.3°C (Fig. 6).
Coryphaenoides rupestris (Gunnerus 1765)
Coryphaenoides rupestris is a large macrourid that
reaches a total length of about 100 cm (Sawatim-
skii 1971; Nodzinski and Zukowski 1971; Marshall
FISHERY BULLETIN: VOL. 84, NO. 1
and Iwamoto 1973), and is found on both sides of
the North Atlantic. In the eastern North Atlantic
it ranges from the Trondhjem area to the Bay of
Biscay. In the western North Atlantic it is reported
to occur from Davis Strait to ca. lat. 37°N (Marshall
and Iwamoto 1973), although two specimens (81 and
100 mm HL) were captured by C. Richard Robins5
at lat. 23°29.8-32.0'N, long. 77°05.5'W. The depth
distribution of C. rupestris varies from about 180
to 2,200 m (Leim and Scott 1966) with highest abun-
dance occurring between 400 and 1,200 m (Marshall
and Iwamoto 1973).
Coryphaenoides rupestris is rarely used as a food
fish in the United States, but the German
Democratic Republic, the Soviet Union, and Poland
fish commercially for it in the western North Atlan-
tic In 1968, the Soviets recorded a harvest of 30,000
tons of C. rupestris off Labrador, Baffin Island, and
Greenland (Nodzinksi and Zukowski 1971). The
catches of this macrourid were reported to increase
during the second half of the year as the catches of
redfish and cod decreased (Sawatimskii 1971).
Coryphaenoides rupestris was captured in the Nor-
folk Canyon area at depths of 578-1,698 m (Fig. 3).
Sawatimskii (1971) reported that C. rupestris is
known to form dense aggregations off the coast of
Labrador. In November 1974 an anomalous catch of
over 6,000 C. rupestris with a total weight >1,000
kg was obtained in a half hour tow in the Norfolk
Canyon area. A random subsample of 1,000 speci-
mens was examined and no sexually mature fish
were found. Although the head length ranged from
59 to 110 mm, the length-frequency curve was
strongly unimodal at 76 mm. The greatest number
and biomass of C. rupestris caught in "normal" half
hour tows was 128 fish comprising 39% of the in-
dividuals and 68 kg, and representing 65% of the
total catch by weight. The largest specimen captured
had a head length of 155 mm.
The head length distribution by depth and by
cruise (Fig. 13) suggested a mass movement of C.
rupestris toward deeper water during the summer
months, and a reciprocating movement to shallower
water in the winter. In January, the majority of C.
rupestris was captured between 700 and 800 m,
while in June and September there appeared to be
a movement toward deeper water. By November the
depths of capture decreased and were similar to
those of January, and the slope of the head length-
depth regression for C. rupestris was significantly
5C. Richard Robins, Rosenstiel School of Marine and Atmospheric
Science, Division of Biology and Living Resources, 4600 Ricken-
backer Causeway, Miami, FL 33149.
48
MIDDLETON and MUSICK: ABUNDANCE AND DISTRIBUTION OF MACROURIDAE
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49
FISHERY BULLETIN: VOL. 84, NO. 1
different from zero. There was no apparent seasonal
size segregation evident as in Nezumia bairdii, but
the graph of numerical abundance against depth also
indicated a general seasonal movement down slope
in September (Fig. 14). Similar seasonal movements
have been shown by Savvatimskii (1971) off
Newfoundland.
Females may be mature from about 104 mm HL
and males from 71 mm HL (Fig. 15).
Podrazhanskaya (1971) supported Zarkharov and
Mokanu's (1970) theory that C. rupestris spawns in
Icelandic waters. She stated that C. rupestris spawn
near Iceland and the Irminger Current could
transport the eggs and larvae to Greenland. From
Greenland the western branch of the West Green-
land Current would transport larvae to Baffin Island
where the Labrador Current would move the fish
down to the Newfoundland banks. When the fish in
the Newfoundland area attain a size of 40-50 cm total
length (TL), they start to migrate back to Iceland.
Podrazhanskaya gave the modal lengths for C.
rupestris in each area. The smallest fish (modal TL
of 45-47 cm) were found on the Northern Newfound-
land bank and the largest (modal TL of 98-100 cm)
were found around Iceland. Fish from between Baf-
fin Island and West Greenland had modal lengths
200
400-
600
800
1 000-1
1200
1400-
1600
1800
2000-
2200-
2400-
2600-
2800-
3000
LOO
0 I I >
JAN.
JUNE
NOV.
SEPT.
Coryphaenoides rupestris
abundance - log(**« I )
FIGURE 14.— Diagram of depth plotted against the log transform-
ed (log (s + 1)) numerical abundance, by cruise, for Coryphaenoides
rupestris.
of 60-62 and 78-80 cm, respectively. Podrazhanskaya's
(1971) modal-length data for each area in conjunc-
tion with Savvatimskii's (1971) age and growth data
reveal that the modal-length fish off the Newfound-
land banks are about 6 yr old, off Baffin Island they
are 9-10 yr, around Greenland they are 15-16 yr, and
at Iceland they are over 20 yr. If a spawning migra-
tion occurs, it does not preclude spawning by some
members of the population not undergoing migra-
tion, thereby accounting for the small percentage of
ripening fish to be found outside of their primary
spawning area.
If Podrazhanskaya's migration theory is valid, some
interesting observations can be made First, the C.
rupestris found on the east coast of the United
States may be derived from the larvae that failed
to metamorphose by the time they reached the New-
foundland banks and continued to drift southwest.
The predominant currents move south and west from
Newfoundland to Cape Hatteras (Worthington 1964;
Webster 1969; Gatien 1976), thereby affording a
means of transport for unmetamorphosed larvae
(Wenner and Musick 1979). Additionally, the modal
length for the 7,011 C. rupestris caught in the Nor-
Coryphaenoides rupestris
3 -
i-
10
a.
EH
4=h
^B-\
I 6
5 -
2 -
-«=E
3H
I I I I
— i 1 1 1 i 1 1 1 i p i
SO 60 70 80 90 100 MO 120 130 140 ISO 160
HEAOLENGTH
FIGURE 15.— The gonadal maturity stages plotted against head
length for Coryphaenoides rupestris.
50
MIDDLETON and MUSICK: ABUNDANCE AND DISTRIBUTION OF MACROURIDAE
folk Canyon area was 46 cm, exactly that which was
found for C. rupestris in the Newfoundland bank
area. However, no small C. rupestris were captured
in the Norfolk Canyon area. We found only 2 fish
with a head length <40 mm (24 cm TL) and only 10
fish with head length <50 mm (30 cm TL).
The regression line for head length against log
(weight) (Fig. 2) was analyzed. The solution for C.
rupestris males was log (weight) = 0.023 (head
length) + 0.82, r2 = 0.898, and for females it was
log (weight) = 0.018 (head length) + 1.16, r2 =
0.885.
Unfortunately these length-weight data cannot be
compared directly with those summarized by Gor-
don (1979) because we measured head lengths in our
study and he gave standard lengths. We do not have
the data at present to compute the regression for
head length on standard length for this species.
Temperatures at which C. rupestris were captured
near Norfolk Canyon ranged from 3.7° to 5.7°C
(Fig. 6). The average temperature was 4.9°C.
Coryphaenoides rupestris does not follow the
"larger-fewer-deeper" pattern shown for N. bair-
dii in Norfolk Canyon because it migrates seasonally
(Fig. 16) and the larger specimens traverse the en-
tire bathymetric range (Fig. 13).
In summary, C. rupestris migrated seasonally to
shallower water in the fall and early winter. Catch
per unit effort increased in the fall and winter, and
a dense aggregation was found in the fall. Podra-
zhanskaya's (1971) spawning and migration theory
appears feasible but further intensive study is need-
ed. No ripe, running, or spent fish were captured
in the Norfolk Canyon area out of 7,011 individuals
examined. There was a trend for the larger C.
rupestris to range deeper but not to the degree that
was found in N. bairdii. It appears that the distribu-
tion of C. rupestris was more closely related to
temperature than to depth, the species being found
mostly within the 4°-5°C range.
Coryphaenoides carapinus (Goode and Bean 1883)
Coryphaenoides carapinus is another small
macrourid which grows to about 390 mm TL, and
is found on the lower slope and abyss from 1,000 to
3,000 m (Haedrich and Polloni 1976). In the western
North Atlantic it has been found between Nova
Scotia and Cape Hatteras (lat 37°N) and in the
eastern Atlantic from lat. 50°N to the Equator. Cory-
phaenoides carapinus has also been reported
from the mid-Atlantic ridge (Marshall and Iwamoto
1973).
In the Norfolk Canyon area C. carapinus was cap-
tured at 1,108-2,767 m (Fig. 3). The largest number
caught in one trawl was 37 (total weight 550 g).
These were captured in September 1975 at a depth
of 1,803 m. Coryphaenoides carapinus comprised up
to 23.4% of a catch in number, but only 4.3% in
biomass. The maximum size captured was 90 mm
HL.
Coryphaenoides carapinus tended to be larger at
the lower end of its depth range (Fig. 17). The slope
of the regression line for head length with depth was
significantly different than zero. The coefficient of
determination was 0.346.
Figure 18 displays low numbers and high vari-
ability in the capture of C. carapinus in relation to
depth. The phenomenon of fewer, larger fish at the
deeper part of the bathymetric range was evident
but obscured because of the relatively small size of
C. carapinus, low numbers, and contagious
distribution.
Coryphaenoides carapinus was taken at temper-
atures of 2.5°-4.2°C with the average temperature
being 3.7°C (Fig. 6). Some overlap in distribution
with depth and temperature occurred among C.
carapinus, C. armatus, and C rupestris. Because
C carapinus is a small species and mostly a ben-
thic feeder (Haedrich and Polloni 1976) and C. ar-
matus and C. rupestris are large species that forage
into the water column (Podrazhanskaya 1971;
Haedrich and Henderson 1974; Smith et al. 1979),
competitive interaction is probably low.
Coryphaenoides armatus (Hector 1875)
Coryphaenoides armatus is cosmopolitan in distri-
bution, being found in all oceans except the Arctic.
It commonly is found from 2,200 to 4,700 m, with
a few specimens being captured as shallow as 282
m (Marshall and Iwamoto 1973). Larger individuals
have been shown to forage off the bottom for pelagic
prey (Haedrich and Henderson 1974; Pearcy 1975;
Smith et al. 1979). Coryphaenoides armatus attains
a size of 165 mm HL and over 870 mm TL (Iwamoto
and Stein 1974). The largest specimen captured in
Norfolk Canyon was 146 mm HL. Although C. ar-
matus is one of the deepest living macrourids, it is
rather well-known biologically because of its broad
distribution and availability to deepwater trawls
(Haedrich and Henderson 1974; Pearcy and Ambler
1974; McLellan 1977; Smith 1978).
Coryphaenoides armatus was taken in every suc-
cessful trawl from 2,100 m to our deepest trawl of
3,083 m in the Norfolk Canyon area and virtually
was confined to below the 3°C isotherm (Fig. 3). In
51
FISHERY BULLETIN: VOL. 84, NO. 1
2
LU
5 3.0-
O
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Coryphaenoides rupestris
o*
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= 73-10
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= 74-04
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= 75-08
X
- 76-01
a a
X
t r
o A
t 1 1 1 1 r
A
a
x a a
~i 1 1 1 -i r
A
o a
T
6.0-1
5.0-
4 0-
x —
(S)
x 3.0-
> o
2 0-
1.0-
x
,a a
° - . x
a d
X
- 1 1 1
1800 2000
— i 1 1 1 1 1 1 1 1 r- — i 1 1 1 1 1 r
200 400 600 800 1000 1200 1400 1600
DEPTH (m.)
Figure 16— The distribution of log transformed (log (x + 1)) abundance and weight of Coryphaenoides rupestris at each station, plotted
against depth.
one trawl C. armatus comprised 92.7% of the bentho-
pelagic fish numbers and 93.4% of the biomass. In
a 1-h trawl the maximum number captured was 76
and the maximum biomass was 21.2 kg.
No increase in fish size with increased depth was
evident in the data (Fig. 19) (Table 1), and the slope
of the regression line for head length with depth was
not significantly different from zero. However, known
depth range of C. armatits was incompletely sam-
pled in this study, and further samples from greater
depth may lead to other conclusions.
The distribution of numerical abundance and
weight with depth are shown in Figure 20. Cor-
yphaenoides armatus increased in abundance from
2,100 to 2,600 m, beyond which its abundance re-
mained constant.
The regression lines for head length against log
(weight) were analyzed (Fig. 2). The solution for
males was log (weight) = 0.017 (head length) +
0.956, r2 = 0.967, and for females it was log
(weight) = 0.016 (head length) + 1.029, r2 = 0.972.
The maturity stages of C. armatus against head
52
MIDDLETON and MUSICK: ABUNDANCE AND DISTRIBUTION OF MACROURIDAE
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Coryphaenoides carapinus
FISHERY BULLETIN: VOL. 84, NO. 1
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DEPTH (m)
Figure 18— The distribution of log transformed (log (x + 1)) abundance and weight of Coryphaenoides carapinus at each station plotted
against depth.
lengths are shown in Figure 21. No mature males
were found, but the females matured at about 78 mm
HL. Coryphaenoides armatus was captured in
temperatures ranging from 2.3° to 3.3°C (Fig. 6).
The majority of individuals, however, were caught
between 2.4° and 2.9°C during the study and the
average temperature was 2.6°C.
Distribution of Macrourids With
Temperature
Depth distribution has been used commonly
throughout the literature to delineate the habitat of
various fishes, including macrourids (Macpherson
1981). The temperature ranges for each species in
54
MIDDLETON and MUSICK: ABUNDANCE AND DISTRIBUTION OF MACROURIDAE
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55
FISHERY BULLETIN: VOL. 84, NO. 1
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Coryphaenoides armatus
3.0-1
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Figure 20— The distribution of log transformed (log (x+1)) abundance and weight of Coryphaenoides armatus at each station plotted
against depth.
the present study showed some overlap, but the
temperatures at which the population modes were
found were fairly discrete except for Nezumia ae-
qualis, Nezumia bairdii, and Coryphaenoides
rupestris.
In Figure 6 the relationship of species with
temperature is more clearly defined. The minimum
temperature of each species remained fairly constant
as did the maximum and modal temperature for
those species in which there was no indication of
seasonal migratory patterns (Coelorinchus car-
minatus, Coryphaenoides carapinus, C. armatus).
The 3.5°C minimum temperature found for C.
carapinus in June was probably not accurate since
the deepest trawl of that cruise did not encompass
the entire range of C. carapinus. Similarly, the
minimal temperatures for C. armatus may not be
representative
Competition Among Macrourids
Competition among macrourids in the Norfolk
Canyon region is probably minimal because the
species differ in body size and feeding strategies or,
if feeding strategies are similar, the species have dif-
ferent distributions with temperature and depth.
Close congeners such as Nezumia bairdii and N.
aequalis might be expected to occupy similar depth
p;r
MIDDLETON and MUSICK: ABUNDANCE AND DISTRIBUTION OF MACROURIDAE
6-1
5
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HE£
EH
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40 SO 60 70 80 90 100 110
HEADLENGTH
Figure 21— The gonadal maturity stages plotted against head
length for Coryphaenoides armatus.
and temperature ranges; however, the N. aequalis
in this area were at the northern limit of their
geographic range, occurred in small numbers, and
may have been in direct competition with TV. bair-
dii. Although C. rupestris also occupied the lower
section of the two Nezumia spp. temperature and
depth regimes, direct competition was probably
low because of their dissimilarity in mouth size and
morphology and related differences in diet
(Podrazhanskaya 1971; Geistdoerfer 1975; McLellan
1977).
Abundance and Density of
the Family Macrouridae
In the study area the abundance of macrourids,
in water shallower than 2,000 m, was fairly constant
with respect to other bottom fishes. The average per-
cent of macrourids by number in each cruise was
16.6% in cruise 73-10 (June), 15.0% in 74-04
(December), 14.6% in 75-08 (September), and 18%
in 76-01 (January). The major peaks of abundance
were found between 300 and 400 m, where Coelorin-
chus c. carminatus was present, and around 800 m
where the complex comprised of Nezumia aequalis,
N. bairdii, and Coryphaenoides rupestris dominated
(Fig. 22). In depths of over 2,000 m the numerical
dominance of C. armatus was evident. Some of the
minor inflections can be attributed to the contagious
distributions displayed by these fishes.
The graph of macrourid biomass (Fig. 23), as per-
cent of the catch, was similar to that for numerical
abundance except for a shift in biomass from 800
m to below 1,000 m between January and June. This
was probably because of the seasonal movement of
the larger macrourid Coryphaenoides rupestris. Be-
tween about 1,400 and 2,200 m, macrourids made
up a very small portion of the biomass, although
their percent by number was comparable with lesser
depths. The dominant macrourid in this area, C.
carapinus, was small, and Antimora rostrata, a
large morid, was the most abundant member of the
benthic fish community from 1,300 to 2,500 m (Wen-
ner and Musick 1977). In depths >2,200 m the
biomass of C. armatus steeply increased with depth,
until it was the predominant member of the benthic
community.
All the macrourid species, with the exception of
C. rupestris, maintained a fairly constant numerical
distribution from cruise to cruise There was ap-
parent variability for C. carapinus and C. armatus,
but this was due to the small number of samples
from deeper areas. Distribution of macrourids as the
percent of catch revealed a gradual replacement of
species with depth, and the predominance of C. ar-
matus in depths >2,500 m.
Macrourids made up a major numerical portion of
the benthic fish community from 300 m to the
deepest station at 3,083 m. Macrourids were also
a main component of the biomass of the commu-
nities from 300 to 3,083 m, excluding the 1,300-
2,500 m range where the morid, A. rostrata,
dominated.
Although Macrouridae is a dominant family in the
Norfolk Canyon area, the potential for a fishery is
essentially nonexistent. Coryphaenoides rupestris is
the only species which attains an appreciable size
in the mid-Atlantic area; a modal length of 46 cm
TL. However, this size is much smaller than typically
found in the North Atlantic and the density of
organisms is generally low (normally <0.86 in-
dividuals/1002). In addition, C. rupestris demon-
strates a tropical submergence, being found deeper
in lower latitudes. The depth range of this species
in the Norfolk Canyon area (578-1,698 m), combined
with smaller size and lower density of organisms, in-
dicate that a commercial fishery would not be
economically feasible
57
FISHERY BULLETIN: VOL. 84, NO. 1
O
O
X
Q-
O
0
2
4
6
8
10
12
14
16
18
20
22
24
26
28
30
0
76-01
2
4 h
6
8
10
I 2
14
16
18
20
22
24
26
28
30
. 75-08
JAN.
73-10
JUNE
SEPT.
. 74-04
NOV.
0 50 00
PERCENT
Figure 22— Depth versus relative abundance (as percent, by number, of total capture) for
the family Macrouridae, by individual cruise
Comparison With Other Studies
The comparison of this study with others in the
North Atlantic lends support to Marshall and
Iwamoto's (1973) hypothesis that the greatest diver-
sity of macrourids is in the bathyal tropical regions.
The number of macrourid species declines from
tropical to boreal regions. Marshall and Iwamoto
(1973) reported 32 macrourid species from the Carib-
bean and Gulf of Mexico, but only 22 species were
captured during our study (Table 2). Bullis and
Struhsaker (1970) found that Macrouridae was one
of the dominant families on the western Caribbean
slope between 201 and 400 fathoms (368-732 m). The
deepest stratum sampled was 451-500 fathoms
(825-914 m), and macrourids (9 species) comprised
about 67% of the individuals captured within these
depths. Within the same depths in the Norfolk Can-
yon area the dominant macrourids (4 species) con-
tributed about 31% to the total catch.
Merrett and Marshall (1981) remarked on the high
diversity (and apparent resource partitioning) of
macrourids from a tropical upwelling area off north-
west Africa and reported 26 species from there They
found 18 species on the slope (< 1,600 m), including
four species of Nezumia. Bathygadine macrourids
were important off Africa but virtually absent in our
study area. Thus macrourid diversity is probably
highest on the continental slope in the tropics, par-
ticularly in areas of higher productivity. In addition,
high diversity is manifested there at several tax-
onomic levels, from the species to the subfamily.
Haedrich et al. (1975) reported the capture of 121
macrourid specimens (3 species) in 29 trawls off
Southern New England. Their trawl depths ranged
from 141 to 1,928 m. Their findings were similar to
58
MIDDLETON and MUSICK: ABUNDANCE AND DISTRIBUTION OF MACROURIDAE
O
O
X
»-
a.
bJ
o
u
2
76-01
JAN.
4
4
6
-
e
10
12
14
16
IS
20
22
24
26
28
2 ■
4 ■
6
8
10
12
14
16
18
20
22
24
26
28
30
73-10
JUNE
75-08
SEPT.
74-04
NOV.
0 50 OO
1 i I
PERCENT
Figure 23— Depth versus relative abundance (as percent, by biomass, of total capture) for
the family Macrouridae, by individual cruise
Table 2. — Species captured during study, with total number and total weight.
Total
Total
Total
weight
Total
weight
Species
number
(g)
Species
number
(g)
Coelorinchus c. carminatus
1,827
38,597
Coryphaenoides colony
1
20
Coelorinchus caribbaeus'1
10
419
Coryphaenoides leptolepis
12
4,922
Coelorinchus occay
1
2
Ventrifossa occidentalis
60
1,449
Nezumia aequalis
285
4,041
Ventrifossa macropogon
1
8
Nezumia bairdii
2,222
72,865
Hymenocephalus gracilis^
1
1
Nezumia longebarbatus2
12
1,299
Hymenocephalus italicus^
1
12
Nezumia sclerorhyncus
1
8
Bathygadus favosus
2
—
Nezumia cyrano*
1
—
Bathygadus macropsy
1
22
Coryphaenoides rupestris
7,120
1,229,304
Sphagemacrurus grenadae2
4
30
Coryphaenoides carapinus
213
4,703
Macrourus bergiax3
2
4,470
Coryphaenoides armatus
391
120,456
Gadomus dispart
1
—
'Range extension from the Gulf of Mexico-Caribbean area.
2Also reported by Haedrich and Polloni (1974).
3Range extension from Boreal Northwest Atlantic.
59
FISHERY BULLETIN: VOL. 84, NO. 1
those in the present study within the 350-1,100 m
depth interval. Respectively, the family Macrouridae
accounted for 21% and 22.4% of the fishes captured
in these depth intervals.
Haedrich and Krefft (1978) studied the fish fauna
in the Denmark Strait and Irminger Sea. In the five
fish assemblages that they reported, macrourids
were abundant in the 2,026-2,058 m assemblage
(22.4%) and very dominant in the 763-1,503 m
(48.3%) and 493-975 m (55.4%) assemblages.
Macrourids were conspicuously absent from their
group three assemblage, although it was well within
macrourid depth and temperature range (280-776 m,
1.4°-7.4°C). An interesting aspect of Haedrich and
Krefft's (1978) study was evident in their group two
assemblage Coryphaenoides rupestris was the
highly dominant fish (48.3%) in this group, and the
temperature range of this group (3.9°-5.6°C) corre-
sponded closely to the temperature range we found
for C. rupestris in the present study (3.7°-5.7°C).
Pearcy et al. (1982) summarized data on deep-sea
benthic fishes collected over several years off Oregon
(Day and Pearcy 1968; Pearcy and Ambler 1974).
Iwamoto and Stein (1974) reported 11 species of
macrourids from the northeast Pacific and Pearcy
et al. (1982) recorded 8 of these off Oregon. A com-
parison of these data with ours shows that the
greatest contrast in the two areas is on the upper
and middle slope (500-1,000 m) where five common
species are regularly encountered in the western
Atlantic (Coelorinchus c. carminatus, Nezumia bair-
dii, C. aequalis, Coryphaenoides rupestris, and Ven-
trifossa occidentalis), but Pearcy et al. (1982) record-
ed no macrourid as common. This faunal difference
may be due to the high density off Oregon of scor-
paeniform and lycodine fishes, many of which may
fill niches on the upper slope occupied by macrourids
elsewhere The macrourid fauna in depths >2,000 m
have many similarities to our study. Coryphaenoides
armatus becomes increasingly dominant below this
depth and often is the only species captured deeper
than 3,000 m in both areas (see also Musick and
Sulak 1979). Among other macrourid species Cory-
phaenoides leptolepis is usually second or third in
abundance at abyssal depths in both regions (Musick
and Sulak 1979).
This distribution pattern is very different from
that reported for the continental rise in the tropics
off west Africa (Merrett and Marshall 1981) where
C. armatus and other large rat tails were very rare
Marshall and Merrett (1981) speculated that the rari-
ty of large predatory scavengers in the upwelling
area they studied might be because of the com-
petitively superior fishes of small size which were
better adapted to use the constant abundant food
supply there This speculation is not supported by
data from the southern Sargasso Sea and Bahamas
(Musick and Sulak unpubl. data), a tropical region
quite low in productivity, in which large rat tails, such
as C armatus, are also very rare The virtual absence
of C. armatus from tropical abyssal areas may be
due instead to some restriction on the life history
of the species. Musick and Sulak (1979) have sug-
gested that this species (along with some other large
species of predator/scavenger such as C. rupestris
and Antimora rostrata) may migrate to boreal areas
to spawn. The tropics may be too far removed from
such spawning areas for individuals to successfully
return.
ACKNOWLEDGMENTS
We wish to thank all colleagues formerly or pres-
ently with the Virginia Institute of Marine Science
for their enthusiastic participation in the deep-sea
program, and particularly to Charles Wenner,
Richard Carpenter, Douglas Markle, George
Sedberry, and Kenneth Sulak. Daniel Cohen of the
Los Angeles County Museum of Natural History
kindly contributed cogent comments on early stages
of this manuscript. Drafts and final copy of this
report were prepared by the Virginia Institute of
Marine Science Report Center.
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Bullis, H. R., Jr., and R T. Struhsaker.
1970. Fish fauna of the Western Caribbean upper slope Q.
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Christensen, J. M.
1964. Burning of otoliths, a technique for age determination
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62
DIFFERENTIATION OF PRIONOTUS CAROLINUS AND
PRIONOTUS EVOLANS EGGS IN HEREFORD INLET ESTUARY,
SOUTHERN NEW JERSEY, USING IMMUNODIFFUSION
Walter J. Keirans,1 Sidney S. Herman,2 and R. G. Malsberger2
ABSTRACT
Immunochemical techniques were used to classify the planktonic eggs of Prionotus carolinus (northern
searobin) and Prionotus evolans (striped searobin) collected from a southern New Jersey estuary. Results
of immunochemical identifications were compared with identifications based upon the commonly used
morphological character of egg oil globule distribution. An average identification error of 22.3% was found
when results using this conventional morphological characteristic were compared with immunodiffusion
results. Improved accuracy of searobin egg identification can be achieved in future ichthyoplankton studies
by using immunochemical techniques. A similar application of immunochemical identification techniques
should also better resolve classification uncertainties among other morphologically similar co-temporal
and co-spatial planktonic fish eggs.
The accuracy of ichthyoplankton analysis is often
limited by the lack of reliable, distinguishing, mor-
phological characteristics that are useful for identi-
fying fish eggs and larvae. Conventional character-
istics used to identify fish eggs include egg and oil
globule diameters; number, distribution, and pigmen-
tation of oil globules; and pigmentation patterns on
developing embryos. However, overlapping diameters
of eggs and a similar if not identical number of oil
globules with comparable pigmentation and size
among closely related species impose a relatively
high degree of uncertainty concerning the identity
of planktonic fish eggs from many areas. Increased
accuracy has been more recently achieved through
the analysis of fish eggs using biochemical, im-
munological, and ontogenetic methods. Morgan
(1975) examined electrophoretic patterns of white
perch and striped bass egg extracts and found dif-
ferentiation was possible on this basis. Orlowski et
al. (1972) differentiated cunner, Tautogolabrus ad-
sperus, from tautog, Tautoga onitis, eggs using
monospecific antisera in microimmunodiffusion
analyses. The technique was especially useful with
early stage eggs which were morphologically iden-
tical. Ontogenetic methods allow careful study of
laboratory-reared eggs and larvae of known paren-
tage to document species-specific developmental
histories. These studies may provide new distin-
1 Department of Biology, Lehigh University, Bethlehem, PA; pres-
ent address: E. I. du Pont de Nemours Co., Inc., Glasgow Research
Laboratory, Wilmington, DE 19898.
department of Biology, Lehigh University, Bethlehem, PA
18015.
guishing morphological features for future egg iden-
tifications. However, additional means are required
where well-documented features shared with other
species do not provide adequate differentiation of
field-collected eggs.
This paper is a report on the results obtained from
a microimmunodiffusion analysis which successful-
ly differentiated the planktonic eggs of the north-
ern searobin, Prionotus carolinus, from those of the
striped searobin, Prionotus evolans, which were col-
lected from the Hereford Inlet estuary, southern
New Jersey, between May 1973 and September 1974
(Keirans 1977). Identifications based separately upon
immunochemical and morphological evidence were
also compared to evaluate the reliability of differen-
tiations based entirely upon conventional mor-
phology. Prionotus spp. were selected in our study
first because the searobins represent a large
breeding population which appears co-temporally
and co-spatially near shore to provide an abundant
source of gravid adults. Eggs of known parentage
became readily available for preparation of ex-
perimental reagents and specimens. Secondly, this
study would expand the application of microimmuno-
diffusion analysis to species differentiation as an ex-
tension of the study of Orlowski et al. (1972), which
documented differentiation of eggs from two genera.
Finally, the identification of Prionotus spp. ova has
never been properly resolved.
Prionotus carolinus ova were described by Kuntz
and Radcliffe (1918) as highly transparent but slight-
ly yellowish spherical eggs ranging from 1.0 to 1.15
mm in diameter. The yolk sphere contained a
Manuscript accepted March 1985.
FISHERY BULLETIN: VOL. 84. NO. 1. 1986.
63
variable number of 10 to 25 unequal-sized oil globules
scattered over the yolk surface which showed some
tendency toward aggregation with progressing
development. The diameter range was extended
from 0.94 mm to 1.20 mm by Bigelow and Schroeder
(1953) and Wheatland (1956), respectively. The up-
per diameter limit extension was verified by Her-
man (1963). Prionotus evolans ova have never been
positively identified. Perlmutter (1939) made a ten-
tative identification, later accepted by Marshall
(1946), from ripe ova stripped from gravid females
collected in Long Island Sound and described as
having similar appearance and diameter as northern
searobin eggs, but with oil globules clustered at one
pole rather than dispersed across the yolk sphere
surface This singular observed morphological dif-
ference of oil globule distribution pattern has beer
used as the primary distinguishing characteristic
between ova of Prionotus carolinus and Prionotus
evolans.
MATERIALS AND METHODS
Conventional Identifications
Field-collected, buffered Formalin3-preserved
plankton samples were physically sorted for all
ichthyoplankton using forceps under a dissecting
microscope, and the criterion of oil globule distribu-
tion differences established by Perlmutter (1939) was
used to tentatively separate P. carolinus from P.
evolans eggs. The annual cycle and species composi-
tion aspects of the field-collected samples using con-
ventional means for egg and larval identifications
have been submitted elsewhere for publication.
3Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
FISHERY BULLETIN: VOL. 84, NO. 1
Immunochemical Identifications
Antigens and Immunizations
Antigen preparations from both species of
searobin eggs were generated using the techniques
developed by Orlowski et al. (1972) with ovarian
tissue from ripe adults and immature individuals.
The four antigen preparations presented in detail in
Table 1 were each used to elicit immune responses
in at least two New Zealand white rabbits to improve
the probability of obtaining useful antisera. Preim-
mune serum samples were obtained from each
animal to establish that no reactivity with antigen
existed prior to immunization.
The soluble protein antigens of Prionotus evolans
(PeSP) and Prionotus carolinus (PcSP) were injected
intravenously in 4.7 and 4.8 mg protein doses (stan-
dard biuret analysis), respectively, to begin the im-
munization program. Maintenance injections of 2 mg
protein followed on a weekly basis. Blood samples
were obtained by cardiac puncture 3 wk following
the first injection and the presence of precipitating
antibody was demonstrated by the standard precip-
itin ring test (Abramoff and LaVia 1970). Additional
monthly cardiac puncture samples were monitored
by quantitative double diffusion (Feinberg 1957) until
after about 12 wk; a titer of 32 was reached in all
animals receiving soluble antigens when sera were
tested with 40 ^g homologous antigen.
Particulate protein antigens from macerated
ovarian tissue of northern (PcPP) and striped (PePP)
searobins were prepared in a 1:1 emulsion with
Freund's complete adjuvant (Cappell Laboratories).
PcPP (8 mg) and PePP (10 mg) protein preparations
were injected subcutaneously along several bilateral
dorsal sites on New Zealand white rabbits. Rabbits
injected with Freund's complete adjuvant developed
Table 1. — Antigen characterization and nomenclature.
Antigen
source and
Range protein
concentration
Method
of
Immunization route and dose
Titer
Double-
Complement
Species
designation
(mg/mL)
determination
Initiation
Maintenance
diffusion
fixation
Prionotus carolinus
Mature ova
8-15
Biuret
Intravenous
Intravenous
32
Northern searobin
(PcSP)
(4.7 mg)
(2mg)
Immature
15-40
Microkjeldahl
Subcutaneous
Intravenous
1,280
follicular
(8mg)
(2mg)
material
(PcPP)
Prionotus evolans
Mature ova
8-15
Biuret
Intravenous
Intravenous
32
Striped searobin
(PeSP)
(4.8 mg)
(2mg)
Immature
15-40
Microkjeldahl
Subcutaneous
Intravenous
1,280
follicular
(10 mg)
(2mg)
material
(PePP)
64
KEIRANS ET AL.: DIFFERENTIATION OF PRIONOTUS EGGS
Arthus reactions following a single dose Subsequent
injections were accomplished intravenously using
Millipore (0.45 /mi) filtrates of PcPP and PePP. Titers
were monitored utilizing the standard complement
fixation assay because of the particulate consisten-
cy of the macerated antigen preparation (Kabat and
Mayer 1961). Maximum titers of 1,280 were obtain-
ed after about 10 wk with immunizations using PcPP
or PePP.
Antiserum Specificity
Antisera elicited in response to both soluble and
particulate antigens were multicompetent and ex-
hibited cross-reactions with heterologous antigens.
The presence of common antigens between the
northern searobin and striped searobin ovarian
material preparations required the specific adsorp-
tion of antisera with these shared antigens to render
a given antiserum monospecific (Eisen 1974).
Although antisera elicited in response to particulate
protein antigens exhibited precipitation reactions in
agar with both soluble antigens and extracts of par-
ticulate antigens from the two species under con-
sideration, they were not competent in reactions with
homologous fish eggs. Therefore, since the selected
method for analysis of planktonic eggs was immuno-
diffusion, only antisera elicited in response to solu-
ble antigens were used in all analyses of unknowns.
Specific adsorption of common antigens shared by
northern and striped searobins was accomplished by
adding PcSP to antisera elicited in response to PeSP
and vice versa. Adsorption lots of 1.5 mL anti-PeSP
antisera combined with 70 \xL PcSP (0.65 mg pro-
tein) were incubated at 4°C for 48 h prior to use.
This adsorption eliminated all reactivity of anti-PeSP
antisera with both PcSP and known ova of P.
carolinus, without significantly reducing activity
with ova of P. evolans. This specifically adsorbed anti-
PeSP, which reacted solely with known homologous
ova of P. evolans under controlled conditions, was
used as the basis for differentiation of northern and
striped searobin eggs. Species-specific anti-PeSP
antisera capable of 100% accuracy in differentiating
known ova of both searobins was the reagent selected
for use in all immunodiffusion analyses.
Microimmunodiffusion Analysis
Unknown planktonic fish eggs were analyzed with
monospecific anti-PeSP antiserum in a micromodi-
fication of the immunodiffusion technique (Ridgeway
et al. 1962). Microscope slides (2.5 x 8 cm) were
washed, rinsed first in distilled water and then
methanol, and wiped dry. Two milliliters of 1% No-
ble Agar (Difco) in FA-Bacto buffer (Difco), pH 7.2,
were applied across each slide on a leveling table and
allowed to harden. Slides were then placed over a
template and wells cut using a Brewer needle with
beveled inner surface (Ridgeway et al. 1962).
Agar plugs were removed from wells by aspiration.
Reagents were applied with either 1 mL syringes
(Burron) or sterile capillary pipettes, and 0.005 to
0.01 mL was required to fill each well. A typical
testing array appears in Figure 1, where corner wells
contain unadsorbed antiserum, the central well con-
tains adsorbed or monospecific antiserum, and re-
maining wells contain individual fish eggs which have
been broken using jeweler's forceps. FA-Bacto buf-
fer was applied to each well following egg disrup-
tion, and slides were allowed to incubate in moist
chambers for 18 h at 20°C. Slides were then washed
for 24 h in FA-Bacto buffer, and stained according
to the method of Crowle (1958). Results were always
recorded at a fixed time interval following slide
preparation to insure comparability from one deter-
mination to another.
RESULTS AND DISCUSSION
A total of 732 searobin ova were recovered from
plankton samples collected in the 1973-74 period.
The combined morphological characteristics of egg
diameter, number, color, and distribution of oil
globules, and embryo pigmentation when present,
allowed the separation of searobin eggs from those
of other species with reasonably high confidence
Preliminary classifications of Prionotus ova into
either evolans or carolinus species was based upon
differential oil globule distribution patterns reported
by Perlmutter (1939). Striped searobin, P. evolans,
eggs were placed into one grouping based upon a
polar or clustered oil globule distribution, and north-
ern searobin, P. carolinus, eggs placed into a second
group having oil globules generally dispersed across
the yolk sphere
Each tentatively classified egg was then analyzed
in the microimmunodiffusion method illustrated in
Figure 1, to establish the immunochemical reactivity
of soluble egg antigens with adsorbed and unadsorb-
ed anti-PeSP antisera. When soluble P. evolans egg
antigens were sufficiently concentrated, a classical
line of identity was observed with fusion of precipitin
bands between adsorbed and unadsorbed anti-PeSP
wells. Identification of P. carolinus eggs was based
upon reactivity with unadsorbed anti-PeSP anti-
serum and no reactivity with adsorbed anti-PeSP.
Previously established reactivity of unadsorbed anti-
65
FISHERY BULLETIN: VOL. 84, NO. 1
Figure 1— Testing array (lOx). C: Prionotus carolinus ovum (1.00 mm); E: Prionotus evolans ovum (1.00
mm); AA: Anti-PeSP antiserum (adsorbed: 0.20 mL antiserum: 0.11 mg PcSP protein); AN: Anti-PeSP antiserum
(unadsorbed). Specific adsorption of cross-reactive antibodies has occurred with PcSP rendering anti-PeSP antiserum
(AA) incompetent to react with antigens of Prionotus carolinus ova (C), indicated by the lack of precipitin bands
about the central well adjacent to (C) egg wells. Corner wells contain multicompetent, unadsorbed anti-PeSP antisera.
PeSP with known P. carolinus eggs was considered
sufficiently definitive for its use in differentiating
P. carolinus from P. evolans ova.
The immunochemical classifications derived from
this analysis indicated that an average 22.3% mis-
classification error had been made when eggs were
differentiated solely on the basis of oil globule
distributions. An approximately equal number of
both northern and striped searobin eggs had been
mistakenly identified, based upon oil globule
distribution patterns. The final classification based
upon immunochemical data was 406 ova of P.
carolinus and 32G ova of P. evolans.
It was confirmed that egg diameters could not
serve as a reliable characteristic for species classi-
fications by retrospectively analyzing diameters of
immunochemically classified eggs according to the
period of field collection. The data presented in Table
2 illustrate that no statistical difference exists in the
diameter ranges of P. carolinus and P. evolans eggs
for the collection period of this study. However, the
trend of declining egg diameters over the spawning
season previously documented by other workers is
Table 2.— Immunochemical classification of
Prionotus spp. eggs collected in plankton
samples.
Average
diameter
Range
Date
(mm)
(mm)
n
Prionotus carolinus
1973
May
1.16
1 .02-1 .24
4
June
1.06
1.00-1.21
10
July
1.08
1.05-1.10
3
August
1.02
0.92-1.18
312
September
0.99
0.90-1.05
32
1974
July
0.98
0.95-1.02
13
August
0.96
0.92-1.02
3
September
0.99
0.92-1.02
29
Prionotus evolans
1973
May
1.12
1.00-1.25
10
June
1.06
1.00-1.12
35
July
1.08
1.00-1.15
2
August
1.03
0.95-1.12
225
September
0.98
0.90-1.08
26
1974
July
0.97
0.95-1.00
6
August
1.02
1.02
1
September
0.99
0.92-1.02
21
66
KEIRANS ET AL.: DIFFERENTIATION OF PRIONOTUS EGGS
confirmed. The data also show that in 1973 and 1974,
the ratios of eggs collected in plankton samples and
identified based upon morphology and immuno-
chemical reactions for nothern and striped searobins
were 1.1:1 and 1.6:1, respectively. These ratios are
similar in magnitude to the ratio of northern and
striped searobin adults observed by Marshall (1946).
Finally, the data indicate that egg diameter and oil
globule distribution cannot serve to reliably dis-
tinguish northern from striped searobin eggs. An
immunochemical distinction can be made that sug-
gests morphology alone is inadequate to provide a
positive identification of P. evolans eggs.
The course of future research in immunochemical
taxonomy of fish eggs should emphasize an increase
in sensitivity, as well as automation of the analysis.
At present, the utility of the immunodiffusion
method is limited by its labor-intensive nature. Ini-
tial stages of the analysis require manual sorting of
ova from plankton samples that is tedious, time-
consuming, and subject to error. Bowen et al. (1972)
initiated studies in which a moderate degree of suc-
cess was achieved in sorting fish ova from pelagic
plankton samples on sucrose density gradients.
However, estuarine plankton samples that contained
a wide range of particulate materials characterized
by different sizes, densities, and shapes, and that also
included high levels of detrital materials, disturbed
the gradients sufficiently to destroy separation
potential. Despite the recognized limitations, there
is currently no practical alternative to manual sort-
ing of plankton samples.
Immunodiffusion analysis requires that individual
fish eggs be subjected to several manual manipula-
tions, with the final determination in solid media re-
quiring the careful applications of reagents. Screen-
ing large numbers of planktonic ova with several dif-
ferent antisera becomes impractical on a large scale.
A more rapid and potentially more specific approach
to immunochemical ichthyoplankton identifications
might employ monoclonal antibodies coupled to
fluorescent indicator molecules. The antibody prod-
ucts of fused mouse lymphocytes and myeloma cells
may be screened and selected for exquisite specificity
to single antigenic determinants or epitopes using
egg antigens of known origin, preferably those
associated with the chorion surface, to procure a
reagent that would specifically label ova without re-
quiring that each egg be mechanically ruptured.
Identifications might be based upon the differential
fluorescence characteristic of a particular fluo-
rescent label associated with a selected antibody and
labelled eggs might be isolated using a fluorescence-
activated cell sorter.
The utility of immunochemical identifications with
demonstrably superior accuracy to conventional
methods has been established with both intergeneric
and interspecific differentiations. Several systems
remain which might benefit from immunochemical
differentiations, such as the complete elucidation of
several sciaenid and clupeid species which occur in
complex estuarine systems, such as the Chesapeake
Bay and Potomac River estuary. Relationships be-
tween scombrids, bothids, and pleuronectids with
more southerly distributions would serve to delineate
adult ratios, population distributions, and spawning
seasons. Finally, the capability of the immune system
to differentiate among epitopes with relatively small
structural difference (Karush 1962) might eventually
be applied to the detection of racial differences or
subpopulation distinctions among fish ova of the
same species.
ACKNOWLEDGMENTS
The Noyes Foundation provided fellowship funds
for the senior author. Michael Criss and Marian
Glaspey assisted in collecting the samples.
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1974. Immunology: An introduction to molecular and cellular
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1957. Identification, discrimination, and quantification in
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Karush, F.
1962. Immunologic specificity and molecular structure Adv.
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1977. An immunochemically assisted ichthyoplankton survey
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68
EFFECTS OF EXPOSURE AND CONFINEMENT ON
SPINY LOBSTERS, PANULIRUS ARGUS, USED AS ATTRACTANTS
IN THE FLORIDA TRAP FISHERY
John H. Hunt,1 William G. Lyons,2 and Frank S. Kennedy, Jr.2
ABSTRACT
Traps in the south Florida spiny lobster fishery are baited with live sublegal-sized lobsters (shorts), many
of which are exposed for considerable periods aboard vessels before being placed in traps and returned
to the sea. Average mortality rate of lobsters exposed Vz, 1, 2, and 4 hours in controlled field tests was
26.3% after 4 weeks of confinement. About 42% of observed mortality occurred within 1 week after ex-
posure, indicating exposure to be a primary cause of death. Neither air temperature during exposure
nor periodic dampening with seawater had significant effects on mortality rate Mortality among confin-
ed lobsters increased markedly in the Atlantic oceanside but not in Florida Bay during the fourth week
of confinement following exposure, probably because more natural food organisms entering traps from
nearby seagrass beds delayed starvation at the latter site. Mortality caused by baiting traps with shorts
may produce economic losses in dockside landings estimated to range from $1.5 to $9.0 million annually.
The fishery for spiny lobster, Panulirus argus, in
south Florida utilizes a method of baiting traps that
is apparently unique among fisheries worldwide
Sublegal [<76 mm carapace length (CL)] lobsters,
locally called "shorts", are confined in traps as living
attractants for legal-sized lobsters. Shorts have been
demonstrated to be effective attractants of other
lobsters (Yang and Obert 1978; Lyons and Kennedy
1981; Kennedy 1982). Some use of shorts as bait
in the Florida fishery occurred as early as the 1950's
(Cope 1959), but use increased appreciably after
1965 when the minimum legal size was reduced from
1 lb (about 79-80 mm CL) to 3 in (76 mm) CL,
and the fishery expanded from Atlantic oceanside
reefs and flats into Florida Bay where availability
of shorts is considerably greater (Lyons et al. 1981).
The practice was widespread but illegal during
early years of its use (Wolff erts 1974) and only
received legal sanction in 1977. Today, bonded
fishermen are allowed to possess as many as 200
shorts aboard a vessel for use as bait. Shorts are
customarily kept in wooden boxes on deck until
replaced in traps, and exposure times vary from
several minutes to 1 h or more As many as 1 million
shorts may be confined in traps as bait during peak
portions of the harvest season (Lyons and Kennedy
1981).
'Florida Department of Natural Resources, Bureau of Marine
Research, Marathon, FL 33050.
2Florida Department of Natural Resources, Bureau of Marine
Research, St. Petersburg, FL 33701.
During 1979, the Florida Department of Natural
Resources initiated a study in which baiting prac-
tices in the fishery were mimicked under controlled
conditions to determine whether starvation occurred
among lobsters confined in traps for long periods.
So much mortality occurred among tested lobsters
during the first 2 wk of confinement that the study
was redirected toward causes of that mortality. Ex-
posure was strongly implicated by preliminary
results (Lyons and Kennedy 1981). Spokesmen for
the fishing industry suggested that observed mor-
tality was caused by other factors related to ex-
perimental design, prompting expansion of the pro-
gram to test those factors.
This report presents results and conclusions from
that expanded program. The relationship between
exposure and mortality is examined, including in-
fluences of season and location. Mortality rates of
lobsters held dry or periodically dampened prior to
placement in traps are also compared. Results from
this study are used in a model which estimates the
relative importance of baiting mortality to economics
of the fishery.
METHODS
Mortality rates of spiny lobsters used to bait traps
were measured in Florida Bay 3 km north of Vaca
Key and in the Atlantic Ocean 6 km south of Vaca
Key. The Florida Bay site was located in shallow
water (~3 m) with a muddy sand substrate overlain
by seagrass beds. The ocean site was located in
Manuscript accepted March 1985.
FISHERY BULLETIN: VOL. 84, NO. 1. 1986.
69
FISHERY BULLETIN: VOL. 84, NO. 1
deeper water (~8 m) just inside the reef tract; the
bottom consisted of a mosaic of scattered seagrasses,
small patch reefs, and open areas of coarse sand.
Salinities at both sites ranged from 34%o to 36%o
and water temperature ranged seasonally from 17°
to 29°C.
The effect of exposure was examined at both sites.
Lobsters were held in shaded boxes for lk, 1, 2, and
4 h and then placed in traps. Entrances were sealed,
and no lobsters were added after treatments were
established. Each treatment utilized 5 standard
wooden slat lobster traps; each trap contained 3
lobsters (total 15 lobsters/ treatment) for each ex-
posure period. Control treatments (minimum ex-
posure) also consisted of 5 traps each containing 3
lobsters, but these lobsters remained in traps in
which they were originally captured and were ex-
posed only for the time required to clean, seal, and
return a trap to the water. Intent was to place
sublegal lobsters in all traps, but use of some larger
lobsters was necessary to conduct experiments.
Traps in oceanside experiments were reinforced with
wire mesh sides to reduce damage by loggerhead
turtles, Caretta caretta; traps in Florida Bay were
not reinforced with wire sides.
In Florida Bay, all lobsters exposed >1 h were
dampened every xk h by pouring a bucket of seawater
into the porous holding box, whereas equal numbers
of lobsters exposed >1 h in oceanside tests were
always treated with and without seawater dampen-
ing every V2 h to test the effect of dampening. Con-
trol and V2-h treatments were the same in dampened
(wet) and undampened (dry) tests because their total
exposure periods were less than or equal to the
period between dampenings.
After initiation, all experiments were sampled at
1-wk intervals for 4 wk by pulling each trap and
counting remaining live lobsters. The mortality
estimate is a combination of missing lobsters and
those observed to be dead. Several lines of evidence
indicate that missing lobsters died and did not
escape Only lobsters too large to fit between trap
slats were used in experiments, and trap entrances
were boarded shut to seal the ordinary avenue of
departure Additionally, observations made during
frequent dives at traps where lobsters died during
other experiments indicated that carcasses could be
broken up sufficiently by scavengers within 24 h
after death to wash through slats when traps were
pulled.
All original data, taken as number of living
lobsters remaining in a trap each week, were con-
verted to weekly mortality rates calculated as the
number of lobsters that died during that week divid-
ed by the initial density during that week. This
method provided the only independent, non-
cumulative estimate of mortality. All other methods
biased the data by either increasing the weight given
to deaths later in the experiment or altering mor-
tality estimates because of trap losses. Although this
method provided unbiased estimates of mortality,
data still were not normally distributed, so all testing
of treatment means used nonparametric Wilcoxon
Two Sample Tests (Sokal and Rohlf 1969) to deter-
mine where the differences of significance occurred.
Standard notations are used to designate signi-
Table 1.— Average weekly spiny lobster mortality (%) for each location, exposure period, and
wet or dry treatment. N = number of traps; x = mean; SE = standard error; W = wet; D
= dry.
Initial
N
Week after initial
exposure
Week 1
Week 2
Week 3
Week 4
Cumulative
mortality
%
Treatment
N
X
SE
N
X
SE
N
X
SE
N
X
SE
Florida
Bay
Control
15
15
0.0
0.0
15
0.0
0.0
15
2.2
2.2
15
0.0
0.0
2.2
V2 h
20
20
8.3
5.3
19
3.5
3.5
18
0.0
0.0
17
0.0
0.0
11.8
1 h
W
20
17
7.8
3.5
17
3.9
3.9
16
6.2
3.4
16
6.2
6.2
24.1
2 h
W
20
18
14.8
5.5
18
1.8
1.8
18
1.8
1.8
18
3.7
2.5
22.1
4 h
W
20
20
15.0
5.6
19
5.3
2.9
19
5.3
2.9
18
0.0
0.0
25.6
Atlantic Reef
Control
29
28
4.8
2.8
23
1.4
1.4
23
0.0
0.0
27
7.4
3.2
13.6
1/2 h
29
29
8.0
3.6
24
1.4
1.4
23
4.3
4.3
27
12.3
4.8
26.0
1 h
W
29
29
16.1
4.8
24
9.7
3.7
19
7.0
4.1
24
12.5
5.2
45.3
D
29
29
11.5
3.8
24
9.7
5.1
22
4.5
2.5
27
11.1
5.3
36.8
2 h
W
29
29
13.8
5.1
17
3.9
2.7
15
4.4
3.0
20
5.0
2.7
27.1
D
29
29
16.1
5.4
23
5.8
2.7
22
4.5
2.5
24
5.6
3.3
32.0
4 h
W
29
29
12.6
3.8
23
4.3
3.2
19
8.8
6.2
22
6.1
2.8
31.8
D
29
29
11.5
4.1
21
7.9
4.5
18
1.8
1.8
23
1.4
1.4
22.6
70
HUNT ET AL.: EXPOSURE AND CONFINEMENT ON SPINY LOBSTERS
ficance at probability levels of 0.05, 0.01, and 0.001.
Weighted cumulative average mortality values
were obtained by multiplying the relative effort (%)
in each treatment (eg, site, exposure period >Vz h)
by the cumulative mortality for that treatment and
then summing those values.
RESULTS
The mortality experiment was conducted four
times between January and September 1980 in
Florida Bay and six times between May 1981 and
June 1982 near Atlantic reefs. Wet vs. dry tests were
conducted with each oceanside replicate The un-
weighted average cumulative mortality calculated
from Table 1 for all lobsters exposed lk, 1, 2, and
4 h, both sites combined, was 26.3% at the end of
4 wk. Average weighted cumulative mortality in
Florida Bay was 20.8%, and that near Atlantic reefs
was 31.9%. When weighted for relative effort at each
site, the overall mortality rate increased to 28.5%.
No tests were established at oceanside stations
during December, January, or February, so effects
of air and water temperatures on mortality during
exposure were tested only in Florida Bay. Of four
tests conducted there, two were established during
cool months (January, February; air 15.2°-21.0°C,
water 17.0°-17.5°C during initiation), and two were
established during warm months (May September;
air 27.6°-33.5°C, water 29.3°-29.5°C). Mean week-
ly mortality rates of lobsters during these tests
(winter x = 4.4%; summer x = 4.6%) were not sig-
nificantly different.
Average mortality rates obtained in wet vs. dry
treatments (Table 1, Fig. 1) were not significantly
different for any exposure or subsequent confine-
ment period. Furthermore, neither wet nor dry treat-
ments consistently caused greater mortality.
Because all Florida Bay lobsters were dampened
when exposed >1 h, comparisons of bay vs. ocean
mortality rates were made using wet treatments
only. All five treatments (Control, V2, 1, 2, and 4 h)
were combined and overall mean weekly mortality
rates were compared. The average weekly mortality
rate of lobsters in bay tests (x = 4.5%) differed
significantly (Z = 2.51, P < 0.05) from that of lobsters
tested in the ocean (x = 7.6%).
45
« 35
o
0 25
J2
E
o
15 -
Figure 1.— Cumulative mortality rates (%) for exposure tests: A.
Florida Bay, wet only; B. Atlantic reefs, wet only; C. Wet (W) vs.
dry (D), Atlantic reefs only. C = controls; exposure periods = Vz,
1, 2, and 4 h.
71
FISHERY BULLETIN: VOL. 84, NO. 1
Comparisons of each exposure period within a
treatment with every other exposure period within
that treatment are shown in Table 2. In the bay, mor-
tality rates experienced by controls were significant-
ly different than those of lobsters exposed 1, 2, or
4 h. Additionally, lobsters exposed V2 h suffered a
significantly lower mortality rate than did those ex-
posed 4 h. However, some of these differences were
not significant among lobsters exposed at the Atlan-
tic reef site Among dampened lobsters tested there,
only the mortality rate of those exposed 1 h differed
significantly from that of controls and from that of
lobsters exposed V2 h. Among undampened lobsters
tested at the ocean site, mean mortality rates of con-
trols differed significantly only from those exposed
1 or 2 h. Differences between controls and 1 h ex-
posures were significant in every treatment, but
mean mortality rates never differed significantly
among lobsters exposed 1, 2, or 4 h.
The mean mortality rate of all tested lobsters dur-
ing the first week following exposure was 11.2%,
which represents about 42% of all mortality; 54%
of all mortality in Florida Bay and 38% of all which
took place near Atlantic reefs occurred during the
first week (Table 1, Fig. 1). High mean weekly mor-
tality rates which occurred during week 1 decreas-
ed to much lower levels during week 2 (4.7%) and
week 3 (3.9%) in both bay and ocean (Fig. 2). Com-
parisons of mean mortality rates incurred during
week 1 with those of weeks 2 and 3 revealed signifi-
cant differences in every instance (Table 3). During
week 4, the overall rate increased to 6.1% (Fig. 2),
but this combined value masked highly divergent
changes in rates of mortality at bay and ocean sites.
Table 2.— Results of Wilcoxon Two Sample Tests (Z values)
from comparisons of mean weekly mortality rates from dif-
ferent exposure periods for various treatments at Florida
Bay (Bay) and Atlantic Reef (Ocean) locations. C = con-
trols; exposure = hours.
Tests
Exposure
C
Vz
1
2 4
Bay wet
C
—
1/2
1.14
—
1
2.48*
1.62
—
2
2.52*
1.68
0.02
—
4
2.93**
2.17*
0.51
0.49 —
Ocean wet
c
—
Vz
1.10
—
1
3.07**
2.02*
—
2
1.87
0.81
1.17
—
4
1.93
0.85
1.16
0.03 —
Ocean dry
C
—
Va
1.10
—
1
2.20*
1.12
—
2
2.12*
1.03
0.10
—
4
1.17
0.08
1.01
0.92 —
Bayside mortality rates actually decreased slightly,
whereas oceanside rates increased dramatically.
Statistical comparisons between mean mortality
rates during weeks 1 and 4 demonstrate significant
differences in the bay but not in the ocean (Table 3).
Graphic depictions of cumulative weekly mortality
rates (Fig. 1) reveal a decrease in slope after week
1 at both bay and ocean sites. These decreases in-
dicate reduced rates of mortality which persist
through the end of the experiment in the bay and
through week 3 in the ocean. However, the slope in-
creases sharply during week 4 in most oceanside
tests, indicating an additional period of high mor-
tality there.
DISCUSSION
Exposure unquestionably causes mortality among
Panulirus argus used to bait traps. Increasing ex-
Week
B
A
D
T
1
1
pg|:p:;::jjj:j::::::::::::::|
B
A
D
T
2
I!!!!!!!!!!!!!!l
B
A
D
T
3
|"E: ::J[r-
B
A
D
T
4
::-:E=:::::::::::::::i:i:::3
, , ....
4 8 12
Percent Mortality
• = P < 0.05;
P*S 0.01;
P< 0.001
Figure 2— Average weekly mortality rates (%) per treatment type
during weeks 1-4, all exposures combined. A = oceanside (Atlan-
tic Ocean) wet; B = bay (Florida Bay) wet; D = oceanside dry; T
= all treatments combined.
72
HUNT ET AL.: EXPOSURE AND CONFINEMENT ON SPINY LOBSTERS
posure periods up to 1 h resulted in corresponding
increases in mortality. Similar mortality has been
observed in the Western Australia spiny lobster
(Panulirus cygnus) fishery (Brown and Caputi 1983;
Brown et al. in press). In that fishery, undersize
lobsters are not used as bait but are often retained
aboard vessels for varying periods during the sort-
ing process. Tb test effects of that practice, Austral-
ian lobsters were tagged, held aboard vessels for 0,
Vi, V2, 1, and 2 h, and then released. Recapture rates
were markedly lower in exposed groups than in con-
trols. As in our experiments, results from exposure
times >1 h were similar to those of 1 h exposures.
The greatest rate of mortality to Panulirus argus
in our tests occurred during the first week follow-
ing exposure (Fig. 2). Although physiological causes
of mortality have not been determined, several fac-
tors may be involved. Dehydration due to desicca-
tion may affect survival, but lobsters dampened at
V2 h intervals died at rates similar to those left un-
attended. One effect of exposure is to dry gills
(Anonymous 1980), which may result in respiratory
problems. Dehydration and gill damage may cause
mortality directly, but more likely are contributory
factors to physiological stress caused by buildup of
toxic compounds in the blood. Handling stress has
been demonstrated to cause temporary acidic con-
ditions in the blood of European lobsters, Homarus
vulgaris (McMahon et al. 1978). After reimmersion
in seawater, lobsters should rehydrate fairly quick-
ly, but effects of physiological stress are likely to
linger.
Contrary to prior expectations, mortality rates of
dampened lobsters did not differ significantly from
those left unattended (dry). Dampening also failed
to enhance survival of the northern lobster, Homarus
americanus (McLeese 1965). McLeese suggested
Table 3.— Results of Wilcoxon Two Sample Tests (Z
values) from comparisons of mean weekly (1-4) mor-
tality rates for various treatments at Florida Bay
(Bay) and Atlantic Reef (Ocean) locations.
Tests
Week
1
2
3 4
Bay wet
1
2
3
4
2.86**
2.40*
3.58***
0.55
0.94
1.48 —
Ocean wet
1
2
3
4
2.72**
3.04**
0.66
0.59
2.08*
2.50* —
Ocean dry
1
2
3
4
2.40*
3.33***
1.31
1.02
1.14
2.13* —
P *S 0.05; * * = P « 0.01 ; * * * = P < 0.001 .
that a relationship existed between metabolic rate
and mortality. An increase in metabolic rate and con-
current more rapid depletion of reserves may have
offset advantages of increasing moisture by dampen-
ing during our experiments as well.
Exposure was probably the principal cause of mor-
tality among bait lobsters during our tests in Florida
Bay. However, a small but distinctly greater level of
mortality among all lobsters, including controls dur-
ing weeks 1-3 and a marked increase in mortality
during week 4 at the ocean site, suggest that other
factors in addition to exposure were responsible for
mortalities there (Figs. 1, 2). When average mortality
rates of controls (Table 1) are subtracted from overall
average mortality rates of exposed lobsters, resul-
tant values (18.6%, Florida Bay; 18.3%, Atlantic
reefs) are nearly equal and probably represent the
rates of mortality actually ascribable to exposure at
each site Thus, effects of exposure were similar
regardless of where traps were placed.
Mortality due to other effects related to confine-
ment evidently do vary depending upon locations
where traps are placed, especially if confinement
periods are lengthy. Increased mortality rates such
as those we observed during week 4 at the Atlantic
reef site may result from starvation. Lyons and Ken-
nedy (1981) presented evidence of weight loss and
starvation among lobsters confined at densities of
3 and 5/trap in Florida Bay for 8 wk. Rate of weight
loss increased during week 4 among lobsters at den-
sities of 5 but did not increase rapidly until week 6
among lobsters confined at densities of 3. Those tests
were conducted in the same portion of Florida Bay
where present exposure tests were conducted, an
area characterized by muddy sand overlain by sea-
grass beds. A disparity in available food organisms
between this area and that where oceanside tests
were conducted may explain differences in mortal-
ity during week 4.
Seagrass beds in Florida Bay are lush and heavi-
ly covered with epibionts (J. H. Hunt, pers. obs.).
These epibionts serve as food for larger organisms
which in turn are appropriate food for Panulirus
argus. Snails in the genera such as Modulus, Turbo,
Astraea, and Cerithium and crabs in the genera
Mithrax and Pitho are abundant in these grass beds
and are frequently seen within or clinging to sides
of lobster traps. All of these also occur commonly
in stomach contents of P. argus in south Florida (W
G. Lyons, pers. obs.). At the ocean site, grass beds
are sparse and patchily distributed, and fewer
organisms enter traps from the surrounding sand.
It seems reasonable to suppose that the weight loss
observed to occur among lobsters confined near lush
73
FISHERY BULLETIN: VOL. 84, NO. 1
grass beds (Lyons and Kennedy 1981) might occur
at accelerated rates in the relatively more sparse
ocean environment. If food is sufficiently scarce, ac-
celerated weight loss may lead to starvation and in-
creased mortality within the observed 4-wk period.
Traps in these experiments had their entrances
boarded over to prevent escape, whereas lobsters
that escape from traps used in the fishery are likely
to recover from effects of starvation. Escape rates,
though, are quite low, ranging from 0.8 to 1.8%/d
(Yang and Obert 1978; Davis and Dodrill 1980; Lyons
and Kennedy 1981).
We offer no explanation for our observation that
highest mortality rates are associated with 1-h ex-
posures nor for the persistent background mortality
among oceanside controls. Nevertheless, neither
seem to be artifacts of experimental design and, in-
stead, probably represent other yet-to-be understood
physiological reactions to stress caused by exposure,
handling, or confinement. If so, they represent other
effects of baiting with shorts and are justly included
among estimates of total fishery-induced mortality.
Economic Effects of Mortality
Baiting traps with shorts results in significant
economic loss to the fishery. Although use of shorts
is an effective means of attracting other lobsters
without requiring out-of-pocket expenses for bait,
each bait lobster that dies is one that potentially will
not enter fishery landings. In addition, repair of
broken legs, antennae, and other injuries caused by
handling may retard growth by as much as 40%
(Davis 1981), increasing the time required for a
lobster to attain legal size and extending the time
during which it may be used as bait. An injured
lobster that escapes from a trap where it was placed
will direct energy toward repair, not growth, thereby
reducing the probability that it will attain legal size
during its next molt. If the lobster does not attain
legal size, it is again vulnerable to capture and to
use as bait. Confinement itself also results in reduced
lobster growth rate (Kennedy 1982), which doubt-
lessly extends the period during which a lobster may
be vulnerable to use as bait.
The hidden costs of baiting with shorts needs to
be considered in future management efforts. The
following model, based only upon observed mortali-
ty rates, estimates that cost:
Y = AxBxCxD
where Y = seasonal mortality of shorts used as bait;
A = number of traps in the fishery;
B = average number of shorts per trap;
C = season length (in months);
D = average monthly mortality rate.
Because the actual allocation of fishery traps
among Florida Bay and Atlantic sites is unknown
but believed to be relatively equal, we selected the
unweighted average cumulative 4-wk mortality rate
to estimate monthly mortality throughout the
fishery. By using a range of values for other
variables, several estimates of the average number
of shorts that die seasonally because of fishery bait-
ing practices may be obtained (Table 4). Thus, if each
trap in the fishery is baited with only 1 short/mo and
all fishermen leave the fishery after only 4 mo, more
than 600,000 sublegal lobsters may die as a result
of their use as bait. If all traps are deployed for the
full 8 mo and each trap uses 3 shorts as bait, more
than 3.6 million shorts may die as a result of that
use Both examples probably represent extreme
cases, and actual fishery-induced mortality probably
lies somewhere between these estimates.
The problem is really more complex. Some lobsters
that die because they were used as bait would prob-
ably fall victim to other causes, but natural mortal-
ity among lobsters of sizes appropriate for use as
bait (65-75 mm CL) may be low, particularly since
incidence of their principal predators, large ser-
ranids, has been greatly reduced in the fishery area.
Furthermore, not all traps are baited with shorts
because shorts are not readily available in some
peripheral areas of the fishery. Both of these factors
suggest that the model may overestimate fishery-
induced mortality. However, values used in the model
for numbers of shorts per trap are probably low.
Fishermen prefer to use 3-5 shorts/trap (Gulf of Mex-
Table 4. — Estimates of the economic effect of baiting with
shorts in the south Florida spiny lobster fishery.
Average
Seasonal
monthly
No. of
No. of
mortality
mortality
traps in
Season
shorts/
of shorts
rate1
fishery2
length3
trap4
as bait
0.263
573,000
4
1
602,796
0.263
573,000
4
3
1 ,808,338
0.263
573,000
6
1
904,194
0.263
573,000
6
3
2,712,582
0.263
573,000
8
1
1,205,592
0.263
573,000
8
3
3,616,776
'Unweighted average cumulative 4-wk mortality rate from this study.
2Number of traps in 1981 (E. J. Little, Jr., Southwest Fisheries Center
Resource Statistics Office, National Marine Fisheries Service, NOAA,
P.O. Box 269, Key West, FL 33041, pers. commun. November 1982).
3The season is 26 July-31 March, 8+ mo; some fishermen begin
removing their traps after November, and many have left the fishery
by the end of January, causing a considerable reduction in the number
of traps fished during February and March.
^Conservative estimates; fishermen try to put as many shorts as
available into traps.
74
HUNT ET AL.: EXPOSURE AND CONFINEMENT ON SPINY LOBSTERS
ico and South Atlantic Fishery Management Coun-
cils 1982), and it seems probable from fishermen's
comments that virtually no shorts are intentionally
released. Similarly, the model only allows one input
of bait per month, whereas in reality additional
shorts are continually introduced, typically at 1-2 wk
intervals, to replace others lost because of death or
escape. These factors suggest that the model may
underestimate fishery-induced mortality.
Regardless of which values are applied, the model
indicates that resultant losses to the fishery are con-
siderable Since a lobster weighs slightly <1 lb at
legal size, fishery-induced mortality may cause losses
ranging from 0.6 to 3.6 million lb. At recent ex-vessel
prices of $2.50 per pound, this represents a poten-
tial loss to the fishery of $1.5-$9.0 million annually.
In 1981, total reported commercial lobster har-
vest was 5.9 million lb valued at $14.5 million3, so
the hidden cost of baiting with shorts is consider-
able
This loss may be viewed as a necessary cost, albeit
large, of doing business in the fishery or as a prob-
lem that may be alleviated by alternative manage-
ment strategies. If the latter course is deemed
necessary, use of other baits and installation of
escape gaps that allow shorts to escape while retain-
ing legal lobsters in traps (Bowen 1963) are poten-
tially effective strategies to increase harvest of
legal lobsters without adversely affecting the popu-
lation.
ACKNOWLEDGMENTS
This project was partially funded by a research
grant (2-34 1-R) from PL 88-309 (Commercial
Fisheries Research and Development Act) through
the Fisheries Management Division, National
Marine Fisheries Service, NOAA, U.S. Department
of Commerce, and was administered by the Florida
Department of Natural Resources (FDNR) Bureau
of Marine Research.
R. S. Brown, Western Australia Department of
Fisheries and Wildlife, provided unpublished manu-
scripts of related recent studies of Panulirus qjgnus.
Field assistance was provided by D. G. Barber, S. F.
Barber, G. F. Bieber, S. E. Coleman, J. W Lowry
R. H. McMichael, Jr., G. K. Vermeer, and M. A.
Winter, all presently or formerly FDNR employees.
G. K. Vermeer, M. A. Winter, and R. G. Muller
Statistical Surveys Branch. 1983. Florida landings 1981.
Southeast Fisheries Center National Statistical Office, National
Marine Fisheries Service, NOAA, 75 Virginia Beach Drive, Miami,
FL 33149.
(FDNR) provided valuable discussion and other
assistance during manuscript preparation. All are
gratefully thanked.
LITERATURE CITED
Anonymous.
1980. The fate of undersized rock lobsters returned to the sea.
West. Aust. Dep. Fish. Wildl, Fish. Ind. News Serv. (F.I.N.S.)
13:10-12.
Bowen, B. K.
1963. Management of the western rock lobster, (Panulirus
longipes cygnus George). Proa Indo-Paa Fish. Counc. 14:
139-154.
Brown, R. S., and N. Caputi.
1983. Factors affecting the recapture of undersize western
rock lobster Panulirus qjgnus George returned by fishermen
to the sea. Fish. Res. 2:103-128.
Brown, R. S., J. Prince, N. Caputi, and J. Jerke.
In press. Fishery induced mortality of undersize western rock
lobster. West. Aust. Dep. Fish. Wildl. Bull.
Cope, C. E.
1959. Spiny lobster gear and fishing methods. U.S. Fish
Wildl. Serv., Fish. Leafl. 487, 17 p.
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 fishery
management. Proa Gulf Caribb. Fish. Inst. 32:194-207.
Gulf of Mexico and South Atlantic Fishery Management
Councils.
1982. Fishery management plan, environmental impact state-
ment and regulatory impact review for spiny lobster in the
Gulf of Mexico and South Atlantic. Gulf of Mexico and
South Atlantic Fishery Management Councils, Tampa, Fla.,
var. p.
Kennedy, F. S., Jr.
1982. Catch rates of lobster traps baited with shorts, with
notes on effects of confinement. In W. G. Lyons (editor),
Proceedings of a workshop on Florida spiny lobster research
and management, p. 20. Fla. Dep. Nat. Resour. Mar. Res.
Lab., St. Petersburg.
Lyons, W. G, D. G. Barber, S. M. Foster, F. S. Kennedy, Jr.,
and G. R. Milano.
1981. The spiny lobster, Panulirus argus, in the middle and
upper Florida Keys: population structure, seasonal dynamics,
and reproduction. Fla. Mar. Res. Publ. 38, 38 p.
Lyons, W. G, and F. S. Kennedy, Jr.
1981. Effects of harvest techniques on sublegal spiny lobsters
and on subsequent fishery yield. Proa Gulf Caribb. Fish.
Inst. 33:290-300.
McLeese, D. W.
1965. Survival of lobsters, Homarus americanus, out of water.
J. Fish. Res. Board Can. 22:385-394.
McMahon, B. R., P. J. Butler, and E. W. Taylor.
1978. Acid base changes during recovery from disturbance
and during long term hypoxic exposure in the lobster,
Homarus vulgaris. J. Exp. Zool. 205:361-370.
SOKAL, R. R., AND F. J. ROHLF.
1969. Biometry: the principles and practice of statistics in
biological research. W. H. Freeman and Co., San Franc., 776
P-
75
FISHERY BULLETIN: VOL. 84, NO. 1
WOLFFERTS, R. C. YANG, M. C. K., AND B. OBERT.
1974. Fishermen's problems in the spiny lobster fishery, hi 1978. Selected statistical analyses of Key West spiny lobster
W. Seaman, Jr., and D. Y. Aska (editors), Conference pro- data. In R. E. Warner (editor), Spiny lobster research
ceedings: Research and information needs of the Florida review; proceedings of a conference held December 16, 1976
spiny lobster fishery, p. 3 [abstr.], 8, 9. Fla. Sea Grant Rep. in Key West, Florida, p. 4-7. Fla. Sea Grant Tech. Pap. No. 4.
SUSF-SG-74-201, Gainesville, FL.
76
TYPE, QUANTITY, AND SIZE OF FOOD OF
PACIFIC SALMON (ONCORHYNCHUS) IN
THE STRAIT OF JUAN DE FUCA, BRITISH COLUMBIA
Terry D. Beacham1
ABSTRACT
The volume, numbers, and size of prey of sockeye, Oncorhynchus nerka; pink, 0. gorbuscha; coho, 0. kisutch;
and chinook, 0. tshawytscha, salmon were investigated for troll-caught salmon in the Strait of Juan de
Fuca off southwestern Vancouver Island during 1967-68. Sockeye salmon was the least piscivorous species
with only 7% of the stomach volume comprised of fish, while chinook salmon was the most piscivorous
species at 56%. Sand lance, Ammodytes hexapterus, and euphausiids were the most important fish and
invertebrate prey, respectively. As predator size increased, mean size of fish prey increased, and predators
shifted to species of larger mean size Similar results were found for the invertebrate prey, with mean
number of prey consumed per predator increasing for the larger invertebrate species as predator size
increased. Rate of increase in mean length of fish prey was proportional to increasing predator length.
The observed increase in invertebrate size with increasing predator length was not statistically signifi-
cant. Although chinook and coho salmon had similar diets, they were caught at significantly different
water depths. Oncorhynchus species with fewer, shorter, and more widely spaced gillrakers have higher
proportions of fish in their diet than species with numerous, long, and narrow set gillrakers.
The life history of Pacific salmon is quite variable
among species, with fry of pink salmon, Oncorhyn-
chus gorbuscha, and chum salmon, 0. keta, migrating
to sea soon after emergence from the gravel, while
those of sockeye salmon, 0. nerka, coho salmon, 0.
kisutch, and chinook salmon, 0. tshawytscha, may
spend up to 2 yr in freshwater. Once in the ocean
they can migrate a considerable distance from their
natal streams and feed on a variety of organisms
(Godfrey et al. 1975; French et al. 1976; Major et al.
1978; Takagi et al. 1981). Salmon thus move through
a number of habitats during their life cycle and con-
sume a diverse array of prey.
Food preferences of salmon in the range of
habitats that they occupy have been an area of con-
tinuing investigation (Allen and Aron 1958; Prakash
1962; LeBrasseur 1966; Parker 1971; Eggers 1982).
Relative amounts of different prey types eaten in
varying environments have been examined, as well
as preferences by different sizes of predators in rela-
tion to the size and abundance of prey. Oncorhyn-
chus species differ considerably in their size, mor-
phology, and ocean distribution (Hikita 1962; Neave
et al. 1976; Takagi et al. 1981; Beacham and Mur-
ray 1983). Morphological differences and diet parti-
tioning have been reported for many fish species
(Keast and Webb 1966; Hyatt 1979), and diet parti-
tioning may thus be expected among Oncorhynchus
species. Prey size is related to predator size (O'Brien
1979; Gibson 1980), and differential prey selection
among Oncorhynchus species may also be apparent.
Stomach contents of sockeye, pink, coho, and
chinook salmon were investigated in a research troll-
ing program conducted off southern Vancouver
Island in the Strait of Juan de Fuca during 1967-68.
The relative importance of different prey types, in-
cluding fish and invertebrates, in the diet of the four
species was studied with respect to prey size, preda-
tor size, predator morphology, and diet partitioning
in relation to salmonid habitat and morphology.
MATERIALS AND METHODS
The salmon were obtained by test trolling in the
Strait of Juan de Fuca during 19 June-11 October
1967 and 1 May-12 July 1968 (Fig. 1). Detailed
methodology of the program has been outlined by
Graham and Argue (1972). For each salmon sampled,
date, fork length (mm), round weight, and sex were
recorded. Stomachs were removed, placed in num-
bered cloth sample bags along with any food
organisms in the mouth cavity, and preserved in 10%
Formalin2 solution.
'Department of Fisheries and Oceans, Fisheries Research
Branch, Pacific Biological Station, Nanaimo, British Columbia V9R
5K6, Canada.
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Manuscript accepted March 1985.
FISHERY BULLETIN: VOL. 84, No. 1, 1986.
77
FISHERY BULLETIN: VOL. 84, NO. 1
I24°00'
Figure 1.— Location of study area in Strait of Juan de Fuca off southwestern Vancouver Island.
Laboratory analysis involved sorting the contents
into the classifications outlined in Table 1 by using
a low-power binocular microscope. Numbers of
organisms in each classification were recorded, if
possible, for each individual salmon. Once individuals
were counted, displacement volumes (mL) were
determined separately for fish contents, for crusta-
cean contents, and for miscellaneous organisms. If
organisms were too digested to assign to individual
classifications but could be identified as fish or
crustaceans, their volumes were included in either
the unidentified fish volume or unidentified crusta-
cean volume classification.
Two techniques of data analysis were used.
Table 1.— Percentage of salmon sampled with empty stomachs and average number of prey per fish with non-empty
stomachs.
N
%
empty
Prey type
Class
CO
o
c
ffl
"O
c
CO
CO
en
c
CO
X
"ST
.C CO
ij -q
o CO
rr<2-
CO
H—
I—
CO
o
CO
;g
(0
Q.
UJ
2
CO
E
CO
CO
CO
£
CO
O
CO
;g
CO
>.
2
*
CO
■o
o
Q.
jc
Q.
E
<
<0
5
6
CO
O CO
C CO
18
CO CO
2 o
Sockeye <55 cm
22
46
—
—
—
3.7
13.2
5.0
0.3
—
—
0.1
Sockeye >55 cm
117
41
0.2
—
—
—
13.5
8.6
0.4
0.1
—
—
0.4
Total
139
42
0.2
—
—
—
12.1
9.3
1.1
0.1
—
—
0.4
Pink <55 cm
301
26
0.7
—
—
—
9.7
13.7
1.0
0.3
—
0.1
0.3
Pink >55 cm
498
32
0.4
—
—
0.1
15.3
13.1
2.4
0.1
0.1
0.1
0.4
Total
799
30
0.5
—
—
0.1
13.1
13.3
1.9
0.2
0.1
0.1
0.4
Coho <40 cm
1,045
49
0.4
—
—
0.2
6.3
1.2
0.4
1.3
0.1
0.2
0.3
Coho 40-60 cm
1,039
28
5.8
—
0.1
0.3
29.8
0.3
0.9
0.3
—
0.2
0.4
Coho >60 cm
130
32
0.5
0.2
—
—
51.0
0.4
0.6
—
—
—
0.6
Total
2,214
38
3.3
—
—
0.2
22.1
0.7
0.7
0.6
—
0.2
0.4
Chinook <40 cm
607
39
1.1
—
—
0.1
5.4
0.1
0.7
0.4
—
—
0.7
Chinook 40-60 cm
786
36
1.6
0.1
—
0.1
15.3
0.2
0.2
0.6
—
—
0.1
Chinook >60 cm
83
47
0.8
0.3
—
—
62.4
—
0.4
0.1
—
—
—
Total
1,476
38
1.4
0.1
—
0.1
13.6
0.1
0.4
0.5
—
—
0.3
'Other than Parathemisto.
78
BEACHAM: FOOD OF PACIFIC SALMON OFF BRITISH COLUMBIA
Methodology for the first, percent occurrence of each
of the prey types, has been outlined by Hynes (1950).
All chi-square tests in the analysis for frequency of
occurrence of prey types have one degree of freedom.
The second technique involved determining percent-
age by volume of total stomach contents for fish,
crustaceans, miscellaneous organisms, and also for
the individual prey classifications. Fish, crustaceans,
and miscellaneous organisms were recorded by
volume, and thus determining percentage of total
stomach volume for each classification was direct.
For individual prey types, it was necessary to con-
vert numbers of individual organisms to volumes by
calculating the volume displaced by a single
organism of each prey type This was done by selec-
ting individual salmon of each species with only one
fish and/or one crustacean prey type in the stomach.
The unit volumes for each prey type were then
calculated as the sum of the fish or crustacean
volumes for the selected fish divided by the number
of the prey type under consideration. If there was
only one unknown in the stomach contents with prey
of known (calculated) volumes (the number of prey
types multiplied by their unit volumes), the total
volume of known prey was subtracted from the total
fish or crustacean volume until only one unknown
prey class remained. Then the volume of the prey
class in question was obtained and its unit volume
calculated. Comparisons of prey size among the
species were analyzed by analysis of variance
For an individual salmon with more than one fish
or one crustacean prey class in its stomach, volume
of each prey class was determined by multiplying the
number of organisms by their unit volume This total
volume obtained was scaled proportionately so that
individual components when summed equalled the
total known fish or crustacean volume
RESULTS
Volume and Frequency of
Food Items
For each species, over 30% of the individuals had
empty stomachs (Table 1). In comparing fish with
non-empty stomachs, sockeye salmon was the least
piscivorous, with a mean 7% fish component in the
diet (Fig. 2). In sockeye salmon <55 cm fork length
(FL), only 2% of the stomach volume was comprised
of fish. At 17% of total food volume, fish was a
greater dietary component of pink salmon than of
sockeye (Fig. 2). However, the fish component of the
diet of sockeye and pink salmon was considerably
less than that of coho (46%) and chinook (56%)
salmon. Fish comprised 30% of the stomach content
volume of coho <40 cm FL, but almost 50% of the
stomach content volume of larger coho. Chinook
salmon was the most piscivorous of the four species,
and the 56% fish component of the diet was constant
for the three size classes of chinook salmon inves-
tigated, although the species composition of the fish
prey changed.
The relative importance of individual prey types
was investigated for the four salmon species. Sand
lance, Ammodytes hexapterus, was virtually the sole
fish component of the diet of sockeye salmon, oc-
curring in 4% of the 81 non-empty sockeye salmon
stomachs sampled (Fig. 3). Euphausiids were the
most important prey for sockeye, occurring in 58%
of non-empty stomachs and comprising 71% of the
total volume of food eaten. The hyperiid amphipod
Parathemisto comprised over 11% of the volume of
food eaten. Of the fish prey species, sand lance was
again the most important for pink salmon, occurring
in 9% of 562 non-empty stomachs and comprising
10% of total stomach contents (Fig. 4). There was
no significant difference between sockeye and pink
salmon in the frequency of occurrence of sand lance
in their diets (x2 = 2.65, P > 0.05). Fish species
other than sand lance (herring, Clupea harengus, and
rockfish, Sebastes sp.) comprised less than 1% of
stomach contents of pink salmon. As in sockeye
salmon, the dominant invertebrate prey types were
euphausiids at 62% of stomach content volume and
Parathemisto at 14%. Frequency of occurrence of
euphausiids (x2 = 1.63, P > 0.05) and Parathemisto
(x2 = 3.54, P > 0.05) were similar for sockeye and
pink salmon.
Fish species were a significant food for coho and
chinook salmon. For example, sand lance occurred
in 27% of 1,364 non-empty stomachs of coho salmon,
and also comprised 27% of total stomach volume
(Fig. 5). Herring comprised <1% of the stomach con-
tent volume of coho <40 cm FL, but 25% of the
volume for coho >60 cm FL. The dominant inverte-
brate prey type was euphausiids, comprising 51% of
total stomach contents, while all invertebrate prey
types combined comprised only 54%. The relative
importance of fish as a prey type was greatest in
chinook salmon, with sand lance again the dominant
prey species, occurring in 34% of 914 non-empty
stomachs, and comprising 35% of total volume of
contents (Fig. 6). Sand lance occurred in the diet of
chinook and coho salmon at similar frequencies (x2
= 0.80, P > 0.05), as did herring (x2 = 0.08, P >
0.05). Herring comprised 9% of the stomach contents
for chinook salmon <40 cm FL, but 33% of the
stomach contents for chinook salmon >60 cm FL.
79
FISHERY BULLETIN: VOL. 84, NO. 1
UJ
O
>
X
o
<
o
h-
^
100-
80-
60-
40
20 -I
0
100
80
60
40-
20-
0
100
80
60
40
20J
0
100
80H
60
40^
20
<55cm
>55cm
Total
SOCKEYE
<55cm
<55cm
PINK
<40cm
40-60cm
>60cm
COHO
<40cm 40-60cm
>60cm
CHINOOK
O !2
in in
II
<=> o
— a>
o O
in
c
o
o
o
O 2
I!
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= o>
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<->o
in
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si
c c
o o
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01
</)
01
o
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3
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25 2?
— C7>
a> z.
Figure 2— Percentage volumes of stomach contents of the fish, crustacean, and
miscellaneous organism component for sockeye, pink, coho, and chinook salmon sampled
in Strait of Juan de Fuca during 1967-68.
Coho ate greater numbers of fish than did chinook
salmon (Table 1), but chinook had a greater volume
of the stomach contents composed of fish (56%
chinook, 46% coho). This result suggests chinook eat
larger fish than coho (Table 2). As with coho,
euphausiids were the dominant invertebrate prey
type of chinook salmon, comprising 40% of a total
invertebrate volume of 44% of stomach contents.
However, euphausiids occurred significantly more
often in the diet of coho salmon than in chinook
salmon (x2 = 4.73, P < 0.01).
Fish were a more significant dietary component
of chinook and coho salmon than of sockeye and pink
salmon. Sand lance occurred significantly more often
in the diet of chinook and coho salmon than in the
diet of sockeye and pink salmon (x2 = 152.9, P <
0.01). Similar results were also found for herring (x2
= 18.1, P < 0.01), rockfish (x2 = 7.2, P < 0.01), and
mixed fish species (x2 = 39.0, P < 0.01). Inverte-
brate prey were more significant in the diet of
sockeye and pink salmon than in that of chinook and
coho. Euphausiids occurred more frequently in the
diet of sockeye and pink salmon (x2 = 199.3, P <
0.01), as did Parathemisto (x2.= 619.5, P < 0.01),
crab larvae (x2 = 171.1, P < 0.01), and amphipods
(x2 = 9.2, P < 0.01). There was no difference in
frequency of occurrence of crabs in the diet (x2 =
0.01, P > 0.05) which occurred only at low levels
or not at all, but mysiids occurred more frequently
in the diet of chinook and coho salmon than in
80
BEACHAM: FOOD OF PACIFIC SALMON OFF BRITISH COLUMBIA
UJ
CL
CT
Z>
O
O
o
o
z
UJ
O
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rr
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>5
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80
60
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20
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100^
80
60
40
20
0
100
80-
60-
40
20
0
S0CKEYE
1 1 1 1 1
<55 cm
III — 1 1 1
-
>55 cm
1 1
100-
80
60-
40-
20
0
<55cm
>55 cm
o
c
D
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o
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3
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Figure 3.— Percentage frequency of occurrence and percentage stomach volume
of prey types listed in Table 1 for sockeye salmon.
that of sockeye and pink salmon (x2 = 36.0, P <
0.01).
Predator and Prey Size
The effect of predator size on the abundance and
size of prey was examined for each of the four salmon
species investigated. Numbers of individuals con-
sumed for each prey type were tallied for each
salmon examined. For the fish prey species, only
sand lance was consumed at a high enough frequency
to enable one to investigate numbers of sand lance
consumed versus predator size For the four salmon
species, there was no consistent trend for sand lance
in this regard (Table 1). For both chinook and coho
salmon— the two primary sand lance predators— the
number of sand lance eaten was greater in the mid-
dle size group than in either the small or large size
classes. Large chinook and coho salmon switched
from sand lance to larger fish species, such as her-
ring (Figs. 5, 6). There were, however, clear trends
for some of the invertebrate prey types. The average
number of euphausiids eaten per individual predator
increased with increasing fish size (Table 1). How-
ever, the average number of Parathemisto eaten
decreased with increasing predator size The other
prey types occurred at a low frequency (Figs. 3-6),
and thus it was not possible to determine reliable
trends.
As predator size increased, more euphausiids, but
81
FISHERY BULLETIN: VOL. 84 NO. 1
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Figure 4— Percentage frequency of occurrence and percentage stomach volume
of prey types for pink salmon.
less Parathemisto, were eaten per individual
predator. The difference in predator response to
euphausids and Parathemisto may be examined in
relation to the size of the prey. The unit volumes of
an individual euphausiid were about four times
larger than those of an individual Parathemisto
(Table 2). In each salmon species examined, as the
predators increased in size, they switched from the
smaller Parathemisto to the larger euphausiids and
also crab larvae, consuming greater numbers of the
larger prey and decreasing numbers of the smaller
prey. Chinook and coho salmon also consumed
significantly larger Parathemisto than did sockeye
and pink salmon (F = 4.9; df = 3,98; P < 0.01). For
the invertebrate prey, an increase in predator size
resulted in greater numbers of larger prey being
consumed.
As predator size increased, there was an increase
in the size of the prey consumed (Table 2). Larger
predators consumed larger sand lance and herring.
Chinook and coho salmon consumed larger sand
lance (F = 3.7; df = 3,613; P < 0.05) and mixed fish
species (F = 2.9; df = 2,128; P < 0.05) than did sock-
eye and pink salmon. In coho and chinook salmon,
there was also a tendency for larger salmon to switch
prey types from the smaller sand lance to the larger
herring and rockfish. Increasing predator size pro-
duced shifts in both the type, number, and size of
the prey consumed.
Changes in size of prey and predators were in-
82
BEACHAM: FOOD OF PACIFIC SALMON OFF BRITISH COLUMBIA
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Figure 5.— Percentage frequency of occurrence and percentage stomach volume
of prey types for coho salmon.
vestigated for the two most frequently occurring fish
prey (sand lance, herring) and crustacean prey
(euphausiids, Parathemisto). Size classes for sock-
eye and pink salmon were below and above 55 cm
FL, and those for chinook and coho salmon below
and above 60 cm FL. I assume that the value of the
cube root of the volume ratio of the prey is propor-
tional to the prey length ratio, and thus changes in
prey size can be compared with changes in predator
size
Mean size of the fish component of the prey in-
creased as predator size increased (Table 3). As the
size of pink, coho, and chinook salmon increased by
13%, 65%, and 69%, respectively, the size of the sand
lance consumed increased by 16%, 83%, and 83%,
respectively. The size of herring eaten also increased
as predator size increased, and for pink and chinook
salmon it was about equal to the increase in size of
the predator species. When the predator responses
to increase in size of both prey species are pooled,
there is a weak correlation between increasing
predator length and increasing prey length (r = 0.69,
n = 6, P > 0.05); but if the coho salmon response
to increasing herring size is deleted, the relationship
is much stronger between increasing predator and
prey size (r = 0.98, n = 5, P < 0.01).
Apparent trends of invertebrate prey size with
predator size were not statistically significant. For
sockeye and pink salmon, mean size of individuals
in the two invertebrate prey classes decreased as
83
FISHERY BULLETIN: VOL. 84, NO. 1
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Figure 6.— Percentage frequency of occurrence and percentage stomach volume
of prey types for chinook salmon.
predator size increased, but not significantly (Table
3) (r = -0.24, n = 4, P > 0.05). For chinook and coho
salmon, mean size of the invertebrate prey increased
as predator size increased (r = 0.42, n = 4, P > 0.05).
However, the increase in prey size was considerably
less than the increase in predator size (Table 3).
The results of the previous analyses are sum-
marized as follows. As predator size increased, in-
dividual predators selected larger fish prey of one
species, but not a greater number of the prey. There
was also a shifting from smaller prey species (sand
lance) to larger ones (herring, rockfish). As predator
size increased, there was a tendency to shift from
smaller invertebrate prey (Parathemisto) to larger
types (euphausiids, crab larvae). Greater numbers
of the larger prey were consumed by an individual
predator, while numbers of smaller prey consumed
declined. Although larger invertebrate prey types
were preferred as predator size increased, larger in-
dividuals of each prey class were not necessarily
selected by larger predators.
Species Comparisons
The dietary components of the four species of
salmon investigated are different, and there is more
than one possible reason for the apparent partition-
ing of diet among the salmon species. Perhaps
because the salmon occupied different depth zones,
the differences in diet are attributable simply to dif-
84
BEACHAM: FOOD OF PACIFIC SALMON OFF BRITISH COLUMBIA
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85
Table 3. — Mean lengths (cm) of salmon and mean size ot prey.
Mean lengths of sockeye and pink salmon were for those in the
size classes below (L,) and above (L2) 55 cm, whereas those for
coho and chinook salmon were those below (L,) and above (L2)
60 cm. The prey ratio v7 V2/ V, is assumed to be indicative of ratios
in prey lengths between the two groups of predators. The two most
frequent fish and invertebrate prey species listed are euphausiids
(EU), Parathemisto (PA), sand lance (SL), and herring (HR).
Predator
Prey
Mean
length
L2
Prey
Mean volume
v2 ?/vT
Species
L,
1-2
Li
types
v.
v2
v, Vv,
Sockeye
50.7
58.7
1.16
EU
1.24
0.81
0.65 0.87
PA
0.18
0.13
0.72 0.90
Pink
51.8
58.5
1.13
SL
3.01
4.75
1.58 1.16
HR
90.00
120.00
1.33 1.10
EU
1.17
0.98
0.84 0.94
PA
0.27
0.17
0.62 0.86
Coho
40.0
65.8
1.65
SL
4.39
26.98
6.15 1.83
HR
159.73
207.50
1.30 1.09
EU
1.31
1.44
1.10 1.03
PA
.45
.60
1.33 1.10
Chinook
41.2
69.5
1.69
SL
8.42
51.4
6.10 1.83
HR
52.70
245.45
4.66 1.67
EU
1.20
1.40
1.17 1.05
PA
0.34
0.55
1.61 1.17
ferences in prey abundances by depth. The numbers
of salmon caught with non-empty stomachs were
tabulated by depth zone of capture (Table 4). Coho
salmon were most abundant in water depths of <18
m, whereas sockeye and pink salmon were most
abundant between depths of 18 and 36 m, and
chinook salmon most abundant in depths >18 m.
Coho and chinook salmon have similar diets, but are
found at significantly different depths (x2 = 714.7,
P < 0.01). Thus partitioning of the diets among
salmon species is not related simply to water depth.
Morphological characters of the salmon species
were compared with their food preferences. Chinook
and coho salmon have fewer, shorter, and more wide-
ly spaced gillrakers than those of sockeye and pink
salmon (Table 5). As gillrakers are used to strain food
organisms from water passing over the gills (Lagler
et al. 1962), I expected salmon species feeding on
planktivorous prey to have more gillrakers that are
longer and more closely set than those in primarily
piscivorous salmon species. Similar arguments could
be made for tooth size (Table 5). Partitioning of the
diet among the species of salmon investigated is
clearly a reflection of morphological differences
among the species.
DISCUSSION
The calculation of unit volumes for individual prey
classes is an important component of the analysis.
Prey types were assumed to be in a similar state of
FISHERY BULLETIN: VOL. 84, NO. 1
digestion for the different size classes of each species
of salmon so that calculated unit volumes would be
comparable Violation of this assumption may ac-
count for the inverse predator-prey size relationship
found for sockeye and pink salmon with euphausiids
and Parathemisto. The analysis of relative sizes of
the species eaten assumes that different prey types
were not more or less digested than others. This is
unlikely to be strictly true, but it was assumed that
differential digestability of the prey species did not
significantly alter their relative sizes.
Previous work on diet description of Oncorhynchus
species has indicated that there can be considerable
variability in dietary components of a particular
species. However, some general conclusions can be
drawn. Sockeye salmon are the least piscivorous of '
the northeast Pacific Oncorhynchus species (Allen
and Aron 1958; LeBrasseur 1966; Foerster 1968).
Euphausiids have been reported consistently as a
major contributor to the diet of pink salmon (Maeda
1954; Ito 1964; Takagi et al. 1981). The fish compo-
nent reported has been variable, ranging from <1%
to over 90% of stomach volume (Takagi et al. 1981).
Chinook and coho salmon tend to be the most
piscivorous (Allen and Aron 1958; Prakash 1962;
Reimers 1964; LeBrasseur 1966; Machidori 1972).
For chinook salmon, fish were reported to provide
Table 4. — Number of salmon caught with non-empty stomachs and
depth of water (m) in Strait of Juan de Fuca, British Columbia.
Salmon were caught by troll gear. Numbers in parentheses are per-
cent of each species caught in each depth zone.
Depth (m)
Sockeye
Pink
Coho
Chinook
<9.1
8 (9.9)
41 (7.3)
385 (28.1)
20 (2.2)
9.1-18.3
10 (12.3)
95 (16.9)
360 (26.3)
60 (6.6)
18.3-27.4
26 (32.1)
159 (28.3)
269 (19.6)
134 (14.6)
27.4-36.6
23 (28.4)
151 (26.9)
211 (15.4)
267 (29.1)
36.6-45.7
7 (8.6)
65 (11.6)
86 (6.3)
119 (13.0)
45.7-54.8
7 (8.6)
50 (8.9)
58 (4.2)
316 (34.5)
Total
81
561
1,369
916
Table 5. — Comparisons of morphometric and
meristic characters of Pacific salmon whose dietary
components were investigated in this study.
Gillraker
Tooth
Species
No.1
Spacing2 •
Length3
size4
Sockeye
Pink
Coho
Chinook
33.7
30.4
21.2
20.7
close
moderate
wide
wide
2.6
3.4
2.1
2.0
smallest
small
moderate
large
'From Hikita (1962).
2From Morrow (1980).
3Gillraker length as percent of postorbital-hypural length.
Gillraker length is from Hikita (1962), postorbital-hypural
length from Beacham and Murray (1983).
"From Vladykov (1962), Hikita (1962).
86
BEACHAM: FOOD OF PACIFIC SALMON OFF BRITISH COLUMBIA
a larger proportion of the diet of larger chinook
salmon than of smaller ones (Milne 1955; Reid 1961).
In my study, the fish component of the diet was
similar for all size classes of chinook salmon. This
may be due to differences in availability of inverte-
brate prey to the smaller chinook salmon among the
studies. For example, Ito (1964) found that squid
were the largest dietary component of chinook and
coho salmon caught in drift nets in high seas
fisheries. Variability in diets of the different species
may be due in part to prey abundance, selection by
the predator, and possible selectivity by the sampling
gear used. Hook and line sampling may select fish
of different diets than would perhaps gill nets.
Salmon caught by trolling may have a higher com-
ponent of fish in the diet than those caught by gill
nets. In my study, fish did constitute a larger pro-
portion of the diet in larger coho salmon than in
smaller ones, as noted for chinook salmon. My study
has examined the distribution of prey types and sizes
for salmon caught from June to October only.
Although the relative proportions of fish and inverte-
brate prey could change seasonally for the salmon
species examined, the relative ranking of the species
in terms of proportion of fish in their diet should re-
main constant.
Availability of prey types can alter markedly the
proportions in a predator's diet. Herring comprised
over 70% of the stomach contents of troll-caught
chinook and coho salmon caught off the east and
west coasts of Vancouver Island in 1957 (Prakash
1962). My study showed that during 1967-68, her-
ring comprised <20% of the stomach contents of
chinook and coho salmon in the same area. Stock
abundances of herring declined rapidly in the late
1960's in British Columbia (Hourston 1978), in-
dicating that during a period of low herring abun-
dance, sand lance became an important dietary com-
ponent of chinook and coho salmon in this area.
Pink salmon in southern British Columbia and
Washington State show 2-yr cycles of abundance,
with returns absent in even-numbered years. This
pattern of abundance has been suggested to be a
result of predation by returning adults of the domi-
nant brood year on fry of the alternate brood year
(Ricker 1962). In my study, fish other than sand
lance, herring, or rockfish comprised <1% of the
stomach contents of pink salmon sampled in 1967.
These results suggest that predation by the domi-
nant broodline on the alternate broodline may be
neither necessary nor sufficient to account for cycles
in pink salmon abundance.
The effect of prey size on selection by planktiv-
orous fish has been examined by Werner and Hall
(1974), O'Brien et al. (1976), O'Brien (1979), Gibson
(1980), and Eggers (1982). Eggers found that
juvenile sockeye salmon prefer large nonevasive prey,
but will eat small and/or evasive prey when the
former is not available I found that as predator size
increased, prey size increased also, both in terms of
size of individuals within a prey type, and a shifting
from smaller to larger prey types. The predators
presumably decrease the amount of time and energy
needed to ingest a given amount of food by switch-
ing from smaller to larger prey, given that the large
prey types are sufficiently abundant. Werner and
Hall (1974) attributed a preference by predators for
only a part of the prey types available as a method
for increasing foraging efficiency. These results sug-
gest that the salmon species examined do select prey
both for size and availability, presumably to increase
foraging efficiency.
Morphological differences and diet partitioning
have been previously noted for many fish species
(Keast and Webb 1966; Hyatt 1979). As outlined by
Hyatt (1979), many planktivorous feeding fish tend
to have numerous, well-developed, close-set gill-
rakers. My study indicated that the more piscivorous
chinook and coho salmon have fewer gillrakers than
the more planktivorous sockeye and pink salmon.
Lake trout, Salvelinus namaycush, populations that
are more planktivorous also have more and longer
gillrakers than less planktivorous ones (Martin and
Sandercock 1967). Oncorhynchus masou (masou or
cherry salmon), found in the western Pacific Ocean,
has fewer gillrakers than either chinook or coho
salmon (Hikita 1962) and, as an adult, feeds largely
on fish (Tanaka 1965). Chum, 0. keta, salmon have
an average of 2-3 more gillrakers than chinook and
coho (Hikita 1962), and the diet of chum salmon sam-
pled in the spring and summer during 1956-63 in
the North Pacific comprised between 10 and 35%
fish (Neave et al. 1976). In the genus Oncorhynchus,
as gillraker number declines, the proportion of fish
in the diet increases. Morphological differences
among the species account for a greater partition-
ing of the diet than do differences in water depths
in which the individual species are located.
Pacific salmon are adaptable in their diet, shift-
ing their preferred prey species in relation to prey
size and abundance It seems unlikely that salmon
abundance is affected by the abundance of any one
type of prey. For example, the decline in abundance
of British Columbia herring stocks was not followed
immediately by declines in salmon abundance
Growth rates of salmon may be affected by changes
in diet and this could have an impact on stock popula-
tion dynamics.
87
FISHERY BULLETIN: VOL. 84. NO. 1
ACKNOWLEDGMENTS
I am indebted to those people who collected and
sampled the salmon for stomach contents that were
analyzed in this paper. Sharon Henderson and Bruce
Bernard were invaluable for their assistance in data
analysis and computer programming. J. G.
McDonald provided the initial suggestion for the
study. Clyde Murray and two referees offered many
valuable criticisms of the manuscript. Lauri Mackie
drafted the figures. The manuscript was prepared
with the help of the staff of the Publications Unit
of the Pacific Biological Station.
LITERATURE CITED
Allen, G. H., and W. Aron.
1958. Food of the salmonid fishes of the western North Pacific
Ocean. U.S. Fish Wildl. Serv., Spec Sci. Rep. Fish. 237, 11 p.
Beacham, T. D., and C. B. Murray.
1983. Sexual dimorphism in the adipose fin of Pacific salmon
(Oncorhynchus). Can. J. Fish. Aquat. Sci. 40:2019-2024.
Eggers, D. M.
1982. Planktivore preference by prey size Ecology 63:381-
390.
Foerster, R. E.
1968. The sockeye salmon, Oncorhynchus nerka. Bull. Fish.
Res. Board Can. 162:1-422.
French, R., H. Bilton, M. Osako, and A. Hartt.
1976. Distribution and origin of sockeye salmon (Oncorhyyi-
chus nerka) in offshore waters of the North Pacific Ocean.
Int. North Pac. Fish. Comm. Bull. 34, 113 p.
Gibson, R. M.
1980. Optimal prey-size selection by three-spine sticklebacks
(Gasterosteics aculeatus): a test of the apparent-size hypothe-
sis. Z. Tierpsychol. 52:291-307.
Godfrey, H., K. A. Henry, and S. Machidori.
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1971. Size selective predation among juvenile salmonid fishes
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89
DETERMINING AGE OF
LARVAL FISH WITH THE OTOLITH INCREMENT TECHNIQUE
Cynthia Jones1
ABSTRACT
Aging of larval fish from otoliths rests on the assumption that increments are formed daily. Indeed, proper
validation of the relationship between increment deposition and age is fundamental to accurate age deter-
mination of field-captured fish, lb evaluate the universality of daily deposition of otolith increments, the
literature was reviewed and exceptions discussed.
Laboratory studies under optimal conditions generally (17 species out of 20) show that larvae deposit
daily increments. However, in studies that examined increment deposition under suboptimal or extreme
conditions, deposition was not daily in over half of the species. Nondaily deposition caused by extreme
conditions (eg, total starvation, abnormal photoperiod) may not invalidate the otolith increment tech-
nique if those conditions do not occur in the field. Nondaily deposition under suboptimal conditions (eg.,
low temperature, intermittent starvation) that larvae may face in nature cause concern about this tech-
nique for aging field-captured larvae Deposition in many species has not been examined under suboptimal
conditions, nor has the effect of suboptimal conditions been shown on the age at first increment forma-
tion. The literature shows that the technique should be validated under both optimal conditions and those
that mimic nature
Otoliths have been used to age fish since Reibisch
(1899) first observed annular ring formation in
Pleuronectes platessa (as reported in Ricker 1975).
Assessing age by counting annular rings works well
in adults of temperate species where pronounced
seasonal changes in growth result in bands (formed
from tightly spaced growth increments deposited in
the winter) in the otolith which correspond to each
year of life Discovery of fine increments, analogous
to annual rings, but instead formed daily, has per-
mitted the age of larval fish to be determined.
While studying temperate water species, Pannella
(1971) observed that about 360 fine increments oc-
curred between annular rings and suggested that
these were deposited daily. He used this knowledge
when reading the otoliths of adult tropical fish
(whose otoliths also had fine increments) to show pat-
terns of growth that were grouped into 14- and 28-d
cycles (Pannella 1974).
The initial application of the otolith aging tech-
nique to larval fish was done by Brothers et al. (1976).
Daily increment deposition was verified for northern
anchovy, Engraulus mordax, and California grunion,
Leuresthes tenuis, which were reared from eggs in
the laboratory. Since this initial application, the
otolith increment technique has been used widely to
Graduate School of Oceanography, University of Rhode Island,
Kingston, RI 01882-1197; present address: Department of Natural
Resources, Cornell University, Ithaca, NY 14853.
estimate age in at least 29 species of larval fish. It
has been used in freshwater and marine species, and
applied to field-captured species, at times without
adequate validation.
The ultimate purpose in developing the otolith
aging technique for application to young fish is the
ability to accurately age field larvae and juveniles.
If the technique is to be applied directly to the field,
based on conclusions drawn from rearing larvae in
the laboratory, then the deposition of increments
must be daily under conditions experienced in the
field during these early life stages. The applicability
of this technique relies on the assumption that 1)
either surviving larvae (or sampled larvae) are those
that grew under moderately good conditions (few lar-
vae under suboptimal conditions survive) or 2) lar-
vae can encounter suboptimal conditions, a propor-
tion of these larvae will survive, and increment
deposition is not affected by these suboptimal con-
ditions. The first assumption is difficult to evaluate
without using the hypothesis that increments are
daily. The second assumption has been tested and
the results can be summarized. The second assump-
tion is based on increment deposition being triggered
by a zeitgeber, an external factor that entrains a diel
cycle within the larvae
Validation of daily increment deposition under con-
ditions within the natural range of experience of the
larvae is fundamental to accurate estimation of age
in field-captured fish. When the estimation technique
Manuscript accepted March 1985.
EISHEEY ptit T itttm. wm Q/i wn i iqoc
91
FISHERY BULLETIN: VOL. 84, NO. 1
used to age larvae is inaccurate, estimates of growth
and mortality, which rely on knowledge of age, will
also be inaccurate
The purpose of this paper is to discuss the use of
the otolith increment technique to age larval fish.
The published literature is used to evaluate the
hypothesis, H0: Larval age is equal to otolith incre-
ment count (plus age at first increment deposition)
under conditions that are encountered in the field.
An additional idea can be evaluated: That time of
initial increment deposition is influenced by incuba-
tion time
The paper will discuss the factors which affect
deposition of increments, validation studies that have
been performed, and application of the technique in
the field. Factors which are likely to affect increment
deposition in the field must be assessed by the valida-
tion procedure In addition, the adequacy of valida-
tion that has been performed is evaluated, and
ramifications in field applications are discussed.
FACTORS AFFECTING
DEPOSITION RATES
Mechanisms that have been postulated as initiators
of differentiation of otolith microstructure are photo-
period, feeding, and temperature Increment deposi-
tion has been tested in the literature under two
conditions: 1) tests within the natural range of
experience of the fish which could be optimal (non-
stressful) and suboptimal (stressful), and 2) abnor-
mal conditions that are wholly outside of their
experience
Taubert and Coble (1977) stated that photoperiod
entrained a diel clock that resulted in daily forma-
tion of otolith increments. Tanaka et al. (1981) stud-
ied the formation of increments in Tilapia nilotica
using scanning electron microscopy and found that
the fast growth (incremental) zone started a few
hours after light stimulus and that the slow growth
(discontinuous) zone was formed immediately after
light stimulus. Neither change in photoperiod length
nor feeding time affected increment initiation.
Brothers and McFarland (1981), however, reported
that the discontinuous zone began near midnight.
These results are contradictory, and without further
investigations force the conclusion that the temporal
formation of increments is species-specific
Abnormal photoperiods have been shown to dis-
rupt daily increment formation in Fundulus hetero-
clitus (Radtke and Dean 1982) and in Tilapia
mossambica (Taubert and Coble 1977). Constant
light, however, did not disrupt daily increment forma-
tion in Oncorhynchus tshawytscha (Neilson and Geen
1982) or in Scophthalmus maximus (Geffen 1982).
Unlike photoperiod changes, which are regular and
gradual in nature, feeding times can occur at irre-
gular intervals and might cause deviations in daily
increment deposition. Two studies have tested the
effects of feeding within the normal range experi-
enced by fish larvae Neilson and Geen (1982) found
that subdaily increments could be induced through
frequent discrete feedings: feeding four times a day
resulted in formation of more than one increment
in Oncorhynchus tshawytscha. Daily and subdaily in-
crements were not distinguished in counts. Tanaka
et al. (1981) found conversely that feeding time had
no effect on the initiation of increment formation
in Tilapia nilotica. Larvae were fed once a day, but
the times of feeding were changed. Perhaps multi-
ple feeding during the day results in the subdaily in-
crements that sometimes appear in otoliths. The ef-
fect of starvation (an extreme circumstance in the
field) on increment deposition has been tested in only
three species: Scophthalmus maximus (Geffen 1982),
Morone saxatilis (Jones 1984), and Oncorhynchus
nerka (Marshall and Parker 1982). Geffen raised the
turbot larvae on rotifers and Artemia until they were
10 d old. Larvae were then starved for 23 d. Jones
did not supply exogenous food from hatch onward.
Both Geffen and Jones found that starvation
disrupted increment formation. Marshall and Parker
fed their sockeye salmon larvae for the first 3 wk
of life, and then starved them for 2 wk. Marshall and
Parker found that starvation over 2 wk had no ef-
fect on increment deposition. It is possible that the
difference might reflect different age-specific sen-
sitivity to starvation, rather than species-specific
responses.
Brothers (1978) has linked temperature as a prime
factor in increment deposition. Working with tem-
perate stream populations, he has found that diel
temperature changes result in daily increment for-
mation. Brothers (1978) stated that "six or more in-
crements per day may be formed as the result of
short term, . . .relatively minor. . . temperature fluc-
tuations." Other investigators (Radtke and Dean
1982; Geffen 1982) found that small temperature
changes had no effect on the rate of increment
deposition. Apparently, temperature response is also
species-specific.
LABORATORY STUDIES OF
INCREMENT DEPOSITION
Initial Ring Deposition
When fish are raised in the laboratory from eggs
92
JONES: DETERMINING AGE OF LARVAL FISH
through the larval stages, two parameters fun-
damental to application of the increment technique
to field populations can be determined: 1) age at first
increment deposition and 2) testing of daily incre-
ment deposition under artificial conditions. Age at
initial increment deposition for 18 species of fish is
listed in Table 1. Radtke (1978) speculated that in
species having slowly developing embryos, initial
deposition occurs at, or before, hatch; in species
having rapidly developing embryos, initial increment
deposition does not occur until yolk-sac absorption
or first feeding. This hypothesis is not substantiated
in the currently published literature. Information for
nine species of laboratory-reared fish larvae (Table
2) shows no such trend for data currently reported
in the literature Even for the same suborder, Clu-
peoidei, opposite development and initial increment
deposition patterns exist for herring (Clupea haren-
gus) and the northern anchovy.
The Case for Daily Increment Deposition
Seventeen species have shown consistent daily
deposition of increments under what are presumed
to be good conditions for growth. The species that
have shown daily increment deposition come from
both freshwater and marine habitats and encompass
a wide variety of lifestyles. In addition, six species
held in the laboratory and sampled over known
periods of time demonstrated daily increment
deposition (Table 3). Four investigation groups
(Struhsaker and Uchiyama 1976 for Stolephorus pur-
pureas, Taubert and Coble 1977 for Lepomis macro-
chirus, Campana and Neilson 1982, Wilson and
Larkin 1980 for Oncorhynchus nerka) brought lar-
vae and juveniles into the laboratory, reared them
for a period of time, then correlated increment
counts to days of captivity. Schmidt and Fabrizio
(1980) took consecutive samples from a field popula-
tion of Micropterus salmoides, which had a short
spawning period and correlated the time between
samples to the change in mean increment count.
Lack of Daily Deposition Rates
The most controversial results obtained so far
come from studies of increment deposition in larval
Clupea harengus (Table 1). Agreement for daily in-
crement deposition has not been obtained. Studies
that observed daily deposition by Gjosaeter2 and
and Gj«isaeter and 0iestad (1981) indicate that
2Harold Gjdsaeter, Institute of Marine Research, P.O. Box 1870
5011 Bergen, Norway, pers. commun. February 1983.
increments are deposited with roughly daily
periodicity and that initial increment deposition
begins at first feeding (4-5 d). Gjosaeter and
0iestad (1981) found that 99 increments were
formed in 97-d-old larvae. Gjosaeter, however, cau-
tioned that these results were based on small sam-
ple sizes. Lough et al. (1982) reported on larval her-
ring reared in the laboratory that lived until age 18
d. They did confirm that increment deposition began
at yolk-sac absorption, but did not find that the in-
crements were daily. In fact, only three increments
were laid down within 18 d. Lack of confirmation
of daily deposition is easy to dismiss, since the lar-
vae did not survive past 18 d.
However, Geffen (1982) has demonstrated an inter-
action between growth rate and increment deposi-
tion rate. Only under circumstances of very fast
growth, 0.42 mm/d (a rate which is faster than
growth rates postulated for field animals) did incre-
ment deposition approach daily periodicity (0.92 in-
crements/d). It is noteworthy that the growth rates
in her study were related to container size; faster
growth occurs in bigger containers. The variance of
increment count at age is small and homogeneous
only under the fastest growth condition (Norway
Pond). The increasing variance with age in the other
conditions leads to the speculation that some of these
larvae were unknowingly starving. However, since
the slope of the regression line for the Norway Pond
condition is significantly different than 1 incre-
ment/d, this result cannot be dismissed. There would
be obvious value in repeating these experiments. Gef-
fen also found that increment formation did not
begin before yolk-sac absorption and was in agree-
ment with the other investigators on this point. The
literature (Table 1) shows only one case (Oncorhyn-
chus nerka) where independent investigators have
confirmed daily increment deposition (Wilson and
Larkin 1980; Marshall and Parker 1982).
Geffen (1982) found that increment deposition was
also a function of growth in Scophthalmus maximus
(Table 4) under various conditions of temperature
and photoperiod. Under two conditions— 1) 20°C,
constant light, and 2) 24°C, 12L:12D— increments
were deposited daily For all other conditions in-
crements were not daily. Under all conditions,
deposition rate was a function of length. Although
Geffen did not point this out, comparisons of growth
at different temperatures can also be drawn from
the data. Larvae were grown under 20°C and 24°C,
both under a 12L:12D cycle. Larvae grew faster and
deposited more increments at 24°C. Such differences
in temperature might be used to explain differences
in increment deposition except that the other case
93
FISHERY BULLETIN: VOL. 84, NO. 1
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JONES: DETERMINING AGE OF LARVAL FISH
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95
FISHERY BULLETIN: VOL. 84, Na 1
Table 2.— Relationship between incubation time, egg size, and initial increment deposition: Determing whether species with long incuba-
tion and large eggs initiate increment deposition on or before hatch, while species with short incubation and small eggs initiate increments
at first feeding or yolk sac absorption, ysa = yolk sac absorption.
Initial
Egg
Temper-
Incubation
increment
size
Species
ature
Source
time
Source
deposition
Source
(mm)
Source
Clupea harengus
=10°C -
Blaxter (1969)
=18 d
Blaxter (1969)
4-5 d ysa
See Table 1
0.9-1.7
Blaxter (1969)
Engraulis
11°-21°C
Lasker (1964)
1-5d
Lasker (1964)
=5 d
Brothers et al.
^2
mordax
(1976)
Fundulus
24°-30°C
Radtke (1978)
14 d
Radtke (1978)
Before hatch
Radtke (1978)
2
Armstrong and
heteroclitus
Child (1965)
Gadus morhua
4°C
Radtke and
Waiwood
(1980)
19 d
Radtke and
Waiwood
(1980)
1 d
Radtke and
Waiwood
(1980)
1.1-1.6
Blaxter (1969)
Menidia menidia
19.4°-
Barkman
7-10 d at
Barkmann
Before hatch
Barkman
1.2
Barkmann and
21.6°C
(1978)
23°-25°C
and Beck
(1976)
from
regression
(1978)
Beck (1978)
Morone saxatilis
18°C
Jones (1984)
2 d
Jones (1984)
6-9 d
Jones (1984)
Parophrys
20°C
Laroche et al.
3-3V2 d
Laroche et al.
4-5 d
Laroche et al.
vetulus
(1982)
(1982)
(1982)
Pseudopleu-
5°-8°C
Radtke and
14 d at
McPhee'
9-10 d
Radtke and
0.8
Smigielski and
ronectes
Scherer
8°C
Scherer
Arnold
americanus
(1982)
(1982)
(1972)
Tilapia nilotica
27°C
Tanaka et al.
(1981)
4 d
Tanaka et al.
(1981)
At hatch
Tanaka et al.
(1981)
'Grace McPhee, P.O. Box 210972, Auke Bay, AK 99821, per. commun. summer 1983.
Table 3.— Otolith increment deposition for larval fish maintained in the laboratory over a known time span.
Are
Known-age
increments
Number
Species
Source
span
<
daily?
Validation
of fish
Lepomis
Taubert and Coble
=6-176 d
yes
Correspondence be-
gibbosus
(1977)
after
swim up
tween age and rings
Lepomis
Taubert and Coble
=6-125 d
yes
Correspondence be-
macrochirus
(1977)
after
swim up
tween age and rings
Micropterus
Schmidt and Fabrizio
Between 47 and 81
yes
Correlation between
98
salmoides
(1980)
rings
change in ring
count and time
interval
Oncorhynchus
Wilson and Larkin
Between 14 and 26
yes
Slope = 1 ring/d
100
nerka
(1980)
rings
Platichthys
Campana and Neilson
8-10 mo old
yes
Slope = 1 ring/d
13 (in situ)
stellatus
(1982)
81 (temp and
light)
Stolephorus
Struhsaker and
yes
Correspondence be-
174
purpureus
Uchiyama (1976)
tween rings and
days
of daily deposition (24L, 20°C) would be an anomaly
under this hypothesis.
Ten studies have investigated deposition rates
under suboptimal, extreme or varying conditions
(Table 4). These studies are important to the under-
standing of the underlying mechanisms causing in-
crement deposition. Two studies, one by Radtke and
Dean (1982) and one by Taubert and Coble (1977),
demonstrated disruption of daily increment forma-
tion under extreme or abnormal changes in photo-
period. Taubert and Coble (1977) found that in
simulated winter conditions, cold temperature and
shorter photoperiod resulted in cessation of incre-
ment formation in Lepomis cyanellus. At and below
temperatures of 10°C, growth and increment deposi-
tion ceased. If such changes occurred gradually, as
occurs in the normal lifetime of fish, acclimation to
these temperature changes might be expected
through most of the temperature range. Within nor-
mal physiological limits (especially where some
growth continued), increment deposition would be
assumed to continue regularly. However, Marshall
and Parker (1982) also found that temperatures
below 10°C resulted in cessation of increment deposi-
tion in sockeye salmon. Hence two studies have
shown that increment deposition is not maintained
96
Table 4.— Otolith increment deposition for known-age larval fish under experiments where various culture conditions were tested.
■
Source
Conditions of growth
Species
Light
Food
Temp Other
tank size
120 L, 500 L,
Effect on increment deposition
Clupea
Geffen (1982)
Increment deposition rate was re-
lated to growth rate. Also, larvae
harengus
310 m3 4,440 m3
grew faster in bigger container and
deposited more rings.
Fundulus
heteroclitus
Radtke and Dean
(1982)
Multiple
L/D con-
ditions
24°C
30°C
Temperature affects growth rate, but
not increment deposition. Increment
deposition rate disrupted under con-
stant dark or under <24-h photo-
period.
Lepomis
cyanellus
Taubert and Coble
(1977)
15L/9D
10L/14D
4°-25°C
Fewer hours of light and lower
temperature resulted in cessation of
ring deposition. At 10°C or less,
growth ceased, as did increment
formation.
Morone
saxatilis
Jones (1984)
14L/10D
Fed, starved,
intermittent
18°C
Increment deposition rate was dis-
rupted during periods of starvation.
starved, then
Increments not daily in sagittae dur-
fed
ing 2-3 mo under optimal conditions.
Oncorhynchus
nerka
Marshall and
Parker (1982)
Fed
Starved
<10°C
>10°C
Starvation for 10 d did not affect in-
crement deposition. Temperatures
<10°C resulted in cessation of incre-
ment formation.
Oncorhynchus
tshawytscha
Neilson and Geen
(1982)
24D
24L
12L/12D
4x/d
1x/d
11°C
5.2°C
Formation of increments was related
to feeding frequency. Temperature
affected width of increment, not
deposition rate. Photoperiod had no
effect.
Salmo salar
Geffen (1983)
24D
6L/6D
12L/12D
8°C
10°C
15°C
Rate of ring deposition increased
with increased light and temperature.
Scophthalmus
maximus
Geffen (1982)
24L
6U6D
12U12D
Fed
Starved
20°C
24°C
Daily increments formed under
24L-20°C and 12L/12D-24°C. Starva-
tion and 6L/6D interrupted increment
formation. Increment formation
related to growth rate.
Tilapia
mossambica
Taubert and Coble
(1977)
24L
24U12D
15U9D
Every 3 h
Every 6 h
Intermittent
Daily increments formed under 24-h
photoperiod, not under 36-h cycle
nor constant light. Subdaily incre-
ments induced. No effect from
feeding cycle.
Tilapia
nilotica
Tanaka et al.
12U12D
3 h before dark
Formation of increment triggered by
(1981)
18L/6D
6U18D
3 h after light
light stimulus. Feeding time had no
effect under 12L/12D.
below certain temperatures. In two other studies
where temperatures ranged from 24°C to 30°C
(Radtke and Dean 1982) and from 5.2°C to 11°C
(Neilson and Geen 1982), these temperatures af-
fected thegrowth rate and width of increments, but
did not alter the increment deposition rate
Six studies looked at the relationship between
feeding and daily increment deposition. Jones (1984),
Geffen (1982), and Marshall and Parker (1982)
showed opposite effects of starvation on increment
deposition. Jones (1984) found that starvation of
young larvae for 2 wk resulted in deposition of only
one increment every other day. However, in addition
to lengthy starvation, the effect of short-term, in-
termittent periods of starvation was also studied and
resulted in nondaily increment formation. Geffen
(1982) found that starvation interrupted deposition
in larval turbot, while Marshall and Parker (1982)
found that starvation for 2 wk had no effect on daily
deposition in sockeye salmon. Long-term starvation
experiments test for interruption of increment
deposition under extreme conditions. lb age larvae
in the field, it is important to determine the mini-
mum number of consecutive days of starvation need-
ed to affect increment deposition. Once these values
are known, it is important to determine whether field
larvae actually experience these levels of deprivation.
Three studies looked at feeding time or frequen-
cy on increment deposition. Neilson and Geen (1982)
found that feeding frequency could induce forma-
97
FISHERY BULLETIN: VOL. 84, NO. 1
tion of subdaily increments in Oncorhynchus
tshawytscha. Both Tanaka et al. (1981) and Taubert
and Coble (1977) found that feeding time had no ef-
fect on increment deposition in larval mouthbrooders
(Tilapia nilotica and T. mossambica).
Little agreement has been reached in these studies
concerning the effect of light, temperature, or
feeding on increment formation. The effects of
variability in temperature, food, salinity, and other
factors (extreme photoperiods would not be en-
countered) relate directly to the problems of ac-
curately aging larvae from the field. At the moment,
environmental effects appear to be species-specific.
Indeed, specific tests of the effect of suboptimal con-
ditions (which are likely to occur in the field) on in-
crement deposition have rarely appeared in the
literature Such analyses, conducted for more
species, might confirm the conventional wisdom that
deviation from daily deposition rate is abnormal.
However, the questions raised by the studies re-
viewed here (Table 4) remain to be fully addressed
or dispelled.
APPLICATION IN THE FIELD
Current Applications
The ability to age larval fish precisely provides
more accurate estimates of growth, mortality, and
the ability to discern the effects of environmental
variables on the first year of life Rapid growth in
the first months of life has commonly been thought
to be critical to survival. Evidence in support of this
hypothesis (Brothers et al. 1983) and contrary to it
(Methot 1983) exists.
The otolith increment aging technique has been
Table 5. — Application of the otolith increment aging technique in field grown larvae.
Species
Source
Based on prior
validations
(validations in
Table 1)
Validation
source
Sample
size
Application
Ammodytes
Scott (1973)
no
71
dubious
Clupea
Graham and Joule
controversial
See Table 1 for
545
harengus
(1981)-
Geffen (1982)
found deposition
details
Townsend and
depended on
300
Graham (1981)
growth rate.
Gjdsaeter and
Lough et al.
(1982)
0iestad (1981)
found deposition
311
was daily. See
Table 1 for
Jones (1985)
details.
481
Engraulis
Methot and
yes
Brothers et al.
587
mordax
Kramer (1979)
(1976)
Fundulus
Radtke and Dean
yes
Radtke and Dean
not
heteroclitus
(1982)
(1982)
given
Gadus mgrhua
Gjdsaeter and
Tilseth (1981)
yes
Radtke and
Waiwood (1980)
30
-
Steffenson (1980)
yes
Radtke and
Waiwood (1980)
138
Haemulon
Brothers and
no, but refers to
=306
flavolineatum
McFarland
(1981)
data as otolith
age
Halichoeres
Victor (1982)
yes
marked juveniles
10
bivittatus
Lepomis
Taubert and Coble
yes
Taubert and Coble
= 150
macrochirus
(1977)
(1977)
Back-calculated growth.
Determine hatching dates and de-
lineate cohorts which are followed
through time.
Determine hatching dates and as-
sess growth rates of larval cohorts.
Noted cessation of growth in winter.
Use age to delineate growth. Fit
Gompertz function of length-at-age
data.
Determination of within-season
growth differences based on uncer-
tainty in otolith aging.
Fit Gompertz function to length-at-
age data to obtain growth rates. Also
mention that starvation slowed incre-
ment deposition.
Compare length-frequency histo-
grams with increment-frequency his-
tograms. Show relationship between
hatching and lunar cycle.
Regression of age estimated from
morphologic development versus in-
crement counts.
Back-calculated hatch date from in-
crements. Compare these to field
observations of spawning time.
Correspondence between otolith
microstructure and events in the life
history. Derive "otolith" growth
rates.
Determine daily deposition of incre-
ments and use to determine settling
pattern.
Allometric relationship between oto-
lith length and fish length tested for
2 lakes.
98
V JONES: DETERMINING AGE OF LARVAL FISH
applied to larval field populations of many species
of fish (Table 5). Most applications have been based
on laboratory validation of daily increment deposi-
tion for the individual species studied. Some have
not. Methot and Kramer (1979), based on validation
of daily increment deposition by Brothers et al.
(1976), obtained growth rates for wild populations
of Engraulis mordax by fitting a Gompertz function
to length-at-age data. Various other field applications
of the increment aging technique are listed in Table
5. Of special interest is a comparison of growth
estimates for Parophrys vetulus from modal progres-
sion of length frequencies and otolith increments
(Laroche et al. 1982). Growth based on the increment
count method was 2-3 times faster. If the increment
count method proves to be accurate, then mortality
estimates could be considerably changed.
For at least four species listed in Table 5, labora-
tory validation was not conducted. These applica-
tions assume a given age at initial deposition and
daily increment deposition thereafter. The validity
of these assumptions depends on the species and on
the sensitivity of the application to inexactness in
the age estimation. For example, controversial results
have been obtained for larval herring, Clupea
harengus. Geffen (1982) showed that growth rates
could be overestimated by as much as three times
the actual rate However, analysis of Gulf of Maine
herring data (Jones 1985) showed that differences
in growth between larvae hatched early and late in
the season could be drawn. Until sensitivity analyses,
laboratory verification, or other evidence exists to
assure daily increment formation as a universal
phenomenon under suboptimal conditions, there will
be some doubt about the accuracy of aging field-
captured larvaa
Transition from the Laboratory
to the Field
A question that remains to be answered when
applying laboratory-derived increment deposition
Table 5.— Continued.
Species
Source
Based on prior
validations
(validations in
Table 1)
Validation
source
Sample
size
Menidia
Barkman et al
menidia
(1981)
Morone
Brothers et al.
saxatilis
(1976)
yes
no
Barkman (1978)
105
(lab)
Application
Oncorhynchus
nerka
Wilson and Larkin
(1982)
yes
Wilson and Larkin
(1980)
64
Parophrys
vetulus
Laroche et al.
(1982)
yes
Laroche et al.
(1982)
331
Rosenberg and
Laroche (1982)
yes
Laroche et al.
(1982)
233
Pseudopleu-
ronectes
Radtke and
Scherer (1982)
yes
Radtke and
Scherer (1982)
120
amencanus
Stolephorus
purpureus
Struhsaker and
Uchiyama (1976)
yes
Struhsaker and
Uchiyama (1976)
213
Thalossoma
bifasciatum
Victor (1982)
Victor (1983)
yes
Victor (1982)
marked juveniles
68
103
28 species of
coral reef fish
Brothers et al.
(1983)
no
210
Compare growth in lab and field.
Calculate hatching dates. Compare
growth between early and late
hatched larvae.
Correspondence between increment
estimated age and spawning
season. Growth through lifetime of
juvenile.
Relationship between fish weight
and otolith size. Use daily in-
crements as time marker.
Determine growth of aged field lar-
vae and fit Gompertz and von Ber-
talanffy functions. Compare length-
frequency and otolith techniques.
Growth during metamorphosis. Re-
late to age and transformation in
morphology.
Comparison of length-frequency and
increment-frequency histograms for
field larvae. Daily growth rate calcu-
lated. Compare growth rates over
time.
Built growth curves based on age.
Discussion of relationship to feeding.
Preliminary study of growth rate dif-
ference between areas.
Determine daily increment deposi-
tion. Calculate pattern of settlement
based on age estimate.
Determine length of larval life prior
to recruitment. Examine otoliths
for marker between postlarvae to
juvenile.
99
1 IOilL.ni UULiLiLillll. »VU. Ol, l*KJ. 1
rates to field populations is the constancy of deposi-
tion rates between these environments. Most labora-
tory studies have occurred under constant tempera-
ture and salinity and under conditions of artificial
food types and densities and low light intensities
compared with the field. Often, increments from
otoliths of laboratory-grown larvae are much fainter
than those from otoliths of field-captured larvae
Since field conditions can fluctuate to extents that
have been shown to cause increment disruption in
laboratory situations, a way to verify daily deposi-
tion in the field would be an important contribution.
A transitional step between the laboratory and the
field has been made by Laurence et al. (1979) and
0iestad (1982). Laurence et al. (1979) raised known-
age larvae in a flow through enclosure This study
was designed to measure the growth and survival
of fish larvae exposed to varying prey concentrations
in the field. Modifications of this system could be
used to study increment deposition in known-age lar-
vae exposed to field conditions. 0iestad (1982) pre-
sented a review of larval fish studies performed in
enclosures. Gjrisaeter and 0iestad (1981) reared
known-age larvae in large enclosures and determined
increment deposition rates (Table 1). Few inves-
tigators have used such enclosures for validation of
otolith increment deposition rates for field simulated
studies. Enclosures should prove particularly
valuable for validation and simulation of suboptimal
field conditions on growth and increment deposition.
Statistical Applications
Once the veracity of daily increment deposition is
established, a wide variety of statistical methods can
be used in otolith studies. Statistical methods that
have been employed in larval otolith studies have
been linear regressions to establish increment
deposition rates and curve fitting techniques to es-
tablish growth rates from length-at-age data. Linear
regression has also been applied regardless of
whether it actually fits the data. It is important to
check for lack of fit, selection of the appropriate
model, and weighting before applying linear regres-
sion blindly. It is recommended that, when possible,
confidence intervals and standard deviations be in-
cluded in the data presentation.
Investigators are beginning to relate increment
widths, as indicators of growth, with environmen-
tal conditions (Methot and Kramer 1979; Lough et
al. 1982). When increment widths are correlated
directly with environmental factors, either no
correlations are seen (Neilson and Geen 1982) or
correlations may be spurious. Problems exist in
measuring the physical conditions to which the lar-
vae have been exposed, especially since larvae may
move from one area to another. In addition, there
are questions concerning food availability and its
concentration and patchiness. Another consideration
in relating growth to environmental conditions is
that, as the fish grows, the width of the outer incre-
ments decreases proportionately to decreases in
length. Better results might be obtained either with
covariance analysis or by fitting a growth function
to data then using the residuals in correlation tests.
Investigations of residuals with exploratory tech-
niques such as principal component analysis or
canonical correlation might prove fertile
Comparison of Scanning Electron and
Light Microscopy
Scanning electron microscopy (SEM) has been
used to confirm otolith structure (Dunkelberger et
al. 1980; Watabe et al. 1982) and to compare incre-
ment counts with those obtained by transmitted light
microscopy (Radtke and Waiwood 1980; Campana
and Neilson 1982; Neilson and Geen 1982; Radtke
and Dean 1982; Tsuji and Aoyama 1982; Ralston and
Miyamoto 1983). Under optimal conditions, counts
using both methods were equivalent except for lar-
val cod. Radtke and Waiwood (1980), using SEM,
determined that cod produced daily increments from
hatch onward, while Gj«teaeter (1981), using a light
microscope, did not observe increment formation un-
til 4-5 d after hatch.
Most investigators did not verify deposition seen
with the light transmission microscope with SEM
studies. Confirmation with SEM is highly desirable
when increments are nondaily. However, extensive
use of the technique for field surveys is prohibited
by the additional cost and preparation time when
compared with light microscopy. In cases where
suboptimal or abnormal field conditions may result
in nondaily increment formation (Jones 1984), SEM,
used in conjunction with ancillary techniques, may
assist identification of the proportion of larvae for
which age is underestimated with light micros-
copy.
CONCLUSIONS
The report of the otolith workshop held in Bergen,
Norway (Anonymous 1982) stated that the ap-
pearance of increments in otoliths of larval fish living
in diverse habitats and representing many families,
argues strongly for the universality of this phenom-
enon. Validation that these increments are indeed,
100
JONES: DETERMINING AGE OF LARVAL FISH
deposited daily has been reported in 17 out of 20
species (Table 1) grown under optimal laboratory
conditions. However, evidence exists that daily
deposition can be interrupted under suboptimal and
abnormal conditions, or can be dependent on growth
rate (Table 6). When the effect of photoperiod is ig-
nored (changes in photoperiod are very gradual in
the field), more than 50% of the tests under subop-
timal and extreme conditions have shown nondaily
increment deposition rates. For other species, tests
under suboptimal conditions were not conducted and
the effect of these conditions on increment deposi-
tion rate is undetermined. The effect of varying con-
ditions on the age at initial increment deposition has
also not been addressed. To apply the otolith aging
technique to fish from the natural environment, the
scientist must either assume that larvae sampled
grew under optimal conditions (those exposed to
suboptimal conditions died) or verify that the species
almost always deposit daily increments under field
encountered conditions, or establish the error
bounds for the relationship between age and incre-
ment count.
Attempts to clarify the natural phenomena that
drive daily increment formation have given con-
flicting results. Photoperiod, feeding periodicity, and
temperature fluctuations have all been cited as
causing daily increment formation. When these fac-
tors are within normal ranges, it is likely, for most
larvae, that deposition is daily. However, for larvae
experiencing conditions outside tolerable ranges or
abnormal conditions, the period of formation is likely
to deviate from daily deposition. It is important to
determine whether the minimum exposure to subop-
timal conditions which result in nondaily deposition
is actually experienced by larvae in the field. These
hypotheses are amenable to further testing. More
basic research on the causation of increment deposi-
tion or more extensive testing under a variety of con-
ditions for a given species will yield more informa-
tion. In situ testing with known-age larvae in
enclosures which closely mimic field conditions could
yield valuable results. The Bergen otolith workshop
report (Anonymous 1982) has recommended that in-
crement deposition be verified for each new species,
under a variety of test conditions.
Two issues, cost effectiveness and accuracy, are im-
portant in determining whether the otolith incre-
ment technique is preferable to length-frequency
analysis. Recommendations made in the report from
the Bergen otolith workshop (Anonymous 1982) are
that "the precision of an age determination ... be
tested against other available methods ... by a cost
benefit analysis (i.e is enough precision gained by
Table 6— Incidence of nondaily increment deposition for
species reared under suboptimal and extreme conditions.
Stars (*) indicate nondaily deposition caused by exposure to
suboptimal conditions; triangles (A) indicate nondaily deposi-
tion caused by exposure to extreme conditions; circles (O) in-
dicates no interruption of daily deposition.
Tank
Species
Light
Food
Temp
size
Clupea harengus
•
Fundulus heteroclitus
• ,A
O.
Lepomis cyanellus
•
•
Morone saxatilis
*,A
Oncorhynchus nerka
O
•
0. tshawytscha
O
O
• O
Salmo salar
A
*
Scophthalmus maximus
O.A
A
Tilapia mossambica
A
O
T. nilotica
*
o
using this method to pay the costs and effort in
preparation)". A good example would be the results
shown in Laroche et al. (1982) when the otolith
method was compared with modal progression of
length frequencies, estimated growth rates differed
by a factor of 2-3. Benefits should also include non-
monetary considerations, such as decrease in error
which will propagate through estimates based on age
determinations (i.e, growth and mortality). Sensi-
tivity analyses can be used to show situations where
more accurate estimates are necessary.
Specific recommendations for improving reliability
and replicability are discussed in the Bergen otolith
workshop report (Anonymous 1982). In addition to
these, Brothers3 has suggested that other otoliths, (
such as the lapillus, be used in analysis.
Aging by the otolith increment technique is a
powerful tool. Not only can population estimates of
growth and mortality be refined, but growth of in-
dividuals can be obtained. Issues such as the impor-
tance of environmental factors to survival, the pro-
portion of fast growing larvae to recruitment, and
demonstration of compensation in field larvae may
become easier to address with the availability of this
technique However, it is equally important to make
sure that the technique is based on good scientific
technique
ACKNOWLEDGMENTS
I thank David Bengtson, John Forney, Saul Saila,
Ann Durbin, and Bernard Skud for their thoughtful
review of this manuscript and Walter Berry for his
many helpful suggestions and discussions.
3Edward Brothers, 3 Sunset West, Ithaca, NY 14850, pers. com-
mun. September 1983.
101
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103
PATTERNS IN DISTRIBUTION AND ABUNDANCE OF A
NONCOEVOLVED ASSEMBLAGE OF ESTUARINE FISHES IN CALIFORNIA
Peter B. Moyle,1 Robert A. Daniels,2 Bruce Herbold,1
and Donald M. Baltz3
ABSTRACT
The patterns of distribution and abundance of the fishes of Suisun Marsh, a portion of the Sacramento-
San Joaquin estuary in central California, were studied over a 54-month period. Tbtal fish abundance
in the marsh exhibited strong seasonality; numbers and biomass were lowest in winter and spring and
highest in late summer. Freshwater inflow was highest in the winter and lowest in late summer, when
salinities and temperatures were highest. Twenty-one species were collected on a regular basis; the 10
most abundant were Morone saxatilis, Pogonichthys macrolepidotus, Gasterosteus aculeatus, Hysterocarpus
traski, Cottus asper, Spirinchus thaleichthys, Acanthogobius fl.avimanus, Catostomus occidentalis, Lep-
tocottus armatus, and Platichthys stellatus. Another 21 species occurred in small numbers on an irregular
basis. Twenty of the 42 species had been introduced to California since 1879. Of the 21 common species,
14 were residents, 4 were winter seasonals, and 3 were spring/summer seasonals. The resident species
fell into two groups: a group of native species that were concentrated in small dead-end sloughs and a
group of native and introduced species that were most abundant in the larger sloughs. The seasonal species
were also a mixture of native and introduced species. Tbtal fish abundance and species diversity declined
through the study period, which seemed to be related to strong year classes of some species early in
the study and the prevalance of freshwater conditions late in the study. The structure of the fish assemblage
was fairly consistent over the study period but changes are expected in the near future The structure
of the Suisun Marsh fish assemblage was similar to that found in other river-dominated estuaries, despite
the mixture of native and introduced species.
The Sacramento-San Joaquin Estuary system is the
largest estuary on the west coast of North America.
It has been highly modified by surrounding urban,
industrial, and agricultural development and by ex-
tensive diversion and pollution of the freshwater that
flows into it (Conomos 1979). It supports a diverse
fish fauna of native and introduced species, but most
previous studies have concentrated on species impor-
tant to sport and commercial fisheries, especially
striped bass, Morone saxatilis, and, to a much lesser
extent, white sturgeon, Acipenser transmontanus;
chinook salmon, Oncorhynchus tshawytscha; Ameri-
can shad, Alosa sapidissima; and white catfish, Icta-
lurus catus (Skinner 1972; Moyle 1976). Studies of
other species have been few (Ganssle 1966; Turner
and Kelley 1966; Baltz and Moyle 1982; Stevens and
Miller 1983; Daniels and Moyle 1983), and there have
been no community-level analyses equivalent to those
conducted on estuarine fish communities in other
'Wildlife and Fisheries Biology, University of California, Davis,
CA 95616.
zWildlife and Fisheries Biology, University of California, Davis,
CA; present address: Biological Survey, New York State Museum,
Albany, NY 12230.
3Wildlife and Fisheries Biology, University of California, Davis,
CA; present address: Coastal Fisheries Institute, Louisiana State
University, Baton Rouge, LA 70803.
parts of the world (e.g., Dahlberg and Odum 1970;
Livingston 1976; Sheridan and Livingston 1979;
Meeter et al. 1979; Blaber and Blaber 1980; Quinn
1980; Thorman 1982). The fish assemblage of the
Sacramento-San Joaquin Estuary system is unusual
because few of its component species are likely to
have evolved together; it is composed of a mixture
of introduced and native freshwater, estuarine, and
euryhaline marine species (Table 1). The introduced
species come from a number of geographic areas,
while most of the native species have their centers
of abundance in either the rivers upstream or the
saltwater bays downstream from the estuary. There
are no really comparable estuaries on the Califor-
nia coast, although some of the much smaller and
more saline estuaries south of the Sacramento-San
Joaquin Estuary do have fish assemblages composed
in part of introduced species (Allen 1982).
We began in January 1979 systematic sampling
of the fishes in Suisun Marsh on a monthly basis.
Suisun Marsh was chosen as a study site because of
its central location on the estuary, its proximity to
the University of California, Davis campus, and the
availability of earlier data from sporadic sampling
by the California Department of Fish and Game The
data indicated that the fish fauna was typical of the
Manuscript accepted March 1985.
FISHERY BULLETIN: VOL. 84, NO. 1, 1986.
105
FISHERY BULLETIN: VOL. 84, NO. 1
Table 1— Fishes collected in Suisun Marsh, Solono County, CA, in decreasing order of
numerical abundance in our trawls. The principal environment of each species is coded as
follows: A = anadromous, E = estuarine, F = freshwater, M = marine.
Species
Numbers
Origin
Striped bass, Morone saxatilis
Splittail, Pogonichthys macrolepidotus
Threespine stickleback, Gasterosteus aculeatus
Tule perch, Hysterocarpus traski
Prickly sculpin, Cottus asper
Yellowfin goby, Acanthogobius flavimanus
Sacramento sucker, Catostomus occidentalis
Common carp, Cyprinus carpio
Threadfin shad, Dorosoma petenense
Staghorn sculpin, Leptocottus armatus
Starry flounder, Platichthys stellatus
Longfin smelt, Spirinchus thaleichthys
Delta smelt, Hypomesus transpacificus
American shad, Alosa spadissima
Sacramento squawfish, Ptychocheilus grandis
Chinook salmon, Oncorhynchus tshawytscha
Hitch, Lavinia exilicauda
Inland silverside, Menidia beryllina
Goldfish, Carassius auratus
Northern anchovy, Engraulis mordax
Sacramento blackfish, Orthodon microlepidotus
Pacific herring, Clupea harengeus
White catfish, Ictalurus catus
Bluegill, Lepomis macrochirus
Mosquitofish, Gambusia affinis
Black crappie, Pomoxis nigromaculatus
Bigscale logperch, Percina macrolepida
White sturgeon, Acipenser transmontanus
Fathead minnow, Pimephales promelas
Brown bullhead, Ictalurus nebulosus
Rainwater killifish, Lucania parva
Green sunfish, Lepomis cyanellus
Pacific sanddab, Citharichthys sordidus
Pacific lamprey, Lampetra tridentata
Surf smelt, Hypomesus pretiosus
Channel catfish, Ictalurus punctatus
Black bullhead, Ictalurus melas
Shiner perch, Cymatogaster aggregata
Golden shiner, Notemigonus crysoleucus
Warmouth, Lepomis gulosus
Rainbow trout, Salmo gairdneri
Longjaw mudsucker, Gillichthys mirabilis
24,154
E. North America (E)
11,250
Native (E)
9,956
Native (F-E)
7,693
Native (F-E)
4,639
Native (F-E)
1,786
Japan (E-M)
1,703
Native (F)
1,573
Asia (F)
1,088
E. North America (E)
985
Native (M)
849
Native (M)
650
Native (E)
450
Native (E)
218
E. North America (A)
140
Native (F)
96
Native (A)
56
Native (F)
50
E. North America (F-E)
45
Asia (F)
34
Native (M)
25
Native (F)
24
Native (M)
23
E. North America (F)
16
E. North America (F)
15
E. North America (F)
14
E. North America (F)
10
Texas (F)
10
Native (E)
9
E. North America (F)
6
E. North America (F)
5
E. North America (E)
4
E. North America (F)
4
Native (M)
4
Native (A)
3
Native (M)
3
E. North America (F)
3
E. North America (F)
3
Native (M)
3
E. North America (F)
1
E. North America (F)
1
Native (A)
1
Native (M)
freshwater dominated portions of the estuary. The
marsh is also of considerable interest because it is
the largest brackish-water marsh in California. It is
managed primarily as a wintering area for migratory
waterfowl, but its importance as a nursery area for
striped bass, salmon, and other fishes is being in-
creasingly recognized (Baracco 1980). The purpose
of this paper is to analyze the distribution and abun-
dance of the fishes of the marsh in relation to each
other, major environmental factors, and major
crustacean species, during a 54-mo period.
STUDY AREA
Suisun Marsh is a large (ca 34,000 ha) tidal marsh
located just downstream of the confluence of the
Sacramento and San Joaquin rivers (Fig. 1). About
11,000 ha of the marsh consist of sloughs that are
influenced by tidal action. The remainder consists
of diked wetlands managed to attract wintering
waterfowl (Baracco 1980) and for pasturage The
sloughs are shallow (most are <2 m deep) and may
fluctuate in depth as much as 1 m during extreme
tides. Salinities have ranged from 0 to nearly 17 ppt
in recent years, with the highest salinities occurring
in late summer of drought years and the lowest
salinities occurring annually in winter and spring
when river outflows are highest (Baracco 1980).
Because increased upstream diversion of water is
threatening water quality in the marsh, major
modifications to the water distribution system within
the marsh are being made to ensure that salinites
do not become too high for production of the plants
that attract waterfowl.
106
MOYLE ET AL.: NONCOEVOLVED ASSEMBLAGE OF ESTUARINE FISHES
Suisun City*
Pey tonia
Study
Area
Figure 1.— Locations of sample sites (*) in Suisun Marsh, Sacramento-San Joaquin Estuary, CA.
During this study, two major habitat types were
sampled: 1) small dead-end sloughs that were 7-10
m wide and 1-2 m deep and 2) Suisun Slough, which
connected all the dead-end sloughs and was 100-150
m wide and 2-4 m deep. A third habitat, Montezuma
Slough, was also sampled, but the data were not used
here because our methods did not sample it ade-
quately. This slough is deep (3-4 m), wide, and
riverlike; it is the marsh's main source of freshwater.
METHODS
Sampling was conducted monthly at seven loca-
tions throughout the marsh (Fig. 1), from January
1979 through June 1983, with the exception of
December 1979 and October 1980. Four of the loca-
tions were in dead-end sloughs (Peytonia, Boynton,
Mallard, and Goodyear), one was a small slough open
at both ends (Cutoff), and two were in Suisun Slough.
Sampling was conducted biweekly from January
1980 through June 1981, but the samples for each
month were lumped together for analysis, as the
samples within months were comparable All samples
were taken during the day, as 24-h studies conducted
in April 1979 and 1980 did not exhibit any signifi-
cant differences between day and night samples.
The principal means of sampling was a four-seam
otter trawl with a 1 x 2.5 m opening, a length of
5.3 m, and mesh sizes that tapered down to 6 mm
stretch in the bag. At each location, the trawl was
towed for either 5 min (small sloughs) or 10 min
(Suisun Slough) at about 4 km/h. The longer periods
were necessary in large sloughs because of the small
catches that prevailed there Each location was sam-
pled at least twice on each date This method of
sampling was biased because large fishes probably
avoided the trawl, and fishes that favor the emergent
vegetation were undersampled, as were fishes in the
upper part of the water column (Kjelson and Colby
1977). However, these problems were minimized by
the narrowness and shallowness of most of the
sampling sites; in any case such biases were consis-
107
FISHERY BULLETIN: VOL. 84, NO. 1
tent across the course of this study, so that com-
parisons should be unaffected. In addition, two loca-
tions on the marsh were sampled with a 10 x 1 m,
6 mm mesh, seine, on an irregular basis. An effort
was made to seine every month but it was often not
possible, as the sites were difficult to seine at ex-
treme high or low tides.
Fishes from each trawl were placed in washtubs
of water to minimize mortality and then identified,
measured to the nearest millimeter (standard
length), and returned to the water as quickly as
possible If more than 100 fish of any one size class
of a species were captured, only the first 100 were
measured; the rest were counted. Early in the study,
samples of all fishes were weighed (wet weight, in
gram), and a length/weight relationship developed
for each species. This was later used to estimate the
biomass of fish in each trawl. The shrimps Crangon
franciscorum and Palaemon macrodactylus in each
trawl were also counted. For the oppossum shrimp,
Neomysis mercedis, an index of abundance was used,
based on a l-to-5 scale, where "1" represented <3
individuals; "2", 3-50 shrimp; "3", 50-200, "4",
200-500, and "5", >500. The index was necessary
because most N. mercedis probably passed through
the net due to their small size (3-5 mm). Neverthe-
less, they were present seasonally in most hauls, at
times in enormous numbers.
At each location, salinity and temperature were
taken with a YSI S-C-T meter and transparency was
measured with a Secchi disk. Tidal height was deter-
mined from a tide tabla An index of monthly fresh-
water outflow from the combined Sacramento and
San Joaquin Rivers at Chipps Island was obtained
from the California Department of Water Resources
(unpubl. data).
For analysis, all the data were summarized by site
and month. A Spearman rank correlation analysis
using data ranked by month (N = 52) was used for
the initial analysis because many of the variables did
not conform to a normal distribution. Because no
single transformation could be applied to all the
variables, nonparametric statistics were used as the
most conservative method. We used 13 variables for
the analysis (Table 2). In addition, rank abundance
(by numbers) by month for the following species
categories was used: 1) total striped bass, 2) year-
ling and older striped bass, 3) young-of-year striped
bass, 4) total splittail, 5) yearling and older split-
tail, 6) young-of-year splittail, 7) total tule perch,
8) tule perch adults, 9) tule perch young-of-
year, 10) total prickly sculpin, 1 1) yearling and older
prickly sculpin, 12) prickly sculpin young-of-
year, 13) carp, 14) longfin smelt, 15) delta
smelt, 16) staghorn sculpin, 17) starry
flounder, 18) threadfin shad, 19) Sacramento
sucker, 20) yellowfin goby, and 21) threespine
stickleback. Because only minor differences were
found among the correlations associated with adult
and juvenile striped bass, tule perch, splittail, and
prickly sculpin, only the results for the totals for
these species will be presented.
Analyses were also run using the data from each
trawl separately. Species were analyzed using both
numbers and grams. Because these data were all of
species abundances, a log-normal transformation
was used to normalize them. The results were similar
in most respects to the analyses using ranks so are
not presented here However, because we were uncer-
tain as to the validity of using ranked data for prin-
cipal components analysis (PCA), we based our
discussion on cautious inspection of the correlation
matrix as generated. A principal components
analysis was run using the correlation matrix (Dix-
on and Brown 1977) of 1„ numbers of fish per trawl
(N = 1,238), to produce groups of species that
presumably were responding to the environment in
the same general ways.
Table 2. — Environmental variables used in the correlation analyses.
Variable
Units
Notes
Month series
1-54
January 1979 to June 1983
Water year
1-5
Begins in October of each
year
Salinity
ppt
Temperature
°C
Secchi depth
cm
Neomysis mercedis
1-5 index
abundance
Mean monthly
0-11 index
California Department of
outflow
Water Resources
Crangon
franciscorum
No./trawl
Palaemon
macrodacytlus
No./trawl
Fish species
No./trawl
Total fish numbers
No./trawl
Total fish biomass
Biomass/
trawl
Wet weight
Species diversity
Index
Shannon-Weiner (H)
RESULTS
Environmental Variables
Salinity and temperature were negatively corre-
lated with river outflows (Table 3, Fig. 2). Salinity
had a strong (P < 0.01) positive correlation only with
Secchi depth. River outflows generally peaked in
February, March, or April, as the result of run-off
from melting snow in the Sierra Nevada. Lowest
108
MOYLE ET AL.: NONCOEVOLVED ASSEMBLAGE OF ESTUARINE FISHES
Table 3. — Spearman rank correlation coefficients between fish species ranked by month by numbers and other variables
ranked by month. Underlined values are significant at P > 0.05.
CO
CO
CO
sz
o
3
CO
o
O
O)
c
Q.
3
O
CO
o
CD
CD
E
■o
CO
sz
CO
c
Q.
3
U
CO
CD
■o
c
3
n
o
ai
C
CO
E
c
o
-o
:=
CD
E
U—
CO
c
•D
o
a>
a.
s
a.
a>
CD
U
o
a.
o
o
£
c
CO
CD
SZ
>>
k_
^-.
a.
CO
CO
fc_
^
CD
o
sz
CO
CO
£
CO
¥
O
Q.
CO
a
_l
1-
CO
CO
Month series
-0.42
-0.72
-0.51
-0.38
-0.53
-0.58
0.16
-0.10
-0.29
-0.09
-0.26
-0.15
-0.21
Temperature
0.54
0.28
0.08
0.21
0.49
0.49
0.41
-0.33
-0.41
-0.28
-0.55
-0.03
0.01
Salinity
0.62
0.24
0.53
0.14
0.43
0.38
-0.36
-0.14
0.18
0.17
0.24
0.13
-0.06
Secchi depth
0.09
-0.09
0.29
-0.18
-0.08
-0.04
-0.54
-0.09
0.33
0.31
0.52
0.06
-0.28
Outflow
-0.74
-0.36
-0.49
-0.27
-0.62
-0.44
0.06
0.04
0.07
-0.12
0.16
-0.06
0.14
Neomysis
mercedis
-0.42
-0.02
-0.24
0.09
-0.45
-0.05
0.28
0.23
0.07
-0.25
-0.10
0.07
0.08
Crangon
franciscorum
0.27
-0.01
0.05
0.06
0.46
-0.18
-0.03
-0.10
0.01
-0.59
-0.15
0.29
-0.23
Palaemon
macrodactylus
0.43
-0.10
0.06
-0.10
0.34
0.20
0.16
-0.18
-0.30
-0.21
-0.32
0.14
0.23
No./trawl
0.67
0.64
0.72
0.53
0.46
0.45
0.07
0.21
0.16
-0.07
0.06
-0.18
-0.10
g/trawl
0.39
0.71
0.53
0.57
0.39
0.81
-0.06
-0.13
0.04
-0.24
0.13
0.04
0.04
Species/trawl
0.42
0.74
0.48
0.56
0.60
0.52
0.24
0.10
0.21
0.15
0.00
0.21
0.43
Diversity (H)
-0.10
0.45
0.23
0.45
0.28
0.35
0.31
0.21
0.26
0.09
0.12
0.36
0.43
flows occurred from August through October. Sali-
nity, temperature, and Secchi depth were generally
lowest (0-1 ppt, 8°-ll°C, and 17-18 cm, respective-
ly) when outflows were highest, and highest (4-9 ppt,
19°-23°C, and 25-40 cm, respectively when outflows
were lowest. There is, however, considerable year-
to-year variation in these cycles. When outflows were
comparatively low (1979, 1981), salinities, temper-
atures, and turbidities peaked at higher levels than
they did in high outflow years. Because 1982 and
1983 were exceptionally wet years, virtual freshwater
conditions prevailed throughout both years.
Invertebrates
Neomysis mercedis became very abundant in the
marsh from April to June, but the population de-
clined rapidly through the summer, reaching a low
in October (Fig. 2). This pattern fits with previous
studies of this species, which showed that its popula-
tions generally followed the mixing zone up and
down the estuary and were reduced at temperatures
higher then 22°C and salinities >7 ppt (Orsi and
Knutson 1979). In this study, N. mercedis abundance
showed a significant positive correlation with out-
flows and significant negative correlations with tem-
perature, salinity, and turbidity (Table 4). It also
showed a significant negative correlation (Table 3)
with two of its major predators in the marsh, striped
bass and yellowfin goby (Herbold 19854).
Palaemon macrodactylus and Crangon francis-
corum also showed seasonal patterns of abundance
(Sigfreid 1980), but the patterns were much less
marked than those of N. mercedis. Palaemon macro-
dactylus were most abundant during July through
October and least abundant during January and
February, while C. franciscorum were most abundant
in November and December and least abundant in
January through March. Palaemon macrodactylus
abundance therefore showed strong positive corre-
lation with temperature and salinity and a negative
correlation with outflows. Crangon franciscorum
abundance was also negatively correlated with
outflows, but had a positive correlation only with
salinity.
Fishes
A total of 42 species, represented by about 67,000
individuals, were collected in the 1,238 trawl hauls
made during the study. The four measures of overall
fish abundance and diversity showed negative cor-
relations with month series and with years, in-
dicating a general decline through the study period
(Table 4, Fig. 3). Numbers, biomass, and number of
species had positive correlations with temperature
and/or salinity and negative correlations with out-
"Herbold, B. 1985. Resource partitioning within a non-co-
evolved assemblage of fishes. Unpubl. Ph.D. Thesis, Univ. Califor-
nia, Davis.
109
FISHERY BULLETIN: VOL. 84, NO. 1
DELTA OUTFLOW INDEX
SALINITY
TEMPERATURE
UATER TRANSPARENCY
1979
Figure 2.— Trends in abiotic factors and Neomysis mercedis abun-
dance within Suisun Marsh. Temperature is in °C. Average outflow
in 10,000 cubic feet per second of the Sacramento River was
calculated by the California Department of Water Resources. Salini-
ty is given in parts per thousand. Neomysis mercedis abundance
rankings are described in text.
20-
1979
flow, indicating that catches were highest in late sum-
mer and lowest in early spring. However, when the
patterns of occurrence of the 12 most abundant
species were examined, three groups appeared: resi-
dent species, winter seasonals, and spring/summer
seasonals.
The "resident species" included the native split-
tail, tule perch, Sacramento sucker, prickly sculpin,
and threespine stickleback as well as the introduced
striped bass, carp, and yellowfin goby. Two additional
species, native white sturgeon and introduced
American shad, probably also belonged in this
category, as they were caught at all times of the year
but too infrequently to draw any firm conclusions.
Splittail, striped bass, tule perch, Sacramento sucker,
carp, and yellowfin goby had similar patterns of
abundance (Figs. 4, 5) and were correlated (P < 0.05)
with each other and with total biomass, numbers,
and species (Tables 3, 4). All six species usually
became more abundant in our catches as the sum-
110
MOYLE ET AL.: NONCOEVOLVED ASSEMBLAGE OF ESTUARINE FISHES
Table 4.— Spearman rank correlation among species ranked by month (lower matrix) by numbers and among environmental and other
variables ranked by month (upper matrix). Underlined values are significant at P > 0.05.
1
8
10
11
12
13. Striped bass
14. Splittail
15 Tule perch
16. Sacramento sucker
17. Yellowfin goby
18. Carp
19. Prickly sculpin
20. Stickleback
21. Delta smelt
22. Longfin smelt
23. Threadfin shad
24. Staghorn sculpin
25. Starry flounder
0.19
0.68
0.46
-0.14
-0.41
-0.11
-0.07
-0.17
-0.24
-0.09
0.15 -
0.50
0.44 0.38
0.51
0.58
0.53
0.13
■0.09
0.08
•0.01
■0.02
■0.13
0.30
0.54
0.27
0.54
0.32
0.38
•0.13
0.05
0.21
0.09
0.38
0.05
0.03
■0.10
0.19
0.46
0.22
0.46
0.34
0.07
0.03
0.12
0.00
0.06
0.30
0.43
0.14
-0.04
-0.04
-0.51
-0.79
-0.80
0.62
-0.29
0.19
0.44
0.33
0.30
0.37
0.78
-0.55
0.42
0.32
0.48
0.37
0.39
0.13
-0.43
0.04
-0.24
0.01
0.01
-0.11
0.51
-0.52
-0.41
-0.58
-0.34
-0.51
0.35
-0.56
-0.32
-0.14
-0.03
-0.10
0.06
0.11
0.34
0.09
-0.19
0.25
0.22
-0.17
0.09
0.12
0.04
0.15
0.05
-0.15
-0.15
0.40
0.55
0.56
0.21
-0.38
-0.15
-0.04
0.43
0.69
0.24
-0.11
-0.47
0.42
0.36
0.21
0.06
-0.02
0.20
0.18
0.17
0.30
0.01
0.18
-0.14
0.25
0.22
0.10
0.37
0.00
-0.64
0.05
0.07
-0.19
-0.06
0.16
0.01
-0.05
-0.08
0.51
0.74
0.07
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
Month series
Temperature
Salinity
Secchi depth
Outflow
Neomysis
Crangon
Palaemon
Numbers/
trawl
Grams/trawl
Species/trawl
Diversity (H)
13
14
15
16
17
18
19
20
21
22
23
24
1O0O
500
MEAN BI0MASS PER TRAUL
MEAN NUMBER OF FISH PER TRAWL
I 979
I 98 1
I 982
I 983
Figure 3.— Trends in mean numbers and grams of fish per trawl.
mer progressed although the two introduced species,
striped bass and yellowfin goby, tended to peak later
than the other species. Consequently, they all showed
significant (P < 0.05) negative correlations with
outflow. All except Sacramento sucker and tule perch
had significant positive correlations with salinity and
temperature. There was a general decline in fish
abundance throughout the 5-yr period. This was
reflected in that four of the six species showed a
positive correlation with species diversity, and all had
a negative correlation with month series.
Prickly sculpin seemed to peak in abundance
earlier in the year than the first six species (Fig. 4)
but the pattern was obscured by the considerable
year-to-year variation in abundance of young-of-year
fish. Adults were resident in the marsh but appeared
in the trawls on an irregular basis because of their
tendency to hide under logs and other objects (Moyle
1976). Overall, prickly sculpin had negative corre-
lations with salinity and Secchi depth, but positive
correlations with temperature, N. mercedis abun-
dance, and species diversity (Table 3). Threespine
stickleback abundance had a negative correlation
only with temperature, presumably because their
reproductive behavior obscured our ability to catch
them. They were most abundant in the trawls in
February through May, and the catch consisted
primarily of gravid females and schools of young-
of-year fish. The males were apparently defending
their nesting territories in emergent vegetation. By
late summer sticklebacks were rare in the trawls but
could be taken in seine hauls made through weedy
areas.
The "winter seasonals" were three plankton-
Ill
10t
PRICKLY SCULPIN
SACRAMENTO SUCKER
I 982
I 983
FISHERY BULLETIN: VOL. 84, NO. 1
TULE PERCH
1988
Figure 4— Capture rates of native resident species within Suisun Marsh. Mean catch per effort is described as percent of the total catch
for each species.
feeding species, delta smelt (native), longfin smelt
(native), and threadfin shad (introduced). All three
species tended to be most abundant in November
through January, although the pattern was not
always consistent (Fig. 6). Threadfin shad were the
most erratic of the three species in abundance; they
were especially abundant in the summer of 1981.
Longfin smelt were largely absent from our samples
in 1979 and 1981. Delta smelt abundance was
positively correlated (P < 0.05) with that of the other
two species, although the correlation between long-
fin smelt and threadfin shad was not significant. All
three species had negative correlations with tem-
perature, and positive correlations with Secchi
depth.
The "spring/summer seasonals" were staghorn
sculpin and starry flounder, both euryhaline marine
species that were represented mainly by young-of-
year. Their patterns of abundance were not consis-
tent (Fig. 6) and the peaks occurred anytime from
March through September. Consequently, staghorn
sculpin did not show any significant correlations with
the environmental variables, although starry
flounder did show negative correlation with Secchi
depth. Both species had a positive correlation with
species diversity, presumably because they were rare
in our samples during the last 2 years when the
marsh was dominated by freshwater.
In addition to the 12 species that appeared regular-
ly in our trawls, there were a number of other species
of potential importance to the fish community that
were either not sampled adequately by the trawl or
were absent because of the effects of the 1976-77
drought. Five species that were not sampled ade-
quately were inland silverside, chinook salmon,
Sacramento squawfish, mosquitofish, and rainwater
killifish. The silversides were abundant year around
in the shallow, sandy or weedy areas found in some
sloughs. Silversides appeared in seine hauls in 20 of
the 22 mo in which seining was done; they were
generally the most abundant fish in these hauls.
Juvenile chinook salmon and squawfish were com-
112
MOYLE ET AL.: NONCOEVOLVED ASSEMBLAGE OF ESTUARINE FISHES
mon in the marsh in February, March, and April
(times of high outflows) and were taken mainly in
seines. The tendency of the salmon to remain close
to the banks and vegetation and to get sucked into
YELLOWFIN goby
CARP
STRIPED BASS
diversions of marsh water consequently has led to
the screening of one major diversion in the marsh.
Squawfish were abundant in the Sacramento River
and juveniles are known to disperse widely during
high flows (Smith 1982). Mosquitofish and rainwater
killifish were present in ponds adjacent to the
sloughs, along with silversides and sticklebacks; mos-
quitofish were planted in some areas for mosquito
control.
Principal Components' Analysis
The PCA using the numbers per trawl matrix
resulted in four components that explained 47% of
the variance in the matrix (Table 5). The first com-
ponent loaded most heavily on tule perch, Sacra-
mento sucker, and splittail, native resident species
most abundant in dead-end sloughs, and to a lesser
extent on carp and threadfin shad, introduced
species common in such sloughs. The second com-
ponent loaded heavily on striped bass, yellowfin goby,
and carp, three introduced species resident through-
out the marsh but most frequently captured in the
main sloughs; all reached peaks of abundance in late
summer. The third component loaded most heavily
on prickly and staghorn sculpins, two benthic species
that peaked in abundance during the summer
months but were relatively scarce during the last 2
Table 5.— Loadings (rotated) of major fish species on four com-
ponents produced by a principal components analysis of numbers
of fish per trawl (n = 1,238). Values over 0.500 are underlined.
Figure 5.— Capture rates of introduced species within Suisun
Marsh. Mean catch per effort is described as percent of the total
catch for each species.
Compo-
Compo-
Compo-
Compo-
nent
nent
nent
nent
1
2
3
4
Splittail adults
0.487
0.300
-0.024
-0.149
Splittail juveniles
0.549
0.100
0.318
0.149
Striped bass adults
0.058
0.701
0.078
- 0.073
Striped bass juveniles
0.183
0.631
-0.157
0.046
Longfin smelt
-0.124
0.029
-0.032
0.747
Delta smelt
0.022
-0.061
-0.027
0.734
Threadfin shad
0.447
-0.286
-0.121
0.319
Common carp
0.403
0.403
0.166
-0.084
Yellowfin goby
-0.011
0.660
0.023
0.016
Tule perch adults
0.827
0.049
0.085
-0.102
Tule perch juveniles
0.833
-0.036
- 0.045
-0.017
Sculpin adults
0.254
-0.038
0.377
-0.263
Sculpin juveniles
0.090
0.043
0.780
- 0.077
Starry flounder
0.117
0.256
0.107
-0.030
Staghorn sculpin
0.043
0.047
0.727
0.118
Sacramento sucker
0.637
0.197
0.341
0.102
Threespine stickleback
0.039
-0.296
0.486
-0.147
Eigenvalue
2.826
1.874
1.829
1.391
Cumulative proportion
of variance explained
0.200
0.304
0.396
0.472
113
THREADFIN SHAD
DELTA SMELT
1979
1980
1982
Figure 6— Capture rates of seasonal species within Suisun Marsh.
Mean catch per effort for each month described as percent of total
for each species.
FISHERY BULLETIN: VOL. 84, NO. 1
LONGFIN SMELT
STAGHORN SCULPIN
1979
years of the study. A similar pattern was shown by
threespine stickleback, which also had a relatively
large positive loading on this component. The fourth
component loaded heavily on delta and longfin smelt,
and to a lesser extent on threadfin shad. This is the
winter seasonal group identified in the previous
analysis.
DISCUSSION
During the 5-yr study period, the fish assemblage
of Suisun Marsh had the following character-
istics:
1. There was a strong seasonal pattern of total fish
114
MOYLE ET AL.: NONCOEVOLVED ASSEMBLAGE OF ESTUARINE FISHES
abundance with numbers and biomass lowest in
winter and spring and highest in late summer. Fishes
were least abundant when river outflows were
highest and most abundant when salinities and tem-
peratures were highest.
2. There was an overall decline in fish abundance
and species diversity through the study period.
3. Of the 21 species that occurred in the marsh on
a regular basis, 14 were residents, 4 were winter
seasonals, and 3 were spring/summer seasonals.
Another 21 species occurred sporadically, in small
numbers. These were mainly marine and freshwater
species that presumably could become established
in the marsh if environmental conditions changed
significantly.
4. The abundant resident species fell into two
groups, one made up of native species that concen-
trated in the small dead-end sloughs and the other
a mixture of introduced and native species that were
widely distributed in the marsh, but most abundant
in the larger sloughs.
5. The structure of the fish assemblage (i.e., the
pattern of distribution and abundance) was fairly
consistent over the 54-mo period.
The seasonal pattern of fish abundance was due
to a number of factors, most importantly 1) varia-
tion in sampling efficiency, 2) influxes of young-of-
year fish, 3) favorable environmental conditions for
most fish species in late summer, and 4) abundance
of Neomysis mercedis. When outflows were high,
water levels in the marsh were high and showed lit-
tle tidal fluctuation. Therefore trawling was less ef-
ficient because there was more water and more
flooded vegetation available as cover for fish. How-
ever, even under these conditions most of the sam-
pling areas were rarely more than 2 m deep, so our
trawl covered at least half the water column, and
large catches were common, especially early in the
study. Therefore, variation in sampling efficiency
may have exaggerated the peaks and valleys of the
catch curves (Figs. 4, 5) but was unlikely to obscure
the general trends in abundance Probably the most
important contributor to the seasonal patterns was
the increase in young-of-year striped bass, splittail,
prickly sculpin, and tule perch, in June through
August. These species (and others, to a lesser extent)
became vulnerable to our trawl at 30-40 mm SL, and
catches of several hundred individuals in a 5-min tow
were made on occasion. The rapid growth of these
species during summer (Daniels and Moyle 1983;
Herbold and Moyle, unpubl. data) indicated that en-
vironmental conditions, including warm tempera-
tures and moderate salinities, were favorable for
them and for other euryhaline species (ag., staghorn
sculpin, starry flounder). These same conditions also
favored N. mercedis, a small shrimp that is an im-
portant food item in summer diets of most of the
fishes (Herbold fn. 4). It is possible that the summer
peak in fish abundance may be due also in part to
fishes moving in to take advantage of an abundant
food resource The decline in N. mercedis abundance
in late summer may be related in part to fish preda-
tion, although it is presumably related mainly to
their seasonal movements within the entire estuary
(Orsi and Knutson 1979).
The overall decline in fish abundance over the
study period seemed to be due to two factors: varia-
tion in reproductive success of major species and the
fact that 1982 and 1983 were years of unusually high
precipitation and runoff, so freshwater conditions
prevailed throughout the summer months of both
years. Splittail showed an unusually strong year class
in 1978, which dominated the 1979, and, to a lesser
extent, 1980 samples (Daniels and Moyle 1983).
Catches of splittail in 1979 were typically 2-5 times
greater than in subsequent years. Striped bass, tule
perch, and carp also showed peaks of abundance in
1979 and had low abundances in 1982-83, with one
or two peaks of abundance in between. Except for
carp, the peaks were largely due to influxes of young-
of-year fish. The reason for the abundance of the
1978 year class of fish was presumably related to
1978 being a year of high, but not excessive, outflows.
Increased reproductive success during high outflow
years has been documented for striped bass (Stevens
1977), splittail (Daniels and Moyle 1983), American
shad, chinook salmon, and longfin smelt (Stevens and
Miller 1983). However, under extreme outflow con-
ditions (such as existed in 1982 and 1983), young-
of-year fish are apparently carried downstream to
areas below the marsh (San Francisco and San Pablo
Bay) where chances of survival may be less (Stevens
1977).
Drought also contributed to the variation in the
fish fauna. During 1976 and 1977, severe drought
reduced freshwater inflows to the marsh, resulting
in sustained high salinities. Freshwater fishes de-
clined dramatically during the drought period (Herr-
gesell et al. 1981) and the fishery for catfish (main-
ly white catfish and black bullhead) was greatly
reduced (Baracco 1980). The catfish populations did
not recover during the study period, but the regular
appearance of young-of-year white catfish in our
trawls in late 1983 indicated a recovery may be in
progress. Other freshwater fishes found in the marsh
(Table 1) showed no signs of increasing. Most were
represented in our samples by <10 individuals that
115
FISHERY BULLETIN: VOL. 84, NO. 1
had presumably been washed into the marsh from
freshwater habitats upstream. However, black crap-
pie and perhaps other centrarchids contributed to
the local fishery prior to the drought, mainly in the
upper ends of the larger sloughs, so a recovery can
be expected.
Despite the decline in freshwater fishes during the
drought, there was no corresponding major increase
in the abundance of euryhaline marine species
characteristic of nearby San Francisco Bay (Herr-
gesell et al. 1981). Marine species (such as northern
anchovy, Pacific herring, and shiner perch) general-
ly appeared in our samples in late summer when
salinities were highest, in parts of the marsh closest
to Suisun Bay.
Considering the annual and long-term variations
in fish abundances and the fact that the fish assem-
blage is made up of a mixture of native and intro-
duced species, the consistency of the assemblage
structure during the study is surprising. Coevolution
has obviously little role in an assemblage in which
the most abundant species (striped bass) entered in
1879 and other abundant species entered in the
1960's (yellowfin goby) and 1970's (inland silversides)
(Moyle 1976). The apparent consistency in structure
seemed to be the result of 1) two introduced species,
striped bass and carp, that were consistently abun-
dant in the marsh, 2) the group of native resident
fishes that was persistent in deadend sloughs, and
3) the native fishes that moved in and out of the
marsh on a seasonal basis.
This does not mean that the structure observed
during this study will persist indefinitely. A number
of changes in the fish fauna may already be occur-
ring. For example, the presence of young-of-year
white catfish in 1983 and 1984 may signify a shift
of the assemblage towards catfishes and centrar-
chids, such as existed before the 1976-77 drought.
Striped bass are presently in a long-term decline in
abundance, a trend which seems to be continuing
(Kelley et al. 1982). Past history indicates that new
introductions of fishes into the system are likely:
specifically, the white bass, Morone chrysops, has
recently become established in part of the San Joa-
quin drainage and may become a major new predator
in the Sacramento-San Joaquin Estuary if planned
eradication attempts fail (California Department of
Fish and Game unpubl. data). Furthermore, addi-
tional diversions of freshwater from the estuary are
planned (Herrgesell et al. 1981), and major modifica-
tions to the marsh channels are planned or under-
way (Baracco 1980), so the environment, especially
in the dead-end sloughs, may change significantly.
It is difficult to predict what the combined effects
of all these changes will be on the present fish
assemblage, but extinctions of both native and intro-
duced species in the estuary have occurred in the
past (Moyle 1976) and could occur again in the future
The structure of the fish assemblage of Suisun
Marsh is similar in may respects to the structure of
the fish assemblages of other large estuaries (e.g.,
Markle 1976; Meeter et al. 1979), despite the impor-
tance of recently introduced species and the stabi-
lizing influence humanity has had on the pattern and
amount of freshwater inflow (Kahrl 1978). In most
such estuaries, as in the Sacramento-San Joaquin,
the assemblages are dominated by juvenile fishes,
and most species have substantial populations out-
side the estuary. As in Suisun Marsh, the fish assem-
blages of such estuaries are made up of a relatively
small number of the species available in nearby
marine and freshwater environments. Presumably,
the species composition of an estuarine assemblage
is determined in large part by the ability of the
species to tolerate the particular set of environmen-
tal conditions that exist there Since these conditions
may change with short-term climatological changes,
the fish assemblages may change as well (Meeter et
al. 1979; Marais 1982). Thus coevolution is given lit-
tle chance to operate in estuarine systems in general.
In this context, it is not surprising that the fish
assemblage of the Suisun Marsh behaves ecologically
in a way similar to fish assemblages in most other
estuarine systems. Because resource partitioning is
commonly observed among estuarine fishes (Sheri-
dan and Livingston 1979; Whitfield 1980), competi-
tion may be an important process in determining the
structure of estuarine fish assemblages (Thorman
1982), a hypothesis we are currently investigating
in the Suisun Marsh.
ACKNOWLEDGMENTS
This project was supported by the California
Department of Water Resources (DWR) and by the
Agricultural Experiment Station, University of
California (Project No. 3930-H). It would not have
been possible without the support and encourage-
ment of Randall L. Brown, Central District, DWR.
Numerous volunteers assisted the sampling effort,
but especially Larry Brown, Sonia Cook, Bart
Daniel, Lynn Decker, Tim Ford, Bret Harvey, Ned
Knight, Tim Takagi, Bruce Vondracek, Eric Wikra-
manayake, and Wayne Wurtsbaugh. The manuscript
was reviewed in various drafts by Larry Brown, Beth
Goldowitz, Ned Knight, and Eric Wikramanayake.
The manuscript was "processed" by Donna
Raymond.
116
MOYLE ET AL.: NONCOEVOLVED ASSEMBLAGE OF ESTUARINE FISHES
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1980. Analysis of temporal changes in fish assemblages in
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1980. Seasonal abundance and distribution of Crangonfran-
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Zool. 115:83-170.
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1977. Striped bass (Morone saxatilis) year class strength in
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Manage 3:425-437.
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1982. Niche dynamics and resource partioning in a fish guild
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117
THE ROLE OF ESTUARINE AND OFFSHORE NURSERY AREAS FOR
YOUNG ENGLISH SOLE, PAROPHRYS VETULUS GIRARD,
OF OREGON
E. E. Krygier1 and W. G. Pearcy2
ABSTRACT
Our trawling studies confirm that age group 0 English sole are common in shallow waters along the open
coast as well as in estuaries of Oregon. Both areas appear to be important nursery areas for this species.
Metamorphosing English sole were recruited to Yaquina Bay over many months between November and
June during the 5 years studied. Seasonal trends in abundance of these transforming fish were rather
similar to both Yaquina Bay and open coastal stations. Transforming individuals, however, were found
earlier in the fall and later in the spring and summer along the open coast than in Yaquina Bay.
Based on catch curves, the densities (no. m"2) of juvenile English sole were much higher in Yaquina
Bay than along the open coast. Transforming sole (20-25 mm) were an exception. They were sometimes
most abundant at the open coast location. Increasing densities of 20-40 mm length fish in the Yaquina
Bay catches were accompanied by decreased catches of this size group at the open coast site This sug-
gests immigration of a broad size range of both transforming and fully transformed individuals into Yaquina
Bay.
English sole, Parophrys vetulus Girard 1854, is a ma-
jor component of the catches in the northeastern
Pacific trawl fishery, usually ranking second only to
Dover sole, Microstomas pacificus, in annual land-
ings off Oregon (Barss 19763; Demory et al. 19764).
It ranges from Baja California to Unimak Island in
western Alaska, with commercial quantities at
depths of 128 m or less (Hart 1973). Tagging studies
have revealed a series of relatively discrete stocks
of English sole off California, Oregon, Washington,
and British Columbia (Ketchen 1956; Forrester 1969;
Jow 1969; Pattie 1969; Barss 1976 fn. 3).
Spawning of English sole is protracted, usually ex-
tending from September through April, and is often
variable in seasonal intensity within and among
spawning seasons (Budd 1940; Ketchen 1956; Harry
1959; Jow 1969; Laroche and Richardson 1979).
Much of this variability among years may be related
to upwelling and bottom temperatures (Kruse and
Tyler 1983). Spawning concentrations of adult
English sole were found in the fall off the central
Oregon coast at depths of 70-110 m (Hewitt 1980).
'College of Oceanography, Oregon State University, Corvallis,
OR; present address: Alaska Trailers Association, 130 Seward
Street, Juneau, AK 99801.
2College of Oceanography, Oregon State University, Corvallis, OR
97731.
3Barss, W. H. 1976. The English sole Oreg. Dep. Fish Wildl.,
Inf. Rep. 76-1, 7 p.
4Demory, R. L., M. J. Hosie, N. Ten Eyck, and B. O. Forsberg.
1976. Marine resource surveys on the continental shelf off Oregon,
1971-74. Oreg. Dep. Fish Wildl., 49 p.
English sole are fecund, producing 327,600-
2,100,000 eggs, depending on the size of female (Ket-
chen 1947; Harry 1959). Eggs are pelagic and hatch
in about 4V2 d at 10° C (Alderdice and Forrester
1968). Larvae are often abundant during late winter
and early spring in coastal waters of Oregon (Rich-
ardson and Pearcy 1977; Mundy 1984). Larval abun-
dance may fluctuate greatly among years, possibly
due to annual differences in ocean conditions
(Laroche and Richardson 1979; Mundy 1984). The
pelagic phase lasts 8-10 wk (Ketchen 1956; Laroche
et al. 1982), and most individuals complete metamor-
phosis and acquire the morphology of benthic pleu-
ronectids at 20 mm SL and 120 d of age (Ahlstrom
and Moser 1975; Rosenberg and Laroche 1982).
While early larval stages are rarely found in estu-
aries (Misitano 1970; Pearcy and Myers 1974), trans-
forming larvae and early juvenile stages of English
sole are common in estuaries (Westrheim 1955;
Smith and Nitsos 1969; Olsen and Pratt 1973; Pearcy
and Myers 1974; Misitano 1976; Toole 1980; Bayer
1981) and shallow protected bays (Ketchen 1956;
Kendall 1966; Van Cleve and El-Sayed 1969). Young
English sole are known to utilize 13 estuaries along
the Oregon coast and were absent in only 3 small
estuaries surveyed along the southern Oregon coast.5
Villadolid (1927, as cited by Misitano 1970) captured
6Report of estuary surveys, July-August 1972. Fish Comm. Oreg.
Intern. Rep. GS-73-1, 14 p.
Manuscript accepted March 1985.
_119_
FISHERY BULLETIN: VOL. 84, NO. 1
0-age English sole in San Francisco Bay but not off
the coast.
Based on the incidence of a parasitic infection, ap-
parently acquired only in estuaries, and the absence
of 0-age English sole in Demory's (1971) surveys off
the northern Oregon-southern Washington coast,
Olsen and Pratt (1973) concluded that estuaries are
likely the exclusive nursery for English sole on the
Oregon coast. Laroche and Holton (1979), however,
captured 0-age English sole in shallow waters along
the open Oregon coast, indicating that estuaries may
not be the only nursery area for English sole off
Oregon.
The main objective of our study is to evaluate the
relative importance of estuarine and open coastal
nursery grounds for young English sole off Oregon.
METHODS AND MATERIALS
Bottom trawl collections provided most of the in-
formation on the distribution and abundance of
juvenile English sola Collections were made in Ya-
quina Bay and along the open coast outside the bay.
These were supplemented with extensive trawl col-
lections farther to the north and south along the
open coast and collections in other estuaries.
Fish were collected using a 1.52 m wide, 56 cm
high beam trawl (see Krygier and Horton 1975) from
the RV Paiute and from a 7.3 m dory. Additional col-
lections with a 2.72 m beam trawl (Carey and Heya-
moto 1972) were made on the RV Cayuse. To retain
small, settling fish, fine-mesh (1.5-3.5 mm stretch)
liners were used in the trawls. The 1.52 and 2.72 m
beam trawls were fitted with a 1.0 or 2.0 m circum-
ference wheel, respectively, and a revolution counter
to estimate the area sampled (Carey and Heyamoto
1972; Krygier and Horton 1975). Tows were made
at 0.7-1.0 m s_1. Tow duration was normally 5-10
min on the bottom in estuaries and 10-20 min along
the coast, usually at a 4:1 scope Most tows were dur-
ing daylight hours.
Collections for juvenile English sole were made in
five different study areas (Fig. 1, Table 1):
ESTUARINE
1) Yaquina Bay: 1.52 beam trawl collections were
made in lower Yaquina Bay from January 1970
through February 1972 by Krygier and Johnson (un-
publ. data) and Krygier and Horton (1975) and sup-
plemented by collections in 1977-79. Additionally, we
used collections made by Myers (1980) with a 100
m beach seine (11.0 mm stretch mesh in the inner
wing and bunt (Sims and Johnsen 1974)).
2) Other estuaries: The 1.52 m beam trawl was
towed from a 7.3 m dory in four estuaries north and
south of Yaquina Bay (Tillamook and Siletz Bays,
107.5 and 35.2 km to the north of Yaquina Bay and
Alsea Bay and Umpqua River estuary, 21.3 and 105.6
km to the south). Each estuary was divided into
seven equal-area portions from which we planned to
take three random trawl collections (2 of the 21
trawls in the Umpqua River estuary were not com-
pleted).
COASTAL
3) Moolack Beach: 1.52 m beam trawl collections
were made on a monthly or bimonthly basis in
shallow (3-31 m depth) nearshore waters in a 1.0
km2 area just north of Yaquina Head during 1977,
1978, and 1979. Moolack Beach is semiprotected by
headlands to the north and south and offshore by
a reef that rises from 15 m to 6 m.
4) Grid stations: Collections were taken with a
2.72 m beam trawl, approximately monthly, during
1978 at 1.9, 5.6, and 9.3 km (1, 3, and 5 nmi) offshore
along lat. 44°41.6'N, 44°36.6'N, and 44°31.6'N. Thir-
teen collections were also made in this area with the
1.52 m beam trawl.
Table 1.— Summary of collections used in this study.
Net
No.
Dates (sampling
Area
type
trawls
frequency)
Yaquina Bay
M.52 m
178
16 Jan. 70-25 Jan. 71
(weekly or biweekly);
17 Feb. 71-25 Feb. 72
(bimonthly)
21.52 m
26
26 Apr.-28 June 77 (bi-
monthly)
21.52 m
96
1 Dec. 77-14 Sept. 79
(monthly to bimonthly)
22.72 m
8
16 Nov. 77, 1 Feb. 78,
27 Nov. 78
beach
196
12 July 77-11 Nov. 78
seine
(various: daily,
biweekly, weekly,
bimonthly)
Moolack
1.52 m
16
28 Apr. 77-23 June 77
(bimonthly)
1.52 m
76
11 Jan. 78-24 Sept. 79
(bimonthly of monthly)
Grid
1.52 m
13
21 Apr. 77-27 June 77;
15 June 78-28 Sept.
78
2.72 m
106
17 Nov. 77-25 Oct. 78
(monthly)
North-South
1.52 m
40
2 June 77-13 June 77,
15 June 78-21 July 78
2.72 m
83
15 May 78, 27 June 78,
25 Oct. 78
Estuaries
1.52 m
82
8-12 May 78, 21 trawls
each in Tillamook,
Siletz and Alsea; 19
trawls in Umpqua
1Net liners 3.5 mm and cod end liner of 1.5 mm stretch mesh, 1970-72.
2Net liners 3.2 mm stretch mesh, 1977-79.
120
KRYGIER and PEARCY: NURSERY AREAS FOR YOUNG ENGLISH SOLE
44°
40'
44°
30'
^ COLUMBIA
-RIVER
-46c
TILLAMOOK
•^BAY
SILETZ BAY
-45c
Xyaquina bay
TTalsea bay
.kUMPQUA
• VF^ RIVER
'COOS BAY
44<
Figure 1.— Location of sampling stations in the North-South coastal survey (right) and at Moolack Beach, the grid stations I, II, III,
and within Yaquina Bay (left). In Yaquina Bay the numbers 1-4 indicate locations of stations for sampling in 1970-72, the solid dots loca-
tions in 1977-79, and the arrows indicate seine stations in 1977.
5) North-south coastal survey: 1.52 m beam trawl
collections were made from 111 km to the north (lat.
45°37.5'N) and 111 km to the south (lat. 45°36'N)
of Yaquina Bay at 9.3 km intervals (Fig. 1) at depths
of 9-18 m in June 1977 and May-October 1978.
Most samples were preserved in 5% Formalin6 and
seawater. In the laboratory fish were identified,
sorted, and standard length (SL) measured to the
6Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
nearest millimeter. Nearly all English sole captured
in Yaquina Bay were 150 mm SL or less and included
0- and I-age fish (Rosenberg 1982). We call these
fishes "juveniles" in this paper.
RESULTS
Variability of Catches
The variability of the number of juvenile English
sole caught per m2 in repeated trawls within the
same area was low. Coefficients of dispersion (s2/x)
121
FISHERY BULLETIN: VOL. 84, NO. 1
were usually <0.1, indicating uniform distributions
within the small areas (10-100 m2) and short inter-
vals of time (1-2 h) sampled. Variability was higher
and coefficients of dispersion sometimes differed sig-
nificantly (chi-square, <0.05) from a random (Pois-
son) distribution among different sampling depths
at the same date (s2fx = 0.36-1.65) and among dif-
ferent sampling dates within a single depth at Moo-
lack Beach (s2fx = 1.2-2.31). Coefficients of disper-
sion did not significantly differ from randomness
either among the grid stations for the same sam-
pling dates (s2/x = 0.87-1.82) or among different
sampling dates at the same station (0.94-1.97). In
general, at the scale of sampling we used, juvenile
English sole had even, nonpatchy distributions.
Gear Comparisons
Tb compare the relative efficiencies of the 1.52 m
beam trawl from the Paiute and the 2.72 m beam
trawl from the Cayuse, 14 pairs of trials were made
at the same time, while the vessels trawled on par-
allel courses within 30 m of each other. No signifi-
cant differences (P > 0.05; Mann-Whitney "U" tests,
Tate and Clelland 1957) were found in the catch/m2
of juvenile English sole <150 mm for any paired
trawl comparison.
No significant differences were found in length-
frequency distributions of P. vetulus captured in 10
of the 14 comparisons [Kolmogorov-Smirnov (K-S)
test, late and Clelland 1957]. In the four pairs of
tows that were significantly different (October 1978)
the 2.72 m trawl caught more small (~20 mm SL)
English sole per m2 than the 1.52 m trawl, while
both trawls caught similar proportions in the 46-100
mm size range
Comparisons were made between the sizes of
English sole in beach seine samples and midchan-
nel trawl samples in Yaquina Bay on six different
dates. Differences were significant (K-S test; P <
0.05) for all comparisons because the beam trawl
caught a much broader size range of fish, including
individuals >40 mm which were rare or absent in the
beach seine catches.
Trends in Catches and
Sizes of Fish
Significant (H-test, P < 0.05) differences in
catches/m2 at different depths at Moolack Beach
and the grid stations show that in general the abun-
dance of juvenile English sole in offshore waters was
greatest in shallow water and decreased with in-
creasing depth. Average catches/103m2 (+1 stan-
dard deviation) of English sole <150 mm were 16
(±20), 61 (±14), 43 (±75), and 10 (±12) at the 9, 9-17,
12-18, and 18-31 m stations off Moolack Beach, com-
pared with only 3 (±3) and 2 (±3) at the 40 and 64
m 1-3 and 1-5 grid stations at about the same latitude
Newly transformed, benthic English sole (<24 mm)
were found at all depths sampled in the Moolack
Beach area, but the highest proportion of these
recently metamorphosed fish was found at depths
<18 m. Within the depth zones sampled the propor-
tion of small English sole <30 mm decreased with
depth and fish >150 mm were only captured at
depths deeper than 18 m (Fig. 2).
Juvenile English sole <150 mm were found along
the entire 222 km coast sampled (Fig. 3). They were
usually moderately abundant (^0.01 m2) between
Siletz Bay and Alsea Bay, and near the Umpqua
River and Tillamook Bay. Average catches, however,
were higher off Moolack Beach than any other area,
averaging 0.21 juvenile English sole/m2, an order of
magnitude greater than most other offshore areas
or the grid stations. Moolack Beach was apparently
a region of the open coast with exceptionally high
densities of English sole
Juvenile English sole were generally most abun-
dant at the shallowest depths in these collections,
corroborating more intense sampling off Moolack
Beach and at the grid stations (Fig. 3). Average
catches at depths of 18 m and 36 m decreased about
an order of magnitude between May (0.026/m2; SD
0.049) and October (0.003/m2; SD 0.003).
Variations in Abundance of
Settling Fish
In our samples, metamorphosis or transformation,
as indicated by migration of the left eye and by body
pigmentation, occurred between 14-26 mm. Most fish
had completed metamorphosis by 23 mm. In Yaquina
Bay, the metamorphosing individuals first appeared
in November of 1971 and 1978 (the 1972 and 1979
year classes) and in January of 1971 and 1978 (1971
and 1978 year classes) (Fig. 4). (In this paper we
designate year classes by the year that most juveniles
settled to the bottom; eg., products of spawning dur-
ing the fall 1978-winter 1979 are called the 1979 year
class.) Metamorphosing fish were present in Yaquina
Bay until June (1970, 1978, 1979) or July (1971), but
none was found after July during the four summer
periods sampled.
Maximum densities of these metamorphosing fish
were observed between March and May in 1970,
1971, and 1978, but between November and January
in 1978-79. Densities were variable Low densities
122
KRYGIER and PEARCY: NURSERY AREAS FOR YOUNG ENGLISH SOLE
_ MOOLACK BEACH STATIONS
<4m
■ . ■ ■■
r-
_■ ,11 ■
m 30r GRID STATIONS
§ 20-
IOh
0
30-
20-
10
0
30r
20
10
0
18m
_a ■»■■! m ■ r « ■ ■■ ■■ u_
40 m
■■■■
64 m
20
40 60
80
_«» — «-_e
r*^
100 120
LENGTH (mm)
^--fh
,4
T-SJ-
^" ^M-ff
140 160 >I70
Figure 2— Length-frequency distributions of juvenile English sole caught at different depths at the Moolack Beach (above) and grid
stations (below).
123
FISHERY BULLETIN: VOL. 84, NO. 1
:S/LETZ
BAY
°&fik. TILLAMOOK
eiS.BAY
YAQUINA
BAY
ALSEA
BAY
-45<
O/m^
O.OOI-0.003
0.004 - 0.009
> 0.010
' UMPOUA R.
R
44<
Figure 3— Catches of juvenile English sole (<150 mm) along the open coast during May, June, July, and October 1978. Hatched areas
indicate untrawlable grounds due to crab pots or rocky outcrops.
124
KRYGIER and PEARCY: NURSERY AREAS FOR YOUNG ENGLISH SOLE
0 ' N ■ D
Figure 4— Abundances of settling (<20 mm SL) English sole in Yaquina Bay for 1970-79 (solid line) and Moolack Beach for 1970-79
(dashed line).
occurred during March 1970, January and February
1971, 1972, and April-May 1979, suggesting sea-
sonal variation in spawning activity of adults (see
Kruse and Tyler 1983), mortality of planktonic
stages, or movement of young into or out of the
estuary.
Seasonal trends in catches of transforming
English sole in Yaquina Bay and at Moolack Beach
for 1978 and 1979 shows that fish <20 mm were
found 1-2 mo earlier at Moolack Beach than in Ya-
quina Bay during both years (Fig. 4). Moreover,
tinued at Moolack Beach from 18 to 50 d after
settling fish were no longer found within the estuary.
Tb our surprise, similar densities of settling fish were
caught in both areas. Seasonal trends were some-
times similar, suggesting a common source of lar-
vae and similar processes affecting variations in
recruitment of metamorphosing fish at both the
open-coast and estuarine areas.
The catches/m2 of age groups 0 and I English
sole (20-150 mm) are plotted as catch curves for each
5 mm size group (Fig. 5) where
no. m2 =
2 of the number of individuals in each 5 mm size group
total area sampled in m2 during sampling periods
in which year class occurred
recruitment of the 1978 and 1979 year classes con- Trends in the abundance of English sole were often
125
FISHERY BULLETIN: VOL. 84, NO. 1
1.0
00
£
b
bfe*S£^^
o.i-
0.01
0.001
25
"Qi.
Y^
\ .A
1971
\/970 V. /£
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-<K
1972
50
75 100
LENGTH (mm)
oj
E
6
0.01 -
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YAQUINA
BAY
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^ BEACH
\
\
\
\
)>--o-_
IBEACH
i SEINE
i^z:
••A
1
L
B
1977
25
50
125
150
75 100
LENGTH (mm)
Figure 5— Abundances of young English sole year classes as a function of length. (A) 1969-72, (B) 1977,
similar for the four year classes sampled between
1969 and 1972 in Yaquina Bay (Fig. 5 A). Abundances
of recently recruited individuals 20-45 mm in length
were similar among the 1970, 1971, and 1972 year
classes. The 1969, 1970, and 1971 year classes also
increased in numbers/m2 between 75 and 90 mm
before declining to low catches at larger sizes. Abun-
dances of small fish of the 1969 year class are low
because this year class was only sampled in 1970,
when most fish were >75 mm.
Catches/m2 of the 1977 and 1978 year classes in
Yaquina Bay were generally larger than the 1969,
1970, 1971, 1972, and 1979 year classes (Fig. 5A,
B, C). The 1977 cohort differed from other year
126
KRYGIER and PEARCY: NURERSY AREAS FOR YOUNG ENGLISH SOLE
E
d
O.OI
0001
25
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YAQUINA
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I
MOOLACK b— o <^^>^>
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LENGTH (mm)
125
150
CO
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0.01
0.001
YAQUINA
BAY
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25
50
75 100
LENGTH (mm)
1979
125
150
(C) 1978, (D) 1979 year classes. Note that some curves are based on incomplete sampling of all seasons.
classes by having a large peak of abundance for 30-70
mm individuals, and the 1978 year class had much
higher abundance of large (100-140 mm) individuals
than other year classes.
Obviously the trends shown by these catch curves
cannot be explained by mortality alone Immigration
of young benthic English sole into our sampling area
of Yaquina Bay is suggested by the increased catches
of 75-100 mm individuals of the 1970 and 1971 year
classes and increased catches of 20 to 40-45 mm in-
dividuals of the 1978 and 1979 year classes.
Beam trawls catches at Moolack Beach for the
1977, 1978, and 1979 year classes and beach seine
catches in Yaquina Bay for part of the 1977 year class
127
FISHERY BULLETIN: VOL. 84, NO. 1
and the 1978 year class indicate that the abundance
of newly recruited, settling fish (<24 mm) of the 1977
and 1978 year classes was higher at Moolack Beach
than in Yaquina Bay (Fig. 5B, C). These high catches
at Moolack Beach were followed by a steep decline
in catches to the 41-44 mm size class. English sole
larger than 30 mm were consistently less abundant
at Moolack Beach than in Yaquina Bay. Densities in-
creased in Yaquina Bay concurrent with the steep
decline of 20-44 mm individuals at Moolack Beach.
These trends suggest immigration of young fish from
the shallow waters of the open coast to Yaquina Bay
over a range of sizes, from 20 to 40 mm.
Two peaks occurred in the beach seine catches of
the 1978 year class: at 20-25 and 40-45 mm. The first
peak coincides with the sizes that decreased marked-
ly in abundance at Moolack Beach. The second peak
coincides with low abundance of 40-45 mm fish at
Moolack, and with a decrease in catches of these
sizes of fish at the trawl stations in Yaquina Bay.
These trends of trawl-caught fish suggest that im-
migration from Moolack Beach first occurred to the
shallow waters of the bay and then to the deeper
trawl stations. The peak in the catches of 40-45 mm
fish at seine stations may be caused by immigration
into these shallower waters of metamorphosed in-
dividuals from either the offshore areas or deep
areas of Yaquina Bay.
Abundances and Sizes in
Five Estuaries
Age-0 English sole were present in all five estu-
aries sampled with trawls during May and June
1978. The mean abundance of young English sole,
which ranged from 0.7/m2 in Tillamook Bay to
0.02/m2 in the Umpqua estuary, generally de-
creased from the northern to the southern estuaries
(Table 2). The exception was Yaquina Bay. It was
latitudinally the middle estuary, yet abundance of
English sole there ranked above that in Siletz Bay.
No consistent relationship was observed between
mean abundances and the area of estuaries, river
flows, tidal prisms, or flushing times using the data
of Choi (1975) or Starr (1979)7.
A broad size range of fish was caught in Tillamook,
Siletz, and Alsea Bays, while we caught few in-
dividuals larger than 36 mm in the Umpqua River
estuary (Table 3). In Yaquina Bay, a higher propor-
tion of large individuals (>65 mm) was found than
in the other estuaries. A much broader range of sizes
Table 2.— Mean abundance and standard deviation of 0-age
English sole in five estuaries north and south of Yaquina Bay and
along the open coast between 9 and 37 m, April-June 1978.
No. of
SD
Location
Date: 1978
hauls
No./m2
(S)
Estuary
Tillamook Bay
8 May
21
0.715
0.916
Siletz Bay
9 May
21
0.184
0.206
Yaquina Bay
10 April;
12 July
6
0.332
0.251
Alsea Bay
10 May
21
0.059
0.075
Umpqua River
12 May
19
0.016
0.037
estuary
Ocean Off
Tillamook Bay
15 May;
17 June
12
0.005
0.013
Siletz Bay
16 May;
29 June
9
0.019
0.020
Alsea Bay
22, 29 June
Umpqua River
28 June
3
0.001
0.001
estuary
North of
16, 23 May;
14
0.006
0.011
Newport
29 June
South of
18 June
9
0.003
0.004
Newport
was captured in these estuaries than in open coastal
areas on the dates sampled.
Growth
Despite prolonged recruitment of young English
sole in Yaquina Bay (Fig. 4) distinct length modes
were usually present for each sampling date Growth
rates in Yaquina Bay, estimated by following the pro-
gression of length modes of cohorts over time, were
generally greatest (0.46-0.49 mm/d) during the late
spring to early fall, while growth rates in winter were
lower (0.26-0.32 mm/d) (Table 4). The growth rate
from January to July 1970 was 0.47 mm/d, similar
to the spring-fall estimates. Growth rates were
estimated only for the spring-fall period off Moolack
Beach. These were similar to those for Yaquina Bay
fish but more variable, ranging from 0.28 to 0.42
mm/d.
DISCUSSION
Larvae of English sole are abundant in coastal
waters off Oregon, ranking first among the flatfishes
in some years (Richardson 19778; Richardson and
Pearcy 1977; Mundy 1984). Young larvae (<10 mm)
of English sole are rare in estuaries of the Oregon-
California coast as evidenced by plankton samples
7Starr, R. M. 1979. Natural resources of Siletz esturary. Oreg.
Dep. Fish Wildl., Estuary Inventory Rep. 2(4):l-44.
8Richardson, S. L. 1977. Larval fishes in Ocean waters off Ya-
quina Bay, Oregon: Abundance, distribution and seasonality,
January 1971 to August 1972. Oreg. State Univ. Sea Grant Publ.
ORESU-T-77-003.
100
KRYGIER and PEARCY: NURSERY AREAS FOR YOUNG ENGLISH SOLE
of only 6 larvae in 393 tows in Yaquina Bay (Pearcy
and Myers 1974), 22 larvae in 84 tows in the lower
Columbia River (Misitano 1977), and 4 larvae in 89
tows from Humboldt Bay (Eldridge 1970; Misitano
1970, 1976). However, young larvae are common in
offshore collections (Porter 1964; Pearcy and Myers
1974; Laroche and Richardson 1979), and transform-
ing larvae (19-22 mm) are frequent in collections
from Humboldt Bay and the Columbia River estuary
(Eldridge 1970; Misitano 1970, 1976). Thus young
P. vetulus that enter estuarine nurseries do so as
large transforming larvae or after completion of
metamorphosis.
Our data confirm the above findings. We found
that settlement of metamorphosing English sole to
the bottom was common both in the Yaquina Bay
estuary and at Moolack Beach along the open coast.
Transforming individuals along the coast were
caught in largest numbers/m2 at depths of 16 m or
less, but they were also captured at the deepest sta-
tions sampled (Fig. 2). Since small larvae were rare
in Yaquina Bay (Pearcy and Myers 1974), these
trends suggest movement into the bay of transform-
ing larval stages. Boehlert and Mundy (in prep.)9 have
subsequently confirmed that small juveniles as well
as transforming larvae of English sole recruit to Ya-
quina Bay.
Although densities of transforming larvae were
sometimes higher at Moolack Beach than in Yaquina
Bay, densities of juvenile fish >30 mm were usually
over an order of magnitude higher in Yaquina Bay
than at Moolack Beach, indicating either immigra-
Table 3.— Length distribution of English sole caught in the five estuaries, Moolack Beach and grid stations, 10 April-12 June 1978.
No. of
<
Standard lengths (mrr
i)
Location
fish
14-20
21-25
26-30
31-35
36-40
41-45
46-50
51-55
56-60
61-65
66-70
71-75
76-80
81-85 86-90
8:V:78
Tillamook
2,979
904
1,619
296
48
19
23
26
31
13
4
4
2
9:V:78
Siletz Bay
673
242
256
72
36
13
13
21
14
5
1
10:V:78
Alsea Bay
306
41
98
49
25
20
15
19
27
9
1
1
1
12:V:78
Umpqua River estuary
54
30
12
5
4
1
1
1
10:IV:78
Yaquina Bay
163
46
16
1
6
11
11
11
23
18
11
6
2
1
12:VI:78
Yaquina Bay
156
2
6
9
9
18
6
6
12
17
23
18
16
8
3 3
10:IV:78
Moolack Beach
221
209
9
3
12:VI:78
Moolack Beach
24
5
12
5
1
1
23:V:78
Offshore grid
47
42
5
Table 4.— Growth of juvenile English sole esti-
mated from modal progression of size-fre-
quency histograms from catches in Yaquina Bay
and Moolack Beach, 1970-79.
mm/d
Area and date
(slope)
?
Yaquina Bay
Jan. 1970-July 1970
0.46
0.98
Dec. 1971 -Feb. 1972
0.26
0.92
Jan. 1972-Feb. 1972
0.32
0.91
Jan. 1978-Apr. 1978
0.31
0.91
Apr. 1970-Oct. 1970
0.46
0.96
May 1971-Oct. 1971
0.47
0.98
Mar. 1979-Sept. 1979
0.49
0.96
Moolack Beach
Aug. 1978-Oct. 1978
0.41
0.98
May 1978-Oct. 1978
0.28
0.93
Apr. 1979-Sept. 1979
0.38
0.96
May 1979-Aug. 1979
0.42
0.99
June 1979-Sept. 1979
0.36
1.00
tion into the bay from the open coast during or after
metamorphosis, or dispersal or higher mortality
rates of young along the open coast than in the estu-
ary. Increasing densities in Yaquina Bay, concurrent
with decreasing densities at Moolack Beach, suggest
immigration into the bay over an extended range of
sizes from 25 to 40 mm.
The mechanisms for such movements are not fully
understood, but vertical movement of young fish off
the bottom during periods of flood tide has been
shown to effect transport into estuaries in several
9Boehlert, G. W., and B. C. Mundy. Recruitment dynamics of the
English sole, Parophrys vetulus, to a west coast estuary. Unpubl.
manuscr., 16 p. Southwest Fisheries Center Honolulu Laboratory,
National Marine Fisheries Service, NOAA. P.O. Box 3830, Hono-
lulu, HI 96812.
129
FISHERY BULLETIN: VOL. 84 NO. 1
flatfish species. Cruetzberg et al. (1978) suggested
that immigration of plaice, Pleuronectes platessa, lar-
vae is based on such a "selective tidal transport," and
that starvation induces the swimming behavior re-
sulting in transport by currents. De Veen (1978) con-
cluded that juvenile sole (Solea soled) use tidal trans-
port to enter the Wadden Sea in the spring. Meta-
morphosing larvae of the stone flounder, Kareius
bicoloratus, also immigrate into estuarine nurseries
with tidal currents; they were most abundant in
plankton net collections during flood tides at night
in an estuary of Sendai Bay, Japan (Tsurata 1978).
Misitano (1976) captured metamorphosing English
sole in a 1 m midwater trawl, especially after dark,
in Humboldt Bay. Boehlert and Mundy (fn. 9) found
that transforming English sole larvae were usually
most abundant during flood tides at night in the
moored plankton net that was nearest the bottom
in the lower portion of the Yaquina Bay estuary and
that recruitment to the bay was correlated with on-
shore Ekman transport.
Our estimates of growth from modal progressions
length-frequency histograms [averaging 0.40 mm/d
(s = 0.10) for Yaquina Bay and 0.37 mm/d (s = 0.06)
for Moolack Beach] were considerably higher than
Rosenberg's (1982) estimates even for the same years
(Table 4). Rosenberg studied growth of 0-age English
sole using fortnightly otolith rings as an aging tech-
nique. He calculated that fish, 140-480 d of age, col-
lected during 1978 and 1979 in Yaquina Bay and at
Moolack Beach grew about 0.28 mm SL/d. Estimates
of growth rates of juvenile English sole from length
data by Westrheim (1955) in Yaquina Bay, as well as
by Smith and Nitsos (1969) in Monterey Bay, and Van
Cleve and El-Sayed (1969) and Kendall (1966) in
Puget Sound were more similar to our estimates
than those of Rosenberg (1982, table 2). The differ-
ences in apparent growth rates between length fre-
quency and otolith measurements are difficult to ex-
plain. Avoidance of nets by larger sole (e.g., Kuipers
1975), emigration of larger fish out of the sampling
area in the late summer, and prolonged immigration
of small fish into the estuary, are likely. Any of these
would result in an underestimates of growth by the
length-frequency method (see Rosenberg 1982 for
opposite explanations). Differential mortality of
small fish (Rosenberg 1982) or methodological diffi-
culties in analyzing otolith growth increments may
also help explain the differences.
Our study confirms the observations of Laroche
and Holton (1979) that small 0-age English sole are
not found exclusively in estuaries along the Oregon
coast, and that average sizes of English sole increase
with depth at Moolack Beach. Laroche and Holton
(1979) suggested that even low density or localized
utilization of the extensive unprotected offshore
areas along the coast could be an important factor
in determining the English sole production off Ore-
gon. Tb evaluate this possibility, we determined total
areas within the range of our sample depths in the
lower reaches of the five estuaries and multiplied
these areas by the average catch/m2 of 0-age
English sole (<90 mm) to obtain an estimate of total
number of young English sole in each estuary. The
average catch was also determined from 47 collec-
tions between 9 and 36 m where we found highest
catches of 0-age fish, along 448 km of the open coast
from our May-June catches (Table 2). The average
catch/m2 of 0-age sole in the five estuaries usually
was many times that along the open coast. But be-
cause of the large differences in areas, the estimate
for total abundance of 0-age sole during the May-
June period on the open coast was about 643 x
105, considerably higher than the estimate for the
five estuaries, 140 x 105. Most of the fish caught
during this period, however, were transforming or
recently metamorphosed juveniles that could have
entered estuaries later in the year. This may in part
explain the 17-fold decrease in average abundance
of small sole along the open coast between 16-23 May
(x = 0.039, n = 18, s = 0.11) and 28-29 June (x =
0.002, n = 29, s = 0.004) in the vicinity of Tillamook
and Siletz Bays. Our estimate of total abundance
along the coast in June is 70 x 105, about half the
estimate for the five estuaries about a month and
one-half earlier. Because of our small sample sizes,
lack of sampling in some estuaries and open coast
areas, and temporal differences (and associated mor-
tality) among samples, these estimates must be con-
sidered crude. Nevertheless, they suggest that shal-
low waters of the open coast are important initial
settling areas for English sole and that both estu-
aries and the open coast are nursery grounds for
fully transformed 0-age sole
We need data on the growth and survival from
estuarine and open coastal areas to evaluate their
importance as nursery grounds and to assess their
relative contributions to the commercially harvested
and spawning population. Olsen and Pratt (1973)
used parasites as indicators of English sole nursery
grounds. The incidence of Echinorhynchus lageni-
formis, an acanthocephalan that they considered was
acquired only in estuaries, averaged 29.9% in 0-age
English sole <117 mm SL captured in Yaquina Bay
and 28.5% in 0-age fish collected offshore at depths
of 10-80 m near the entrance of Yaquina Bay dur-
ing November and December, a period after most
0-age fish had emigrated from the bay. They con-
130
KRYGIER and PEARCY: NURSERY AREAS FOR YOUNG ENGLISH SOLE
eluded from these similar incidences of infection that
there was no sizable influx of 0-age English sole to
their offshore study area other than from estuarine
nursery grounds. Their results imply that any 0-age
fish that reside along the open coast during the
spring and summer have much higher mortality
rates than estuarine residents and do not contribute
significantly to the offshore population of 0-age fish.
Growth rates of 0-age English sole from Moolack
Beach and Yaquina Bay, however, do not support this
hypothesis. They appear to be similar (Rosenberg
1982; Table 4). Our catch curves (Fig. 5C, D) also pro-
vide no evidence for grossly higher mortality rates
at Moolack Beach. The total declines in abundances
per m2 are fairly similar for English sole 50-100
mm, presumably a size range that occurs after immi-
gration into the estuary but before emigration of
larger sizes out of the estuary in the fall.
The fact that 0-age English sole immigrate from
offshore into estuaries where they are found in high
concentrations suggests that this behavior is adap-
tive Standing stocks and productivity of small ben-
thic food organisms are undoubtedly higher in estu-
aries than along the open coast, but because of the
higher concentrations of young flounder in Yaquina
Bay than Moolack Beach (Fig. 5), competition for
food probably results in similar growth rates in these
two habitats. The rapid decreases in the estuarine
densities of 0-age English sole during the fall and
winter months are evidence of emigration out of
estuaries to offshore areas. In Yaquina Bay, we found
a decrease in density of 0-age fish in the late fall as
well as a decrease in average size at this time. Fre-
quently age-0 (20-55 mm) and age-I (75-115 mm) fish
were both present in the winter, with the age-I fish
disappearing entirely from catches in the spring.
Westrheim (1955) and Olsen and Pratt (1973) also
found decreases in catch per effort and average sizes
of young English sole that indicated definite emi-
gration from Yaquina Bay after October. Forsberg
et al. (1975)10 reported emigration of English sole
from Tillamook Bay in early fall with few individuals
remaining in November.
According to Bayer (1981), small English sole were
common at intertidal stations in Yaquina Bay most
of the year, but they were absent during November
and were less common during other fall months.
Toole (1980) also found that English sole disappeared
from intertidal areas in early fall at an average size
of 68 mm SL and subsequently resided in subtidal
10Forsberg, B. O., J. A. Johnson, and S. M. Klug. 1975. Identi-
fication and notes on food habits of fish and shellfish in Tillamook
Bay, Oreg. Fish Comm. Oreg. Contract Rep., 85 p.
channels until they were about 120 mm SL in Hum-
boldt Bay. He associated these different distributions
with changes in feeding habits, and possibly with a
reduction in intraspecific competition among small
and large 0-age English sole Indeed, emigration out
of bays and estuaries in the fall may be related to
limitations in the carrying capacity for high densities
and standing stocks of young English sola
We conclude that estuarine and offshore nursery
grounds combine to significantly increase the sur-
vival and total population size of 0-age fish. Utiliza-
tion of these two diverse habitats may also improve
the chances for good survival of young fish from at
least one habitat even when adverse conditions af-
fect the other.
LITERATURE CITED
Ahlstrom, E. H., and H. G. Moser.
1975. Distributional atlas of fish larvae in the California Cur-
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Alderice, D. F, and C. R. Forrester.
1968. Some effects of salinity and temperature on early
development and survival of the English sole (Parophrys
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Bayer, R. D.
1981. Shallow-water intertidal ichthyofauna of the Yaquina
estuary, Oregon. Northwest Sci. 55:182-193.
Budd, P. L.
1940. Development of the eggs and early larvae of six Califor-
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Carey, A. G., Jr., and H. Heyomoto.
1972. Techniques and equipment for sampling benthic or-
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Columbia River estuary and adjacent ocean waters, bioen-
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Choi, B.
1975. Pollution and tidal flushing predictions for Oregon's
estuaries. M.S. Thesis, Oregon State Univ., Corvallis, 163 p.
Creutzberg, F, A. Th. G. W. Eltink, and G. J. Van Noort.
1978. The migration of plaice larvae, Pleuronectes platessa,
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Demory, R. L.
1971. Depth distribution of some small flatfishes off the north-
ern Oregon-southern Washington coast. Res. Rep. Fish.
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De Veen, J. F
1978. On selective tidal transport in the migration of North
Sea plaice (Pleuronectes platessa) and other flatfish species.
Neth. J. Sea Res. 12:112-147.
Eldridge, M.
1970. Larval fish survey of Humboldt Bay. M.S. Thesis, Hum-
boldt State Coll., Areata, 52 p.
Forrester, C. R.
1969. Results of English sole tagging in British Columbia
waters. Pac. Mar. Fish. Comm. Bull. 7:1-10.
Harry, G. Y., Jr.
1959. Time of spawning, length at maturity, and fecundity of
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FISHERY BULLETIN: VOL. 84. NO. 1
the English, petrale, and Dover soles (Parophrys vetulus,
Eopsetta jordani, and Microstomia pacificus, respectively).
Oreg. Fish Comm., Res. Briefs 7(1):5-13.
Hart, J. L.
1973. Pacific fishes of Canada. Fish. Res. Board Can. Bull.
80, 740 p.
Hewitt, G. R.
1980. Seasonal changes in English sole distributions: An anal-
ysis of the inshore trawl fishery off Oregon. M.S. Thesis,
Oregon State Univ., Corvallis, 59 p.
Jow, T.
1969. Results of English sole tagging off California. Pac
Mar. Fish. Comm. Bull. 7:15-33.
Kendall, A. W., Jr.
1966. Sampling juvenile fishes on some sandy beaches of
Puget Sound, Washington. M.S. Thesis, Univ. Washington,
Seattle, 77 p.
Ketchen, K. S.
1947. Studies on lemon sole development and egg production.
Fish. Res. Board Can., Prog. Rep. Pac. 73:68-70.
1956. Factors influencing the survival of the lemon sole (Paro-
phrys vetulus) in Hecate Strait, British Columbia. J. Fish.
Res. Board Can. 13:647-694.
Kruse, G. H., and A. V. Tyler.
1983. Simulation of temperature and upwelling effects on the
English sole (Parophrys vetulus) spawning season. Can. J.
Fish. Aquat. Sci. 40:230-237.
Krygier, E. E., and H. F. Horton.
1975. Distribution, reproduction, and growth of Crangon
nigricauda and Crangon franciscorum in Yaquina Bay,
Oregon. Northwest Sci. 49:216-240.
Kuipers, B.
1975. On the efficiency of a two-meter beam trawl for juvenile
plaice (Pleuronectes platessa). Neth. J. Sea Res. 9:69-85.
Laroche, J. L., and S. L. Richardson.
1979. Winter-spring abundance of larval English sole, Paro-
phrys vetulus, between the Columbia River and Cape Blanco,
Oregon during 1972-75 with notes on occurrences of three
other pleuronectids. Estuarine Coastal Mar. Sci. 8:455-476.
Laroche, J. L., S. L. Richardson, and A. A. Rosenberg.
1982. Age and growth of a pleuronectid, Parophrys vetulus,
during the pelagic larval period in Oregon coastal waters.
Fish. Bull., U.S. 80:93-104.
Laroche, W. A., and R. L. Holton.
1979. Occurrence of 0-age English sole, Parophrys vetulus,
along the Oregon coast: An open coast nursery area? North-
west Sci. 53:94-96.
Misitano, D. A.
1970. Aspects of the early life history of English sole (Paro-
phrys vetulus) in Humboldt Bay, California. M.S. Thesis,
Humboldt State Coll., Areata, 57 p.
1976. Size and stage of development of larval English sole,
Parophrys vetulus, at time of entry into Humboldt Bay.
Calif. Fish Game 62:93-98.
1977. Species composition and relative abundance of larval
and post-larval fishes in the Columbia River estuary, 1973.
Fish. Bull., U.S. 75:218-222.
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. M.S. Thesis, Ore-
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Myers, K. W W
1980. An investigation of the utilization of four study areas
in Yaquina Bay, Oregon, by hatchery and wild juvenile sal-
monids. M.S. Thesis, Oregon State Univ., Corvallis, 234 p.
Olsen, R. E., and I. Pratt.
1973. Parasites as indicators of English sole (Pa rophrys vetu-
lus) nursery grounds. Trans. Am. Fish. Soc 102:405-411.
Pattie, B. H.
1969. Dispersal of English sole, Parophrys vetulus, tagged off
the Washington coast in 1956. Pac Mar. Fish. Comm. Bull.
7:11-14.
Pearcy, W G., and S. S. Myers.
1974. Larval fishes of Yaquina Bay, Oregon: A nursery ground
for marine fishes? Fish. Bull., U.S. 72:201-213.
Porter, P.
1964. Notes on fecundity, spawning and early life history of
petrale sole (Eopsetta jordani) with descriptions of flatfish
larvae collected in the Pacific Ocean off Humboldt Bay,
California. M.S. Thesis, Humboldt State Coll., Areata, 98 p.
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.
Rosenberg, A. A.
1982. Growth of juvenile English sole, Parophrys vetulus, in
estuarine and open coastal nursery grounds. Fish. Bull., U.S.
80:245-252.
Rosenberg, A. A., and J. L. Laroche.
1982. Growth during metamorphosis of English sole,
Parophrys vetulus. Fish. Bull., U.S. 80:150-153.
Sims, C. W, and R. H. Johnson.
1974. Variable-mesh beach seine for sampling juvenile salmon
in Columbia River estuary. Mar. Fish. Rev. 36(2):23-26.
Smith, J. G., and R. J. Nitsos.
1969. Age and growth studies of English sole, Parophrys vetu-
lus, in Monterey Bay, California. Pac Mar. Fish. Comm. Bull.
7:73-79.
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, IL, 171 p.
Toole, C. L.
1980. Intertidal recruitment and feeding in relation to optimal
utilization of nursery areas by juvenile English sole (Paro-
phrys vetulus: Pleuronectidae). Environ. Biol. Fishes 5:
383-390. ,
Tsuruta, Y
1978. Field observations on the immigration of larval stone
flounder into the nursery ground. Tohoku J. Agric Res. 29:
136-145.
Van Cleve, R., and S. Z. El-Sayed.
1969. Age, growth, and productivity of an English sole (Paro-
phrys vetulus) population in Puget Sound, Washington. Pac
Mar. Fish. Comm. Bull. 7:51-71.
Westrheim, S. J.
1955. Size composition, growth and seasonal abundance of
juvenile English sole (Parophrys vetulus) in Yaquina Bay.
Oreg. Fish. Comm. Res. Briefs 6(2):4-9.
132
ORGANIC AND TRACE METAL LEVELS IN
OCEAN QUAHOG, ARCTICA ISLANDICA LINNE,
FROM THE NORTHWESTERN ATLANTIC
Frank W. Steimle,1 Paul D. Boehm,2 Vincent S. Zdanowicz,1
and Ralph A. Bruno1
ABSTRACT
Chemical contamination of biological resources is an important problem for resource managers. This study
reports on body burden levels of several contaminants of concern: polychlorinated biphenyls (PCB), poly-
nuclear aromatic hydrocarbons (PAH) of both petroleum and combustion sources, total petroleum hydrocar-
bons, and seven trace metals (Ag, Cd, Cr, Cu, Ni, Pb, and Zn) in a resource species, the ocean quahog,
collected between Virginia and Nova Scotia. Organic and trace metal contaminants were detected, at low
levels, in all samples examined, with highest levels being generally found in samples from the inner New
York Bight and Rhode Island Sound. The highest PCB and PAH values were 27 and 55 ppb, respectively;
Ag, Cd, and Cr values were generally <5 ^g/g dry weight; Cu, Ni, and Pb generally <15 ^g/g dry weight
with a few exceptions; and Zn ranged from 50 to 153 uglg dry weight.
The ocean quahog, Arctica islandica Linne, is a
large, bivalve mollusc found on both sides of the
North Atlantic In the northwestern Atlantic, it oc-
curs from just north of Cape Hatteras, NC, to New-
foundland, Nova Scotia, being most abundant on the
middle to outer continental shelf at depths between
about 30 and 150 m (Merrill et al. 1969). The species
is edible and some commercial harvesting has oc-
curred since 1943 in the Rhode Island area; however,
intensive fishing for this species did not begin until
the 1970s when surf clam, Spisula solidissima (Dill-
wyn), stocks, an inshore species, were drastically
reduced by overfishing (Ropes 1979).
Arctica islandica generally inhabit silty sand sedi-
ments of the middle to outer continental shelf that
are less influenced by waves and strong currents
than shallower areas. Areas of silty sand are thought
to be at least partially depositional in nature, i.e, fine
organic-rich particles tend to accumulata It is gen-
erally agreed that many chemical pollutants, intro-
duced to the marine environment via impacted estu-
aries and coastal areas, ocean dumping, and atmo-
spheric sources, often are bound to and associated
with fine organic and inorganic particle aggregates,
both in the water column and at the sediment sur-
face These aggregates ultimately can accumulate
in these natural depositional areas as the results of
some recent studies show that contaminants ap-
'Northeast Fisheries Center Sandy Hook Laboratory, National
Marine Fisheries Service, NOAA, Highlands, NJ 07732.
2Battelle, New England Marine Research Laboratory, 397 Wash-
ington Street, Duxbury, MA 02332.
parently are accumulating in silty areas relatively
remote from most possible sources, eg., organic con-
taminants found south of Cape Cod, MA, in the mid-
dle to outer continental shelf (Boehm 1983a). Some
authors have also reported a trend of increasing sedi-
ment trace metal levels with depth on the Middle
Atlantic shelf (Harris et al. 1977), but the specific
sources of these contaminants are still unknown.
Because A. islandica is a common, sedentary, long-
lived (Thompson et al. 1980) inhabitant of these sil-
ty sands that frequently contain higher levels of con-
taminants than coarser sands, the species may be
particularly susceptible to contamination. Wenzloff
et al. (1979) reported "greater average concentration
of silver, arsenic, cadmium, copper, and zinc
... in ocean quahogs than in surf clams" for the Mid-
dle Atlantic Surf clams are generally found in
shallower, medium sand areas. Thus, A. islandica
may be a good offshore "indicator" species to moni-
tor for trends in marine chemical pollution. Although
some studies on contaminant body burdens of A.
islandica have been reported (ERCO 19783; Sick
1978, 1981; Wenzloff et al. 1979; Reynolds 1979;
Payne et al. 1982), these studies have been limited
generally to a particular restricted area, have not
examined both types of contaminants or only a few
components of each contaminant class, or have ex-
amined only certain tissues, not whole body levels.
The present study provides body burden data over
Manuscript accepted April 1985.
FTSHF.RY RTTT.T.F.TTN- VDT, 84 NO 1 IftSfi
3ERCO (Energy Resources Company). 1978. New England
OCS Environmental Benchmark. Draft Final Rep., Vol. II, to U.S.
Dep. Inter., Bur. Land Manage, Miner. Manage Serv., 628 p.
133
FISHERY BULLETIN: VOL. 84, NO. 1
a wide range of this species' occurrence in the north-
western Atlantic and includes information on or-
ganic, La, polychlorinated biphenyls (PCB), polynu-
clear aromatic hydrocarbons (PAH) from combustion
and petroleum sources, and bulk levels of the petro-
leum hydrocarbon (PHC) class, and seven trace metal
contaminants. The study includes the first known
set of PCB data for this species.
MATERIALS AND METHODS
Ocean quahog samples were obtained at random
stations from wide areas on the continental shelf of
the northwestern Atlantic (Fig. 1). These were col-
lected from annual, summer hydraulic dredge shell-
fish surveys of NOAA's Northeast Fisheries Center
from 1981 and 1982. At most stations, 10-12
medium-sized clams were selected, as available Half
of the collection was prepared for organic analysis
by wrapping them in aluminum foil that had been
prewashed with spectral grade acetone followed by
dichloromethane; the remaining half for trace metals
were placed in polyethylene plastic bags. All were
quickly frozen at -20°C. In certain areas where
there were not sufficient samples at a particular sta-
tion to provide material for both organics and trace
metal analyses, samples were collected at a nearby
station, with similar environmental characteristics,
to complete the collection for the area. These paired
station samples were not intermixed.
Chemical Analysis - Organics
In the laboratory, the thawed whole meats of each
of the five or six individual clams in each station sam-
ple were removed from the shells, pooled, and homo-
genized in a high-speed blender. A 100 g (wet weight)
aliquot was removed from the homogenate and pro-
cessed according to the extraction, fractionation, and
analytical methodology described by Warner (1976),
as modified by Boehm et al. (1982). After aqueous
caustic (0.5N KOH) digestion of the tissue for 12 h,
the digestate was back-extracted three times with
hexane The hexane extract was concentrated by ro-
tary evaporation, then fractionated on a 5% deacti-
vated alumina/activated silica gel column. The first
eluting fraction from the alumina/silica column (fj)
contained the saturated PHC; the second fraction
(f2) contained the PCB and PAH. Quantitation pro-
cedures closely followed those by Boehm (1983b).
PHC factors were quantified using the internal
standard method whereby all peaks are quantified
relative to androstane in the fj fraction and 0-ter-
phenyl in the f2 fraction.
PCBs were quantified relative to the internal
standard tetrazene (2, 3, 5, 6 tetrachloronitroben-
zene). The average relative response factors of two
or three isomers in each of the di-, tri-, tetra-, penta-,
hexa-, hepta- and octachlorobiphenyls groups were
applied to the sum of the peaks in each grouping.
Thus, PCBs were quantified by isomer group rather
than according to the Aroclor4-type quantification
(Duinker et al. 1980, 1983; Boehm 1983b). PHCs
were determined by the total of f: and f2 fractions,
as analyzed by high resolution (fused silica capillary)
gas chromatography with flame ionization detection
(GC2/FID). A Hewlett Packard model 5840A gas
chromatograph was used for all GC2 deter-
minations. A 30 m fused silica SE-30 (0.25 mm i.d.;
J and W Scientific) column was used to analyze the
saturated hydrocarbon (ft) fraction. A 30 m SE-52
fused silica column was used to analyze the aroma-
tic/olefinic (f2) fraction by GC2/FID and the same
fraction by gas chromatograph/mass spectrometer
(GC/MS) (see below). The f2 fractions were analyzed
by GC2/ECD (electron capture detection) to obtain
the PCB concentrations. PCBs were analyzed on a
30 m SE-52 fused silica column. The f2 fraction was
also analyzed by a Finnegan MAT model 4530
computer-assisted GC/MS system for PAH deter-
minations. GC/MS conditions were as follows: ioniza-
tion voltage, 70 ev; electron multiplier voltage 2,000
volts; scan conditions 45-450 amu at 400 amu/s.
Chemical Analysis - Trace Metals
Whole clams, 5 or 6 per station, were thawed, and
the whole body removed from the shells. Each indivi-
dual clam was weighed in Pyrex beakers and dried
for 16-20 h at 105°C. Twenty mL of 70% trace metal
grade nitric acid were added to each beaker, which
was covered with a Pyrex watch glass and heated
(70° -75°C) on a ceramic hot plate until dry. After
cooling to room temperature, another 20 mL of con-
centrated nitric acid were added and the dissolution
continued. After 3 or 4 repeated acid additions and
evaporations, 10 mL of 30% hydrogen peroxide were
added, the solutions evaporated to near dryness and
removed from the heat. When cooled, samples were
filtered through Whatman #4 filter paper and
brought to a final volume of 25 mL in a Pyrex glass-
stoppered graduated cylinder by adding 5% (w/v) ni-
tric acid. Analysis was performed on a Perkin Elmer
model 5000 atomic absorption (AA) spectrophotom-
eter employing an air-acetylene flame and conven-
4Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
134
STEIMLE ET AL.: ORGANIC AND TRACE METALS IN OCEAN QUAHOG
44"
76°
74
!£
NARRAGANSETT BAY,
NEW YORK BIGHT
APEX
"Mud Patch'
"NEW BEDFORD HARBOR
AND BUZZARDS BAY
GEORGES BANK
®379
245
LEGEND
•
HEAVY METALS
o
ORGANICS
®
BOTH
50 100 150 200
KILOMETERS
44"
^
42-
40°
38°J
36
■ ■ ■
■-.- •_■ NMFS SanOv Hoc*
70°
68°
66"
Figure l.-Station locations' collections oi Arctic a islandica. Stations 367, 335 and 349 are on the Scotian Shelf at the following coor-
dinates: Station 367 (lat. 43°44'N, long. 61°08'W), Station 335 (43°25'N, 61°42'W) and Station 349 (43°21'N, 61°23'W).
tional AA techniques. Reagent blanks were carried
through the same procedure All reagents used were
of trace metal analytical grade Deionized water was
of 18 megohm purity. The National Bureau of Stan-
dards (NBS) SRM 1566, freeze-dried oyster homog-
enate, was used as the tissue standard. Recoveries
were at least 80% of this standard in all cases.
RESULTS
The analytical results for organic contaminants are
presented in Tables 1 (PHC and PCB) and 2 (PAH).
PHC values are given as total saturated and aromatic
hydrocarbons as determined by GC2. PCB values
are given as total tri-, tetra-, penta-. hexa-, and hepta-
135
FISHERY BULLETIN: VOL. 84, NO. 1
Table 1.— PHC (petroleum hydrocarbon) and PCB (polychlorinated biphenyl)
levels in northwestern Atlantic Arctica islandica.
Area
and
station
PHC O^g/g wet weight)
Saturated Aromatic Total
PCB
(ng/g
wet weight)
Cl3
Cl4
Ci5
Cl6
Cl7
Total
Inshore New York Bight
22
0.2
1.3
1.5
4.8
5.1
1.6
4.4
0.2
16.1
26
6.0
0.9
6.9
0.4
0.3
0.2
0.5
0.1
1.5
27
0.4
0.8
1.2
7.2
2.8
1.6
1.8
<0.1
13.4
28
0.2
0.9
1.1
6.7
4.2
2.6
6.5
0.1
20.2
32
3.2
4.1
7.3
5.4
5.1
4.1
10.7
0.7
26.8
47
<0.1
0.2
0.2
1.1
0.4
0.1
0.3
—
1.9
59
3.1
1.5
4.6
3.4
3.6
3.0
5.7
0.5
16.4
Offshore NJ-VA
77
1.7
0.7
2.4
5.6
1.2
2.9
2.3
0.3
12.2
107
0.2
0.8
1.0
8.0
1.7
0.8
2.8
0.2
13.3
168
0.2
1.1
1.3
2.3
1.3
1.0
3.5
0.5
8.5
173
0.4
0.5
0.9
4.4
4.5
1.3
3.4
—
14.0
174
1.0
0.3
1.3
2.6
0.8
0.4
1.5
<0.1
5.5
224
1.7
0.2
1.9
2.3
1.5
0.5
0.5
<0.1
4.9
Inshore S. New England
237
0.1
0.8
0.9
1.0
0.6
<0.1
<0.1
—
1.7
246
1.2
0.4
1.6
2.0
2.8
2.2
1.5
—
8.5
244
2.2
1.3
3.5
4.9
9.5
2.3
3.8
—
20.4
261
2.0
0.4
2.4
3.4
3.5
2.1
3.1
<0.1
12.1
239
2.9
1.1
4.0
1.4
2.1
1.6
1.9
<0.1
7.0
240
2.8
0.9
3.7
2.2
2.6
2.7
3.5
<0.1
11.0
241
2.3
1.6
3.9
4.1
6.6
6.2
6.3
0.2
23.2
242
1.9
1.8
3.7
2.9
4.6
5.9
6.5
0.2
20.1
Georges Bank
379
0.8
1.1
1.9
0.7
1.2
0.9
1.0
<0.1
3.8
Scotian
Shelf
367
0.6
0.2
0.8
0.8
0.5
0.4
0.3
0.3
2.2
335
1.1
0.1
1.2
0.9
0.4
0.5
2.3
0.1
4.2
349
4.5
0.6
5.1
0.8
0.9
0.4
0.1
—
2.2
chlorobiphenyls (C13-C17), as well as total PCB. PAH
values are presented as individual compounds (e.g,
napthalene) or as homologous series (SN). Table 3
lists the mean trace metal concentrations and stan-
dard deviations; data are presented on a dry weight
basis to simplify comparisons with other studies.
DISCUSSION
PCB levels observed in this survey ranged from
2 to 30 ng/g (ppb) wet weight (Table 1). These values
are in general agreement with other data reported
for PCB levels in other coastal bivalves (Giam et al.
1976; Goldberg 1978; Gadbois 1982), but are lower
than those (to 400 ppb) reported for estuarine spe-
cies (Goldberg 1978; MacLeod et al. 1981; O'Connor
et al. 1982; ERCO 1983). However, we have found
little data on PCB levels in offshore molluscs nor any
other data on PCB levels in A. islandica for compari-
son. None of the A. islandica levels approach the cur-
rent 2 ppm (= 2,000 ppb) U.S. Food and Drug Ad-
ministration (FDA) "seafood action limit" for human
consumption.
In spite of the wide geographical range sampled,
PCB levels were relatively uniform with only an
order of magnitude difference between the high and
low values. Clearly the Georges Bank (station 379)
and remote Nova Scotia (stations 367, 335, 349)
ocean quahogs were minimally contaminated, with
their levels (2-5 ppb) reflecting the global PCB trans-
port phenomena. The ocean quahogs in the near-
shore New York Bight, Rhode Island Sound, and
Buzzards Bay were more contaminated, with values
up to 25 ppb. It is not surprising as previous biogeo-
chemical studies in the western North Atlantic have
clearly shown that several major urban pollutant
sources influence the nearshore environment. For
example, inputs of PCBs are specifically known to
occur in the New York Bight, from esturine fluxes
and via direct ocean dumping (Boehm 1983b) and
in Buzzards Bay, MA, from industrial inputs to the
New Bedford Harbor region (Weaver 1982). Some-
what surprising were the elevated levels at some sta-
tions on the outer New Jersey shelf (12-16 ppb) and
in the Hudson Canyon area (20 ppb). Offshore trans-
port of PCB material towards these stations via
riverine fluxes followed by southerly transport along
the New Jersey shore and down-canyon transport
of ocean-dumped material are possible modes of
transport to these stations (Boehm 1983b).
136
STEIMLE ET AL.: ORGANIC AND TRACE METALS IN OCEAN QUAHOG
Table 2.— PAH (polynuclear aromatic hydrocarbon) levels in northwestern Atlantic
Arctica islandica (ng/g wet weight).
Area
and
station N IN
P
IP
IDBT
IF
1202
1228
1252
B(a)P
IPAH
PPI1
Inshore New York Bight
22 nd nd
4.0
11.9
2.0
1.2
5.5
1.1
<1
<1
23
40
26 nd nd
1.1
1.1
nd
nd
1.1
nd
nd
nd
3.3
0
27 1.0 4.5
2.1
9.1
2.7
1.2
2.7
<1
<1
nd
22
54
28 9.1 12.0
1.3
5.2
<1
nd
1.8
nd
nd
nd
20
72
32 nd nd
3.9
12.4
nd
nd
11.1
14.1
17.3
6.0
55
7
47 4.3 5.1
2.9
2.9
nd
nd
3.1
3.0
4.0
2.0
18
28
59 1.0 5.3
1.0
11.5
<1
nd
1.5
<1
nd
nd
20
77
Offshore NJ-VA
77 <1 3.7
3.3
9.2
<1
1.0
2.4
<1
nd
nd
18
65
107 <1 6.7
2.5
10.0
2.5
3.5
1.5
<1
<1
nd
26
77
168 nd nd
1.8
1.8
nd
nd
2.4
nd
nd
nd
4.2
0
173 1.3 5.9
1.8
6.2
1.3
2.0
2.3
<1
nd
nd
19
72
174 <1 4.0
1.0
5.0
<1
nd
4.0
1.0
1.0
nd
16
56
224 1.4 6.1
2.0
7.8
2.1
1.5
1.3
<1
<1
<1
21
74
Mud Patch
237 <1 <1
2.8
5.0
<1
nd
5.7
3.7
5.4
2.5
19
31
246 nd 11.9
2.2
11.5
1.0
1.3
3.3
nd
nd
nd
29
81
Inshore S. New England
244 nd nd
nd
nd
2.4
nd
1.7
<1
<1
<1
6.1
39
261 nd nd
3.6
9.2
<1
<1
3.3
nd
nd
nd
15
51
239 nd nd
1.6
1.9
nd
nd
2.9
<1
1.2
<1
7.0
4
240 <1 3.3
1.8
5.6
<1
<1
2.8
<1
<1
<1
16
51
241 nd nd
nd
5.0
nd
nd
4.0
1.0
1.0
<1
12
42
242 nd nd
<1
<1
nd
nd
1.5
nd
nd
nd
2.5
40
Georges Bank
379 nd nd
<1
<1
nd
nd
<1
nd
nd
nd
<1
0
Scotian Shelf
367 1.0 1.0
1.5
1.5
nd
nd
1.1
nd
nd
nd
3.6
28
335 nd nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
0
349 4.3 5.1
2.9
2.9
nd
nd
3.1
3.0
4.0
2.0
18
28
Wet weight concentrations = dry weight concentration 4- 7.
N = naphthalene.
IN = total naphthalenes (C0-CJ.
P = phenanthrene.
IP = total phenanthrenes (Cq-CJ.
IDBT = total dibenzothiophenes (C0-C3).
IF = total fluorenes (C0-C3).
1202 = fluoranthene + pyrene.
1228 = benzanthracene + chrysene.
1252 = benzofluoranthenes + benzopyrenes.
B(a)P = benzo(a)pyrene.
nd = not detected (<1 ng/g wet weight).
dd, . . , *N + IDBT + (IP-P) + IF
PPI = percent petroleum index =
IPAH =3M + IP + IDBT
'From Boehm (1983a).
+ IF + 1202
IPAH
1252 + 1228
TV-ends in the PHC and PAH data reveal large-scale
homogeneity in the concentrations observed. PAH
levels ranged from nondetectable to 55 ppb, the high-
est values occurring at the station 32 samples from
the New York Bight, where the highest PCB level
(27 ppb) was also observed. Although our sampling
on Georges Bank consisted of only one station,
results were similar to those of a more extensive
study by Payne et al. (1982), the only other study
of A. islandica we could locate that includes PHC
data. If the entire Northeast region is considered a
sample set, then the PAH values were 16.7 ± 12.0.
However, the composition of the PAH which com-
prises the total PAH number varied considerably,
ranging from 0 to 81% "petroleum" PAH (Table 2).
The percent petroleum index (PPI), developed by
Boehm (1983a, b), estimates the relative contribu-
tions of uncombusted fossil fuels, eg, petroleum, and
from combustion sources to the total PAH assem-
blage This indice, presented in Table 2, is based on
the relative abundance of petroleum constituents,
such as naphthalene, flourenes, dibenzothiophenes,
and alkylated phenanthrenes, to the total PAH mix.
The differences in PPI values for the various samples
cannot, at this time, be ascribed to specific trans-
port or selective uptake factors. However, a knowl-
137
FISHERY BULLETIN: VOL. 84. NO. 1
Table 3—Arctica islandica trace metal body burdens (mean and standard deviation, ^glg-6ry weight)
in areas of the northwest Atlantic; N = number of individual clams examined at each site. Results of
analysis of SRM 1566 are also included; 5-8 NBS (National Bureau of Standards) samples were ex-
amined for each metal (nd = nondetectable).
Area Ag
Cd
C
r
Cu
N
i
Pb
Zn
station N X
±SD
X
±SD
X
+ SD
X
±SD
X
±SD
X
+ SD
X
±SD
Georges Bank
379 6 0.79
0.25
1.36
0.33
3.07
1.38
10.30
2.22
3.46
1.17
4.08
2.07
61.8
11.4
Nantucket
245 5 0.96
0.09
2.75
0.66
2.98
0.83
7.25
1.41
9.54
3.81
5.02
2.21
88.3
21.3
S. New England
237 6 2.65
2.08
3.22
0.65
2.72
0.65
12.76
3.30
27.19
8.18
6.90
1.87
153.9
87.6
181 6 1.14
0.95
3.49
1.39
2.24
0.23
11.70
2.97
21.84
7.22
11.03
4.48
124.7
30.8
244 6 0.56
0.14
1.36
0.47
2.19
1.02
6.49
3.29
4.47
1.75
2.99
1.33
84.1
25.7
Rhode Island Sol
nd
239 6 0.79
0.25
1.36
0.33
3.07
1.38
10.30
2.22
3.46
1.17
4.08
2.07
61.8
11.4
240 6 1 .76
0.65
1.39
0.48
4.02
1.26
11.47
2.92
6.28
1.61
6.71
2.51
87.4
12.8
241 6 1.59
0.93
0.96
0.14
3.96
2.23
12.47
3.80
5.83
2.42
4.61
1.71
126.3
55.4
Block Island Sound
261 6 1 .53
1.82
1.94
0.68
4.56
0.33
10.22
1.55
11.64
3.28
10.17
2.48
101.9
32.6
S. Long Island
189 6 0.74
0.60
2.48
0.63
1.88
0.59
8.78
0.94
18.73
4.75
3.30
0.80
128.4
35.2
23 6 1.18
0.53
2.17
0.67
1.09
0.19
10.31
3.27
17.28
6.07
3.41
1.12
120.2
19.6
26 6 0.84
0.45
1.43
0.56
5.47
1.22
15.78
5.83
9.87
2.73
8.66
3.25
117.6
35.7
29 6 5.25
1.64
1.06
0.29
4.78
3.35
13.65
3.20
8.93
5.06
9.67
4.11
100.7
49.9
New Jersey Shelf
32 6 0.52
0.26
0.67
0.35
2.38
0.20
8.16
5.38
4.47
2.90
3.46
2.24
50.2
22.0
47 5 0.53
0.36
1.20
0.42
1.46
0.83
8.37
2.49
9.87
5.09
3.11
0.87
84.1
31.8
59 3 0.44
0.15
0.23
0.05
0.90
0.09
6.01
1.37
6.01
1.68
1.64
0.28
62.2
18.8
174 6 1.50
0.91
2.19
0.93
1.87
0.65
4.08
0.82
7.79
2.70
4.16
1.60
50.8
6.0
224 6 0.46
0.13
3.06
0.91
1.78
0.43
5.63
1.02
14.91
6.92
5.60
2.23
91.9
33.9
Delmarva Shelf
107 6 0.39
0.25
1.87
0.62
2.44
0.90
4.16
1.02
10.27
2.52
4.80
2.77
58.9
14.2
173 5 0.44
0.30
2.34
1.54
1.62
0.48
4.46
1.76
11.14
4.94
4.35
2.32
61.4
26.2
171 6 0.51
0.12
1.66
0.56
1.71
0.44
5.25
1.57
10.91
3.21
3.55
1.09
75.8
31.8
167 6 0.52
0.29
1.59
0.48
1.98
0.56
7.04
4.36
9.45
4.20
3.54
1.21
76.2
43.4
168 5 2.22
1.36
3.08
1.03
2.38
0.68
5.19
1.79
13.74
5.34
6.51
2.57
74.6
14.8
123 6 2.40
1.68
2.53
0.58
3.34
1.01
4.98
1.16
14.13
3.95
5.91
1.58
77.9
20.6
165 5 0.54
0.36
2.09
0.68
2.36
0.78
6.44
2.39
11.48
4.78
4.35
2.21
74.4
28.5
NBS SRM 1566
— 8 0.71
0.24
2.86
0.19
1.07
0.52
49.50
4.00
1.72
0.35
nd
—
772.0
53.0
edge of a baseline PPI value can be important for
discerning the source of any change in contaminant
levels in benthic animals.
In a similar manner, the PCB value has been
separated, by virtue of the use of capillary GC, into
isometric groupings (Table 1). Again, there were dif-
ferences in PCB composition between samples. For
example, samples from stations 22, 28, 32, and 244
were largely comprised of tri-, tetra-, and hexachloro
PCB isomers, while those from stations 107 and 27
contained significantly greater quantities of the tri-
chlorobiphenyls. Aroclor 1016 and 1242 contain pro-
portionately more of the C\l to Cl4 isomers while
Aroclor 1254 contains a greater abundance of Cl4
to Cl6 isomers. In the future, it may be possible to
ascribe the differences in the PCB composition in
animals to possible sources through capillary
GC/ECD measurements.
Highest trace metal concentrations in A. islandica
varied from metal to metal (Table 3); however, high-
est mean Ag, Cr, Cu, and Pb concentrations were
found in New York Bight (stations 26 and 29), while
Ni and Zn were highest in the "Mud Patch" (stations
181 and 237) with the highest Cd values off Dela-
ware (Table 3). Lowest concentrations, overall, were
observed at midshelf stations off New Jersey and
Maryland (with the exception of stations 167, 168,
and 123 that could have been influenced by dump-
ing at a nearby dumpsite) and station 379, on
Georges Bank. Comparison of these data with those
of Wenzloff et al. (1979), who analyzed metals in
ocean quahogs from the New York Bight to an area
off Chesapeake Bay, was attempted for temporal
trends. Unfortunately, the Wenzloff et al. (1979) data
were obtained from only foot muscle composites of
5 or 6 quahogs at each station, reported as means
of all composites per half degree of latitude; hence,
a direct comparison was not possible. The geogra-
phic pattern, a decrease in metal concentrations with
latitude believed present in the Middle Atlantic Bight
138
STEIMLE ET AL.: ORGANIC AND TRACE METALS IN OCEAN QUAHOG
by Wenzloff et al. (1979), was not apparent from the
present data or from the studies summarized in Table
4. Results of other studies involving whole body anal-
ysis (Table 4) suggest that Cd, Ni, and Zn could also
be high on Georges Bank; otherwise, the values pre-
sented do not support any consistent latitudinal
trends.
Results indicate, however, on a local level, elevated
trace metal levels were also usually associated with
known areas of inputs, eg., waste dumpsites or ad-
jacent to heavily industrialized coastal areas, such
as the New York Bight apex (station 29), or natural
depositional areas where trace metals from unknown
sources are apparently accumulating, ag, the "Mud
Patch" (stations 181, 237).
The uptake and accumulation of trace metals by
marine organisms are known to be affected by a
number of variables. These variables include season,
age, size, temperature, and interactive effects of
several metals (Phillips 1977), and can be sources of
some of the variability shown between the results
of studies in the same area. Methodology is another
source of variability between the results of each
study, especially when intercalibrated results with
standards are not available It is interesting to note
that an expected close correlation between trace
metal levels in the sediment and in A. islandica
tissues was not evident in at least one study (Rey-
nolds 1979), suggesting that the water and food or
other suspended material could be the primary
source of contaminants to this filter-feeding species.
In conclusion, a set of measurements of several
organic and seven trace metal contaminant levels in
the commercially valuable ocean quahog have been
obtained from a wide range of northwestern Atlan-
tic locations. This set can be used as a base to moni-
tor long-term changes in the assimilated levels and
distributions of these compounds in this species and
the risk to its health of future use as food. The levels
found were well below the FDA seafood action limit,
but elevated values were associated with impacted
coastal habitats and possibly waste dumpsites.
ACKNOWLEDGMENTS
This study would not have been possible without
the generous cooperation of the Northeast Fisheries
Center's Resource Survey Group, specifically Thom-
as Azarovitz, Charles Byrne, Donald Fletcher, Mal-
colm Silverman, and others, who supplied us with
the samples from annual clam assessment surveys.
We also express our thanks to John B. Pearce and
John O'Reilly for their support, and to Catherine
Noonan, Maureen Montone, and Michele Cox for
their assistance in preparing the manuscript. The
paper was improved significantly from the comments
of Donald Gadbois, Richard Greig, Carl Sindermann,
Robert Reid, and unidentified reviewers. Funding for
Table 4.— Comparison of mean trace metals levels {^g g 1 dry wt.) in Arctica islan-
dica of the northwest Atlantic.
Area and reference
Ag
Cd
Cr
Cu
Ni
Pb
Zn
Tissue type
Georges Bank-Nantucket
Sick (1978)
0.1
1.1
0.9
3.5
12.4
0.35
252
Whole body
Erco (1978)
5.1
3.9
7.6
21.0
1.00
260
Whole body
Payne et al. (1982)
4.5
1.7
5.4
27.0
3.50
150
Whole body
Present study - stn. 379
0.8
1.4
3.1
10.3
3.5
4.1
62
Whole body
Block Island Sound
Steimle et al. (1976)
1.8
31
18.0
18.0
183
Whole body
Rogerson and Galloway
(1979)1
1.4
8.1
23
11.8
10.2
138
Whole body
Present study - stn. 261
1.9
4.6
10
11.6
10.2
102
Whole body
Southern Long Island
Guarimo et al. (1979)1
3.0
5.6
17.4
27.9
14.1
122
?
Present study - stn. 189
2.5
1.9
8.8
18.7
3.3
128
Whole body
New York Bight
Wenzloff et al. (1979)1
15.8
3.5
<7.5
43.2
<5.0
9.8
107
Foot muscle
Sick (1981)
0.7
7.9
5.3
"muscle"
Present study - stn. 23,
26, 29, 32, 47
1.7
1.3
3.0
11.3
10.1
5.7
95
Whole body
Off Delaware
Reynolds (1979)
2.4
7.7
9.0
Whole body
Present study - stn. 123,
167, 168
2.4
5.7
12.4
Whole body
Chesapeak Bight
Wenzloff et al. (1979)1
9.3
3.3
<8.0
34.6
<4.7
8.5
98
Foot muscle
Present study - stn. 107
and south
1.0
2.2
2.3
5.4
11.6
4.7
71
Whole body
'Original wet weight data converted into dry weight by multiplying by 8.
139
FISHERY BULLETIN: VOL, 84, NO. 1
chemical analyses was provided, in part, by NOAA's
Northeast Monitoring Program.
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for the Thames River (Conn.) dredging project. Final Rep.
to U.S. Navy, New London, CT, Informal Rep. #110, 63 p.
NOAA, NMFS, MACFC, Sandy Hook Laboratory, Highlands,
NJ.
Thompson, I., D. S. Jones, and D. Dreibelbis.
1980. Annual internal growth banding and life history of the
ocean quahog Arctica islandica (Mollusca:Bivalvia). Mar.
Biol. (Berl.) 57:25-34.
Warner, J. S.
1976. Determination of aliphatic and aromatic hydrocarbons
in marine organisms. Anal. Chem. 48:578-583.
Weaver, G.
1982. Status report on PCB pollution in New Bedford, Massa-
chusetts. Mass. Executive Off. Environ. Aff., Boston, MA,
69 p.
Wenzloff, D. R., R. A. Greig, A. S. Merrill, and J. W. Ropes.
1979. A survey of heavy metals in the surf clam, Spisula
solidissima, and the ocean quahog, Arctica islandica, of the
Mid-Atlantic coast of the United States. Fish. Bull., U.S.
77:280-285.
140
AN ECOLOGICAL SURVEY AND COMPARISON OF
BOTTOM FISH RESOURCE ASSESSMENTS
(SUBMERSIBLE VERSUS HANDLINE FISHING) AT JOHNSTON ATOLL
Stephen Ralston,1 Reginald M. Gooding,1 and Gerald M. Ludwig2
ABSTRACT
The deep slope (100-365 m) environment at Johnson Atoll in the central Pacific was surveyed with a submer-
sible and the standing crop of commercially important bottom fishes (i.e, lutjanids, serranids, and carangids)
estimated by visual quadrat censusing. Results are compared with an assessment made by hook-and-line
fishing.
Overall, 69 species of fish were recorded from the submersible and 10 from fishing. Well over half
of the sightings from the submersible were new locality records. Bottom fish abundance estimates (fish/hec-
tare and fish/line-hour) varied by site but agreed broadly with one another. Tbgether they are used to
estimate catchability (0.0215 hectare/line-hour), which is shown to vary through the day.
Bottom fish were contagiously dispersed along both vertical and horizontal dimensions, with increased
numbers of the snapper Pristipomoides filamentosus in upcurrent localities. On a finer scale this species
and Etelis coruscans were aggregated near underwater promontories and headlands, but at different
depths.
Numerous observations concerning the deep slope environment of this central Pacific Ocean atoll
are included.
Perhaps the most widespread precept in fisheries
today is the supposition that catch rate is propor-
tional to stock abundance (Gulland 1974; Ricker
1975; Pitcher and Hart 1982). Even so, there are
numerous studies which demonstrate exceptions to
this assumption (see for example MacCall 1976; Ban-
nerot and Austin 1983). A departure from linearity
in the relationship of these two variables reflects
varying catchability. This variation may be due to
schooling behavior, gear saturation, or any number
of other factors which affect catch per unit effort
(CPUE) in addition to stock abundance (Rothschild
1977). It is often difficult, if not impossible, to
evaluate the validity of the linearity assumption in
most practical situations. A multiple approach to
stock assessment has often been suggested as a
means of circumventing this problem, including the
use of hydroacoustics (Barans and Holliday 1983;
Thorne 1983), underwater television-diver surveys
(Powles and Barans 1980), and submersibles (Uz-
mann et al. 1977) to corroborate CPUE data. Con-
sistency in results among a set of independent
assessment techniques is necessary for validation
and verification of data.
'Southwest Fisheries Center Honolulu Laboratory, National
Marine Fisheries Service, NOAA, Honolulu, HI 96812.
2U.S. Fish and Wildlife Service, Honolulu, HI 96850; present ad-
dress: Florida Fishery Research Station, U.S. Fish and Wildlife Ser-
vice, P.O. Box 1669, Homestead, FL 33030.
Submersibles in particular have also proven useful
in studying the distribution of fishes in various deep-
water habitats (Brock and Chamberlain 1968; Stras-
burg et al. 1968; Colin 1974; Shipp and Hopkins
1978), in identifying nursery grounds of commercial-
ly important rockfish species (Carlson and Straty
1981), and in assessing the effectiveness of baited
longline gear (High 1980; Grimes et al. 1982). In
many situations submersibles provide an ideal means
of independent assessment (Uzmann et al. 1977) if
questions concerning bias in visual surveys can be
adequately addressed (Colton and Alevizon 1981;
Sale and Douglas 1981; Brock 1982).
The purpose of this study was to examine the
distribution and abundance of tropical deep slope
bottom fishes (i.e, lutjanids, serranids, and carangids)
at Johnston Atoll in the central Pacific Ocean with
a research submersible and to compare the results
with an assessment made by fishing. This compari-
son provides not only a basis for testing the validity
of a CPUE statistic, but also for estimating the
catchability coefficient. Both are important issues
because of the widespread use of hook-and-line catch
and effort statistics in resource assessments of bot-
tom fish stocks worldwide (Moffitt 1980; Ralston
1980; Ivo and Hanson 1982; Ralston and Polovina
1982; Munro 1983; Forster 1984). Of special interest
was determining the relationship between CPUE
and visual estimates of bottom fish standing stock.
Manuscript accepted April 1985.
UlCirfDV DITI T ITTTTM. VOI O A M(l 1 1QOC
141
FISHERY BULLETIN: VOL. 84, NO. 1
In addition, a variety of observations made from the
submersible substantially improved our understand-
ing of factors controlling the distribution and abun-
dance of the entire deep slope fauna at Johnston
Atoll.
DESCRIPTION OF THE STUDY AREA
A National Wildlife Refuge since 1926, Johnston
Atoll is located 1,250 km southwest of Oahu, HI. The
atoll's physical environment has been reviewed by
Amerson and Shelton (1976) and is summarized
here.
Located between lat. 16°40'-16°47'N and long.
169°24'-169°34'W (Fig. 1), Johnston Atoll lies in the
North Pacific central water mass, where salinities
range from 34.8 to 35.3°/00. Surface water temper-
atures show little seasonality, ranging from 25° to
27 °C. The atoll is directly in the path of the wester-
ly flowing North Equatorial Current, with surface
currents typically 0.5 kn (0.25 m/s). Deeper layers
flow smoothly past the atoll, but an island wake
forms in lee surface waters, with effects evident up
to 600 km downstream (Barkley 1972).
The atoll is composed of a coral platform, encom-
passing over 130 km2 of reef under water <30 m
deep. A narrow lagoon lies between the northwest
barrier reef and Johnston and Sand Islands to the
southeast (Fig. 1). The atoll is unusual in that the
main outer reef extends only about one quarter of
the way around its perimeter (Fig. 1). A large por-
tion of the atoll lies exposed to prevailing easterly
weather conditions without benefit of barrier reef
protection. Evidence suggests that subsidence and
tilting of the reef platform to the southeast created
this unusual condition.
The climate is tropical marine, i.a, there is little
seasonal variation in temperature and windspeed,
but substantial variation in rainfall. A 4-mo "winter"
season extends from December to March, when
temperatures drop slightly, winds become more vari-
able, and precipitation increases. The mean annual
air temperature is 26.3 °C, with a daily range of
4.0° -4.5° C. Daily maximum and minimum temper-
169°30' W
I ^ 1
16°45'N
A-J Makalii dive sites
1-6 Cromwell fishing stations
Figure 1— Map of Johnston Atoll. The lines encircling the atoll are isobaths of constant depth (fathoms). The four shaded areas
at the upper left are emergent lands (Johnston, Akau, Hikina, and Sand Islands). Letters (A-J) indicate the 10 dive sites of the Makalii
during the study. Numbers (1-6) indicate fishing stations of the Townsend Cromwell.
142
RALSTON ET AL.: BOTTOM FISH RESOURCE AT JOHNSTON ATOLL
atures vary little throughout the year, as do sea sur-
face temperatures, which are in near equilibrium
with the air. Strong easterly trade winds prevail all
year but increase during the summer period. Annual
mean wind speed at Johnston Island is 13 kn (7.5
m/s) and monthly means range from 11 to 14 kn
(5.5-7.0 m/s).
METHODS
Makalii
The Makalii is operated by the National Undersea
.esearch Laboratory at the University of Hawaii. It
is a two-man, battery powered, 1-atmosphere sub-
mersible which is 4.8 m long, with a pressurized cap-
sule 1.5 m in diameter. When carrying a pilot and
one observer, its normal operating speeds range
from 1 to 3 kn (0.5-1.5 m/s). Maximum dive duration
is 4-5 h and depth capability is 365 m. Equipment
carried in this study included hydraulic manipulator,
internal and external color video cameras, 2 video
monitors, video recorder, video flood lights, Photo-
sea3 35 mm still camera with strobe, current and
temperature meters, and a dictaphone tape recorder.
In addition, the Makalii is equipped with an environ-
mental monitoring system for continuous recording
of temperature, salinity, conductivity, oxygen, solar
radiation, and depth.
All three authors participated as observers dur-
ing a series of dives at Johnston Atoll over the 2-wk
period between 22 September and 5 October 1983.
Once on station, a launch-recovery-transport plat-
form was submerged to 20 m and divers released the
Makalii, usually in 120 m of water. The submersible
descended until encountering the bottom and
locating the atoll's shelf break. Observations made
on fishes during the dives were voice and video re-
corded for later analysis. Slope angle was periodi-
cally measured with a hand-held inclinometer.
Visual estimates of the density of commercially im-
portant bottom fishes (sensu Ralston and Polovina
1982) were made by a series of "quadrat" samples.
These fishes included Cookeolus boops, Epinephelus
quernus, Aphareus furcatus, A. rutilans, Etelis car-
bunculus, E. coruscans, Pristipomoides auricilla, P.
filamentosus, P. zonatus, Carangoides orthogram-
mus, Caranx lugubris, Seriola dumerili, and Pon-
tinns macrocephalus.
During quadrat sampling the observer would look
out his port and count the total number of bottom
3Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
fish, without regard to species, over an area of the
bottom judged to be 30 m2. Quadrat areas always
lay on the oblique planar surface of the slope face
and were away from the immediate vicinity of the
submersible A sampling period consisted of four
counts systematically performed, one every 15 s. To
the extent possible, each count was made at an in-
stant in time. All bottom fish seen in the water
column above the sample area were included in
counts.
The submersible progressed stepwise down the
slope (100-365 m) in a clockwise direction around the
atoll, with the observer's starboard port always
oriented to the slope face. Upon reaching the
Makalii' s depth limit, a slow stepwise ascent would
begin to 100 m, where the dive would end. Descents
generally lasted 2.5 h and ascents 1.5 h. Thus the
entire vertical distribution of the deep slope was
sampled more or less equally (i.e, observations were
not concentrated in any particular depth zone).
Townsend Cromwell
The National Oceanic and Atmospheric Adminis-
tration's (NOAA) RV Townsend Cromwell is 50 m
long and when rigged for bottom handline fishing
carries four hydraulic fishing gurdies (Charlin motors
and Pacific King fishing reels), each with 365 m of
braided prestretched 90 kg Dacron line The terminal
rig is composed of four No. 28 Tonkichi round fishing
hooks and a 2 kg weight. Stripped squid was used
for bait and fishing was conducted only during the
day.
The vessel spent 3 d (3-5 November 1983) at John-
ston Atoll sampling deep slope bottom fish by drift
fishing. After wind and current directions had been
determined, the vessel was positioned over the
desired depth and fishing lines were dropped. Fish-
ing continued until the vessel drifted over an un-
suitable water depth, when lines were retrieved and
the Townsend Cromwell repositioned. Single drifts
were the fundamental sampling unit by which catch
and effort statistics were summarized. Six fishing
stations were occupied (Fig. 1), one during the morn-
ing and afternoon of each day. Fork length to the
nearest millimeter and depth of capture were re-
corded for all fish landed.
RESULTS
Makalii
Ten dives were completed at Johnston Atoll (Fig.
1). Due to precipitous dropoffs which occur through-
143
out the study area (100-365 m), the length of the
atoll's 183 m (100 fathom) isobath (64 km) provides
a convenient measure of total deep slope habitat
(Ralston and Polovina 1982). The average point-to-
point distance covered by the submersible during one
4-h dive was 2.27 km (s = 0.56 km). An aggregate
22.7 km were thus surveyed during this study, com-
prising 35% of the deep slope habitat at the atoll.
Temperature
Ambient temperature and depth were recorded
often during dives, from which temperature-depth
profiles were later constructed. The results are sum-
marized in Figure 2. The solid line represents me-
dian temperatures at depth, with the shaded area
encompassing the range of temperatures observed
among all 10 dives. Surface water temperature was
typically 27°C and the mixed layer 100 m deep. A
second weak thermocline was found around 240 m.
Although its depth varied somewhat (220-245 m), it
was present around the entire atoll, i.e., both wind-
ward and leeward exposures, and was observed as
a shimmering layer below the submersible as it
descended. This effect is believed due to refraction
of light passing through variable density water, a
result of the thermocline in association with a de-
crease in salinity.4 Ambient water temperature usual-
ly had dropped to 8.5 °C at a depth of 350 m.
Slope Angle
The relationship between the bottom's slope and
depth was also measured. These data were sum-
marized after each dive and bottom contours plot-
ted. Overall, there was little variation in slope angle
around the atoll, i.e., the general pattern was one of
uniformity at all sites visited. Figure 3 presents pool-
ed results for all slope angle-depth determinations.
In the figure, horizontal and vertical scales are equal
and the composite contour of the bottom (100-365
m) at Johnston Atoll is shown in profile. The slope
was stratified into three 50-fathom depth zones for
later analysis.5 The slope angle between 50 and 100
fathoms averages Q1 = 25° (Table 1). Similarly, 02
= 47° and 03 = 59°. There is a definite trend at
Johnston Atoll for the slope to steepen with in-
4E. Chave, Hawaii Undersea Research Laboratory, University of
Hawaii, Honolulu, HI 96822, pers. commun. June 1984.
Stratification of depth into zones was performed using units of
fathoms (1 fathom = 1.83 m) because nautical charts, hydrogra-
phic surveys, and fathometers are so measured. For the sake of
brevity and clarity, isobaths and depth strata will henceforth be
given only in this unit of measure
FISHERY BULLETIN: VOL. 84, NO. 1
Temperature - °C
10 15 20 25 30
50
100
150
E
i
Q.
0
Q
200
250
300
350
Figure 2.— The pooled relationship (w = 10) between temperature
and water depth at Johnston Atoll. Solid line = median values;
shaded area = range of values.
Table 1.— Total habitat areas stratified by depth zones at Johnston
Atoll.
Digitized
Depth
horizontal
Oblique planar
stratum
planar areas
Slope
habitat areas
(fathoms)
(ha)
angle
(ha)
Emergent lands
305(1%)
—
0-10
15,012(60%)
—
—
10-50
6,123(24%)
—
—
50-100
1 ,624 (7%)
25°
1,785
100-150
964 (4%)
47°
1,418
150-200
1 ,020 (4%)
59°
1,962
Total
25,048(100%)
—
5,165
creasing depth, at least between 100 and 365 m.
In the shallowest regions surveyed (<125 m) the
bottom was a monotonous sandy plain in the shore-
ward direction, but at 125 m it began to slope steeply
144
RALSTON ET AL.: BOTTOM FISH RESOURCE AT JOHNSTON ATOLL
downward. Although not easily seen in the figure,
a small but prominant ledge 5-10 m high encircled
the atoll between 130 and 140 m. Somewhat deeper,
between 180 and 275 m, the bottom was uniform in
slope and its surface relatively smooth and devoid
of features. Slope angles approached the vertical at
most sites in the 300-350 m depth range, with over-
hanging caves formed by subaerial dissolution.6 At
the deepest points visited (360 m) the bottom became
less precipitous, and in some areas a sediment-laden
terrace had formed along the base of the deep
dropoff.
Based on estimates of slope angle, existing charts,
and a hydrographic survey by the Townsend Crom-
well, habitat areas for the three depth zones were
determined. The positions of the 10 and 100-fathom
isobaths were already known, but they were refined
and the locations of the 50-, 150-, and 200-fathom
isobaths estimated. Figure 1 is a simplified repre-
sentation of a much larger chart which was digital-
ly analyzed to determine the horizontal (i.e., level)
areas bounded by isobaths (Table 1). The results show
that emergent lands (Johnston, Akau, Hikina, and
Sand Islands) account for only 1% (305 ha) of the
level planar area of the atoll. The largest area
(60%) lies between sea level and 10 fathoms. The
6Keating, B. H. Geologic history and evolution of Johnston
Island: Submersible dive results. Manuscr. in prep. University of
Hawaii, Honolulu, HI 96822.
total horizontal extent of the atoll is about 25,000
ha.
These results can be misleading, however, because
a vertical slope provides no horizontal habitat area,
and yet both reef fish diversity and standing crop
are known to be positively correlated with topo-
graphic relief (Luckhurst and Luckhurst 1978; Glad-
felter et al. 1980; Carpenter et al. 1981). At John-
ston Atoll the structural complexity of the sub-
stratum frequently increased with slope angle. A
better estimate of total habitat is the area of bot-
tom irrespective of slope angle, estimated by dividing
the horizontal planar area of a depth stratum by the
cosine of the slope angle within it. This adjustment
almost doubles the estimate of total habitat area in
the 150-200 fathom zone, simply due to the precipi-
tous dropoff found there. A composite 5,165 ha of
habitat occurs between 50 and 200 fathoms.
General Observations
While this study focused primarily on the deep-
water ichthyofauna of Johnston Atoll, many obser-
vations were made on the oceanographic, geologic,
and biotic characteristics of the study area. These
are briefly recounted here.
Currents running in directions parallel to the slope
were frequently encountered. They were generally
weak and did not exceed 0.3 kn (0.15 m/s). They
sometimes exhibited reversals with depth. During
100-
150-
i 200-
a
s
a
250-
300-
350-
— i 50
100
E
o
x:
O
N
150
200
Figure 3— Composite reconstruction of the deep slope at Johnston Atoll. Horizontal and vertical scales equal.
Average slope angles (0) were measured for each of three 50-fathom depth strata.
145
FISHERY BULLETIN: VOL. 84, NO. 1
dive F, for example (Fig. 1), a 0.2 kn (0.10 m/s) cur-
rent was observed at 125 m running south (i.e,
counterclockwise when viewed from above). There
was no current between 180 and 275 m. At 300 m,
however, a 0.1 kn (0.05 m/s) current was observed,
traveling in a northerly direction (i.e, clockwise). A
similar depth-related current reversal was observed
during dive C, although on this occasion the
shallower current (170 m) ran clockwise and the
deeper one (290 m) counterclockwise. In contrast,
a weak downslope current (0.1 kn or 0.05 m/s) was
observed but once (dive E at 305 m). No upwelling
currents were encountered.
Geologically, the deep slope of Johnston Atoll was
grossly similar at all points visited. The low escarp-
ment at 130 m was most likely due to erosion of an
ancient limestone reef. This feature was character-
ized by mounds of coral rubble, boulders, small
undercut caves, and a profusion of fishes. Below it
the slope angle was remarkably uniform, with low
topographic relief. The bottom was still composed
of limestone and showed severe biological and chem-
ical weathering (i.e, dissolution) along the slope gra-
dient, being pitted and striated with numerous
shallow depressions. Few sediments or boulders were
observed. At a depth of 240 m topographic relief in-
creased, as large slab boulders became increasingly
prominent. Subaerial dissolution had produced low
shallow limestone caves, and fine sediments were
more common. Between 290 and 335 m the slope was
very steep, with a well-developed system of sharp
ridges and deep erosional channels. The substratum
had the superficial appearance of dark basalt but was
composed of thin manganese crusts overlying an-
cient limestone reef materials (Keating see footnote
6). Fine sediments spilled down the channels in the
slope and piled up at the base of the deep dropoff
(350 m). More limestone boulders were arrayed along
this deep terrace and fine sediments covered the
bottom.
As expected, few fleshy macroalgae were seen. The
only algae encountered regularly were two coral-
lines, Halimeda sp. and an unidentified crustose
species. The former occurred in small scattered
clumps between 100 and 200 m, with loose remnant
exoskeletal "sands" found in sediment pockets as
deep as 290 m. The crustose form was abundant be-
tween 150 and 250 m where it covered much of the
slope face Otherwise, an unidentified species of
brown algae seen on dive H between 150 and 250
m was the only other algae seen. A more detailed
description of the algal biota at Johnston Atoll is in
preparation.7
In contrast to the depauperate flora, the inverte-
brate fauna was rich. Listed here are those forms
seen often enough to constitute indicator species for
particular depth strata. In addition to these a great
many others were observed and photographed.
In the Cnidaria, three stoney corals were especially
plentiful: Leptoseris hawaiiensis (115-165 m),
Stylaster sp. (135-245 m), and Madracis sp. (140-200
m). Several species of black corals (Order An-
tipatharia) were also common. Of the crustaceans,
a single large Panulirus marginatum, previously
known only from one specimen (Brock 1973), was
observed in a small hole during dive A at 122 m, and
at least two types of galatheid crab were very
abundant in small holes pitting the reef slope
between 230 and 350 m. In deep water the remain-
ing attached valves of dead rock oysters were seen
in patches along the base of the deep dropoff
(350 m), as was an unidentified species of solitary
tunicate (335-365 m). Echinoids were particularly
abundant immediately below the shelf break; eg,
Diadema cf. savignyi (110-170 m), Chondrocidaris
gigantea (120-160 m), and heart urchins (Brissidae,
130-200 m). Other than galatheid crabs, the 220-310
m zone was largely barren and devoid of mega-
benthos.
Ichthyofauna
A total of 69 fish species in 29 families were ob-
served during Makalii dives (Table 2). Overall, the
proportional representation of different families was
similar to that of the shallow water community
(Gosline 1955; Randall et al. in press), although the
representation of genera was grossly different. Ser-
ranid species were most numerous with nine species
observed (eight in the anthiine subfamily). Lutjanids
were also abundant (eight species), but no members
of the ubiquitous genus Lutjanus were seen. Forty
of the species listed in Table 2 (58%) are new records
for Johnston Atoll (Randall et al. in press). Photo-
graphs of several fishes observed during dives are
presented in Figure 4.
An indication of species' depth distributions is
given in Table 2. Because no observations were made
in <100 m, upper limits can be misleading. This is
particularly true of shallow-water species which
penetrated to the 135 m escarpment but not beyond,
including: Triaenodon obesus, Parapercis schau-
inslandi, Aphareus furcatus, Chromis verater, Paru-
peneus cyclostomus, P. multifasciatus, Forcipiger
flavissimus, Holacanthus arcuatus, Bodianus bilu-
7C. Agegian, University of Hawaii, Honolulu, HI 96822, pers. com-
mun. June 1984.
146
RALSTON ET AL.: BOTTOM FISH RESOURCE AT JOHNSTON ATOLL
Table 2— Fishes encountered during dives (100-365 m) of the Makalii at Johnston Atoll. Included for each species are the minimum and
maximum depths (m) of observation as well as the median and range of the depth distribution. Under the sighting column a value of
1 indicates a species was seen repeatedly (>5 times) during each dive of the submersible, 2 means the species was occasionally seen
on each dive (<5 times), 3 signifies sightings on most dives but not all (i.e., species seen on several occasions), and 4 indicates rarity
(see only once or twice during all dives). An asterisk to the left of a species name signifies a new record for Johnston Atoll (Randall et
al. in press).
Median
Median
Family-species
Min-max
(range)
Sighting
Family-species
Min-max
(range)
Sighting
Carcharhinidae
Carangidae
Carcharhinus amblyrhynchos
90-275
185(185)
1
Carangoides orthogrammus
105-170
135(65)
2
Carcharhinus sp.
Caranx lugubris
105-355
190(250)
1
(probably galapagensis)
225-250
225(25)
3
C. melampygus
130-230
135(100)
2
Triaenodon obesus
120
4
Decapterus sp.
100
4
Mobulidae
*Elagatis bipinnulata
90-150
120(60)
3
Manta sp.
120
4
'Seriola dumerili
120-335
215(215)
1
Muraenidae
Apogonidae
'Gymnothorax berndti
220-260
260(40)
3
'Epigonus sp.
330-365
355(35)
2
*G. nudivomer
120-205
1 79(85)
2
Pomacentridae
*G. nuttingi
185-300
250(115)
3
Chromis verater
120-140
130(20)
3
Ophichthidae
Mullidae
Myrichthys maculosus
150-215
185(65)
4
Parupeneus cyclostomus
125
4
Synodontidae
P. multifasciatus
125
4
Unidentified synodontid
240
4
Chaetodontidae
Holocentridae
'Chaetodon modestus
125-255
190(130)
2
'Myripristis chryseres
135-240
155(105)
2
'C. tinkeri
105-160
145(55)
3
"Neoniphon aurolineatus
150
4
Forcipiger flavissimus
125-145
130(20)
4
'Pristilepis oligolepis
165-345
230(180)
3
'Heniochus diphreutes
120-215
135(95)
2
Ophidiidae
Pomacanthidae
Brotula sp.
Geniacanthus sp.
150
4
{multibarbata or townsendi)
230
4
* Holacanthus arcuatus
130-150
135(20)
3
Priacanthidae
Labridae
'Cookeolus boops
165-260
220(95)
1
Bodianus bilunulatus
130-135
130(5)
3
Serranidae
Cheilinus unifasciatus
120
4
'Anthias fuscinus
135-280
215(145)
1
'Polylepion russelli
245-280
275(35)
3
'A. ventralis
105
4
Acanthuridae
Callanthias sp.
240-330
285(90)
4
"Acanthurus dussumieri
130
4
'Epinephelus quemus
135-350
230(215)
1
*Naso hexacanthus
120-165
150(45)
2
'Grammatonotus laysanus
310-350
335(40)
3
*Naso sp.
120-175
135(55)
1
'Holanthias elizabethae
155-260
230(105)
1
Zanclidae
*H. fuscipinnis
160-215
170(55)
1
Zanclus comutus
125
4
Luzonichthys sp.
Scorpaenidae
(perhaps earlei)
105
4
'Pontinus macrocephalus
200-365
305(165)
2
'Plectranthias helenae
215-220
215(5)
3
"Scorpaena colorata
272
4
Mugiloididae
Scorpaena sp.
225-355
290(130)
2
'Parapercis roseoviridis
215-270
245(55)
2
Triglidae
"P. schauinslandi
105-170
145(65)
1
'Satyrichthys engyceros
355-365
365(10)
4
Lutjanidae
Bothidae
Aphareus furcatus
105-145
135(40)
2
Bothus mancus
270-350
310(80)
4
"A. rutilans
190-250
220(60)
3
Balistidae
'Etelis carbunculus
245-365
310(120)
3
'Sufflamen fraenatus
105-170
140(65)
1
*£. coruscans
250-355
270(105)
3
Xanthichthys auromarginatus
115-155
135(40)
1
* Pristipomoides auricilla
215-250
230(35)
3
Monacanthidae
'P. filamentosus
120-260
205(140)
3
Unidentified monacanthid
125
4
'P. zonatus
205-295
240(90)
1
Tetraodontidae
* Symphysanodon maunaloae
230-365
300(135)
1
"Canthigaster sp.
Emmelichthyidae
(likely inframacula)
260-270
265(10)
4
'Erythrocles scintillans
295-320
300(25)
4
Unidentified tetraodontid
Ostraciidae
Ostracion sp.
Diodontidae
Diodon hystrix
135-150
145(15)
135
135
4
4
4
nulatus, Acanthurus dussumieri, Zanclus comutus,
Xanthichthys auromarginatus, and Diodon hystrix.
These fishes accounted for an increase in diversity
at the 135 m dropoff. Similarly, due to the submer-
sible's 365 m depth limit, lower bounds for some
species are likely in error (eg., Symphysanodon mau-
naloae, Epigonus sp., Pontinus macrocephalus, and
Satyrichthys engyceros). Nonetheless, due to the
large depth range sampled (100-365 m), the data still
provide useful estimates of the depth distributions
for most of the species listed.
The data suggest that large species have great
147
FISHERY BULLETIN: VOL. 84, NO. 1
148
RALSTON ET AL.: BOTTOM FISH RESOURCE AT JOHNSTON ATOLL
depth ranges. For example, all species with depth
ranges exceeding 200 m are large (i.e, Caranx lugu-
bris, Epinephelus quernus, and Seriola dumerili).
Moreover, among extensively observed species, a
significant Spearman correlation exists between
ranked average weight and depth range (rs = 0.52,
df = 25, P < 0.01). This finding should be viewed
with caution because of potential biases in depth
distributions (see above).
The last column in Table 2 gives sighting scores
for all species. Those assigned a value of 1 indicate
species dominating the deep slope fish community
in terms of species sightings. Note that some species
were seen infrequently, but when encountered they
were observed in large numbers (eg, Elagatis bipin-
nulata, Fig. 4). Similarly, Pristipomoides filamen-
tosus was not seen on every dive and was thus as-
signed an abundance score of 3. In spite of this, when
seen, it was abundant and it was the most frequent-
ly caught while fishing (see next section). Sighting
scores therefore do not indicate relative species' con-
tributions to total standing crop biomass of the deep
slope fish fauna.
Quadrat Sampling
A total of 974 quadrat sample counts were made
during the 10 submersible dives. No attempt was
made to estimate abundance separately for each
species. Rather, the total number of bottom fish was
recorded, regardless of species composition. Al-
though severely reducing the detail of the data base,
this did have the desirable effect of averaging biases
due to attraction or repulsion of fishes to and from
the Makalii. It was evident, for example, that some
species were attracted to the submersible and follow-
ed it about (e.g., Seriola dumerili and Caranx lugu-
bris), whereas others were repelled and actively
avoided the submersible's lights (eg., Pristipomoides
filamentosus and Etelis coruscans). Still others did
not seem to be greatly influenced (eg., Cookeolus
boops, Epinephelus quernus, Pristipomoides zonatus,
and Pontinus macrocephalus). By pooling species
quadrat counts, the abundance of some species was
overestimated, some underestimated, and some
estimated without bias. Due to averaging, we believe
that pooled counts provide the best available
Figure 4— Johnston Atoll deep slope fishes. A. Caranx lugubris
with wire coral; B. Epinephelus quernus peering out of cave; C.
Seriola dumerili (foreground) and Caranx lugubris (background);
D. school of Elagatis bipinnulata with Carangoides orthogrammus
(above); E. Heniochus diphreutes with black coral; and F. aggrega-
tion of Myripristis chryseres and Neoniphon aurolineatus.
estimates of total bottom fish density along the deep
slope of Johnston Atoll.
Some 367 bottom fish were counted in quadrat
samples, resulting in a mean encounter rate of 0.38
fish/quadrat. The data were fitted to the Poisson
distribution to ascertain the dispersion pattern. A
chi-square goodness of fit test yielded x2 = 325.32,
df = 3, P « 0.005, demonstrating nonrandom dis-
persion. The variance to mean ratio calculated from
the frequency distribution of bottom fish/quadrat
observations was 4.64 and was significantly greater
than 1 (P « 0.005), indicating strong contagion.
One of the principal explanations for this result
is shoaling by Pristipomoides filamentosus and Ete-
lis coruscans. Both are large species, which formed
aggregations of up to 100 individuals well off the bot-
tom (20 m) in the vicinity of underwater headlands
and promontories. These monospecific groups ap-
peared to feed in open water on plankton, consis-
tent with previous dietary studies of P. filamentosus
(Kami 1973; Ralston8). When either was observed,
there was an increased likelihood of encountering
conspecifics. As a consequence 10 or more P. fila-
mentosus were seen in one quadrat on 7 occasions.
Another factor contributing to clumping was non-
random distribution with depth (Fig. 5). This figure
presents the relationship between mean number of
bottom fish per count and depth (vertical bars =
standard errors). Note the two abundance peaks, the
first at about 170 m and the second at 250 m. The
former was due primarily to large numbers of
Caranx lugubris and P. filamentosus. The location
of the second peak was just below the second
thermocline and was largely the result of local in-
creases in numbers of Epinephelus quernus and P.
zonatus.
The mean numbers of bottom fish per quadrat,
stratified into 50-fathom depth intervals, are also
shown in Figure 5 (i.e, 0.57, 0.47, and 0.06 fish/count).
These data were converted to densities (1 quadrat
= 0.003 ha) such that from 50 to 100 fathoms an
average of 190 bottom fish are estimated to occur
per hectare of habitat. Similarly, in the two deeper
strata, estimated densities of 156 and 20 bottom
fish/ha occur.
Given estimates of bottom fish density and depth-
specific estimates of total available habitat (Table 1),
estimates of the total standing crop of bottom fishes
at Johnston Atoll indicate that about 339,000 fish
occurred in the 50-100 fathom zone, 221,000 between
"Ralston, S. Unpubl. data. Southwest Fisheries Center Hono-
lulu Laboratory, National Marine Fisheries Service, NOAA, Hono-
lulu, HI 96812.
149
1.1-1
1.0-
0.9-
~ 0.8
•o
^ 0.7
i °6
o
o 0.5
n
o 0.4
c
a
T3
% 0.3
<
0.2
0.1 H
0.0
FISHERY BULLETIN: VOL. 84, NO. 1
200
50
— I —
100
— I —
150
T
200
Depth
250
— I —
300
350
400
[ml
Figure 5— The abundance of bottom fish (see text) in relation to depth. Solid line represents
fish densities with changing depth (measured in meters or fathoms). Error bars are standard
errors of means. Three 50-fathom depth zones are indicated, and mean fish densities within
these are shown as circled points.
100 and 150 fathoms, and only 39,000 in the deep-
est (150-200 fathom) zone. Roughly 600,000 com-
mercially exploitable bottom fish are estimated to
comprise the deep-sea hook-and-line resource at
Johnston Atoll. Because the fish are spread over a
total habitat of 5,165 ha (Table 1), this corresponds
to average densities of 118 bottom fish/ha.
Townsend Cromwell
Anywhere from 2 to 4 lines were deployed while
fishing, resulting in an aggregate 41.8 line-h of
fishing effort spread over 23 vessel drifts. A catch
of 133 fishes (Table 3) produced an overall CPUE of
3.18 fish/line-h. Another 12 fish were hooked but lost
to sharks before landing. All species caught while
fishing were observed from the submersible with the
exception of the bramid, Eumegistus illustris. Deep-
water lutjanids predominated (69%), but substantial
numbers of serranids (22%) and carangids (8%) were
caught, a composition typical of tropical deep slope
fisheries worldwide (Talbot 1960; Ralston and Polo-
vina 1982; Munro 1983; Forster 1984).
Species Composition By Location
Examination of catch data suggested a difference
in species composition between upcurrent (sites 5
Table 3. — Species composition of the bottom fish catch from the
Townsend Cromwell at Johnston Atoll.
Family-species
Catch
Percent
Average
size
(cm FL)
Lutjanidae (snappers)
Pristipomoides filamentosus
P. zonatus
P. auricilla
Etelis carbunculus
E. coruscans
43
35
5
5
4
32
26
4
4
3
54.4
40.8
34.6
51.2
72.7
Subtotal
92
69
Serranidae (groupers)
Epinephelus quernus
29
22
69.8
Carangidae (jacks)
Caranx lugubris
Carangoides orthogrammus
Seriola dumerili
7
2
2
5
2
2
48.1
43.5
79.5
Subtotal
11
9
Bramidae (pomfrets)
Eumegistus illustris
1
1
70.3
Grand total
133
101
and 6) and downcurrent (sites 1-4) locations (Fig. 1).
Landings were pooled into these two classes, and al-
so by species category into Pristipomoides filamen-
tosus, P. zonatus, Epinephelus quernus, and "others".
The resulting 2x4 contingency table showed a lack
of statistical independence between locations and
species (x2 = 22.36, df = 3, P « 0.005). Examin-
150
RALSTON ET AL.: BOTTOM FISH RESOURCE AT JOHNSTON ATOLL
ing individual contingency table cells showed that
the greatest contribution to the total chi-square was
for P. filamentosus (58% of total). Specifically, under
the hypothesis of independence, 16.5 were expected
downcurrent but only 5 were caught, while 26.5 were
expected upcurrent where 38 were landed. The ap-
parent surplus of P. filamentosus along the eastern
exposure, where trade winds prevail and oceanic cur-
rents first impact the atoll (Barkley 1972), may relate
to this fish's habit of feeding on large deepwater
plankton, especially salps (genus Pyrosoma). Bray
(1981) has shown that small resident planktivores
will travel to the upcurrent edge of a reef to access
pelagic plankton. The distribution of P. filamentosus
at Johnston Atoll may represent a similar situation
on a much larger scale.
Bottom Fish Catch Rate
One-way analysis of variance (ANOVA) of CPUE
data was used to examine whether geographical dif-
ferences exist in bottom fish abundance, i.e, the two
treatment classes were upcurrent and downcurrent
regions (see above). The ANOVA was insignificant
(F = 1.62, df = 1, 21, P = 0.21), although the mean
catch rate along the eastern exposure (5.6 bottom
fish/line-h) was 60% greater than downcurrent (3.5
bottom fish/line-h). This result suggests the lack of
significance may have been due to small sample size
The CPUE data were analyzed by time of day to
determine if catchability fluctuates through the day.
The results in Figure 6 show that fishing was
distinctly better during the morning than afternoon.
In this figure individual values of drift CPUE (n =
23) have been plotted against the midpoint of the
drift time interval. The solid line represents aggre-
gate catch rates, calculated by pooling both catch and
effort statistics from all areas into 1-h intervals and
then forming CPUE ratios. Different symbols repre-
sent each of six separate fishing locations (Fig. 1).
Note that catch rates were highest when fishing
began each day and consistently declined to a low
during the midafternoon. The data further indicate
that catch rates may increase again with the onset
of the evening crepuscular period, although the data
are meager. This pattern was evident both within
and among the six sites fished and, when averaged
out, resulted in morning catch rates 2.07 times
greater than afternoon rates.
Catchability
Having the Makalii and Townsend Cromwell at
Johnston Atoll at similar times prompts comparison
15 -i
10
Q.
(J
5-
O-1
I 1 1 1 1 1 1 1 1
0800 1000 1200 1400 1600
Time of Day
Figure 6.— The effect of time of day on the catch rate of bottom
fish at Johnston Atoll. Catch rates calculated for each drift of the
vessel and presented for each of six different fishing stations (see
Figure 1).
of the assessment techniques. We assume that in the
1-mo interim between visits no changes occurred in
overall levels of abundance, because Johnston Atoll
is a National Wildlife Refuge where no fishing is per-
mitted and the fishes are typically long lived (Ralston
and Miyamoto 1983; Ralston see footnote 8). Any
differences in assessment are then likely due to dif-
ferences in method.
To compare surface estimates of bottom fish abun-
dance with those derived from submersible surveys,
we matched fishing stations (numbers) with submer-
sible dives (letters) which occurred nearby (Fig. 1).
Specific pairings were F-l, E-2, B-3, H-4, 1-5, and D-6.
For each dive the overall abundance of bottom fish
was estimated by forming the ratio of total fish
counted to total number of quadrat counts, and then
converting to density measured in bottom fish/ha.
The CPUE statistics were used to estimate abun-
dance for each fishing station, after correcting for
fluctuating catchability (Fig. 6). The result is pre-
sented in Figure 7. There is a positive correlation
between CPUE and bottom fish density (r = 0.54),
although it is insignificant.
One means of estimating catchability, q, is to deter-
mine the slope of the regression of CPUE on stock
density. We estimated the functional regression
(Ricker 1973) of the data presented in Figure 7 (solid
line) and determined that q = 0.0215 ha/line-h. A
second estimate of q is obtained by forming the ratio
of the average catch rate of bottom fish at the atoll
151
FISHERY BULLETIN: VOL. 84, NO. 1
8-1
6-
a, 5_
4 -
3
al
2 -
1 -
~ I 1 1 1 I
50 100 150 200 250
Abundance I f ish / ha I
300
Figure 7— The relationship between Townsend Cromwell CPUE
and Makalii abundance estimates. Line fitted by functional regres-
sion. See text for further discussion.
(3.18 fish/line-h) to the average density of bottom fish
viewed from the submersible (118 bottom fish/ha).
The resulting estimate of q is 0.0269 ha/line-h.
DISCUSSION
The most enlightening aspect of this study was our
ability to perform an in situ assessment of factors
controlling the distribution and abundance of the
deep slope biota at Johnston Atoll. Organisms
showed not only distinct zonational patterns with
depth but clumped dispersion along horizontal
gradients as well.
The fish fauna of Johnston Atoll is often con-
sidered a depauperate outlier of the Hawaiian fauna
(Gosline 1955; Randall et al. in press). In a later
paper, Gosline (1965) examined vertical zonation in
Hawaiian fishes, arguing that depth zonation pat-
terns are often sharply demarcated in intertidal and
shallow-water habitats, but these become increasing-
ly attenuated with depth. The results of our study
and Randall et al. (in press) support his conclusion
(see also Forster 1984). Some deep slope species have
extremely broad depth ranges (exceeding 200 m), yet
few representatives of the shallow-water communi-
ty extend appreciably beyond the 130 m escarpment
encircling the atoll. Other investigators have noted
that many Hawaiian species, which are commonly
thought of as strictly associated with coral reefs,
penetrate to depths well in excess of those favoring
the growth of scleractinian corals (Brock and Cham-
berlain 1968; Strasburg et al. 1968; Clarke 1972). Yet
the distributions of these fishes are limited largely
to areas near the shelf break or shallower, while a
true deep slope ichthyofauna, comprised largely of
anthiids and lutjanids, exists along outer reef drop-
offs at both Johnston Atoll and in the Hawaiian
Islands.
Distributional patterns of fishes were nonrandom
along horizontal gradients as well, as was readily ap-
parent in the atoll-wide distribution of Pristipo-
moides filamentosus . Based simply on catch totals,
60% more P. filamentosus were expected to occur
on the upcurrent exposure of the atoll than down-
current, although 760% more were observed there,
illustrating the clumped dispersion pattern which
characterized this species during fishing surveys.
Contagion was also evident in quadrat samples.
Future studies would be well advised to incorporate
statistical models consistent with these findings, in-
cluding use of the negative binomial distribution to
describe spatial patterns.
On a more local scale, it was clear from submer-
sible observations that P. filamentosus and Etelis cor-
uscans were concentrated near underwater head-
lands. Brock and Chamberlain (1968) made similar
observations on deepwater populations of Chaetodon
miliaris, attributing the very localized distribution
of this species to increased accessibility of its food
(plankton) in the vertical turbulence plumes formed
by the impact of currents on underwater prom-
ontories. Because of its known planktivorous food
habits, this hypothesis could explain abundance pat-
terns of P. filamentosus. Moreover, fishermen empha-
size the importance of currents in locating feeding
aggregations of both P. filamentosus and E. cor-
uscans. These two species taken together comprise
the most important species landed in the Hawaiian
deep-sea hook-and-line fishery, both in terms of yield
and economic value. The relative abundance of these
species in the deepwater bottom fish community may
be due to their utilization of an allochthonous plank-
ton resource transported to neritic waters from the
open sea.
Bottom Fish Abundance
Certain methodological problems hindered this
study and should be reviewed before comparing the
abundance estimates from the two surveys. Any
technique, including those used here, has its own spe-
cific combination of advantages and disadvantages.
There is ample reason to suspect bias in assess-
ments based on underwater visual surveys. Sale and
Douglas (1981) have shown that a single visual fish
152
RALSTON ET AL.: BOTTOM FISH RESOURCE AT JOHNSTON ATOLL
census seldom records all individuals present at the
time of the census. Similarly, Colton and Alevizon
(1981) showed that a quarter of the community they
studied was characterized by significant diurnal
changes in abundance. They concluded that unless
sampling time is carefully controlled and standard-
ized, results from visual abundance surveys may be
seriously biased. Standardization was achieved in this
study because all 10 dives started between 0840 and
0950 in the morning and each lasted 4 h. Further-
more, Brock (1982) showed that large, conspicuous,
diurnally active species are accurately censused with
visual assessment techniques, although the most
abundant are often underestimated. With the excep-
tion of Cookeolus boops, which, although nocturnal,
shelters in the open along the slope face, all of the
species included in the quadrat sampling fit these
criteria. Biases which frequently accompany visual
assessments have thus been considered and mini-
mized here
Another factor which may have affected the results
of Makalii surveys is attraction and repulsion of cer-
tain species to and from the submersible Previous
investigators have typically ignored this problem (Uz-
mann et al. 1977; High 1980; Powles and Barans
1980; Carlson and Straty 1981), while at the same
time acknowledging that some species are attracted
(ag, black sea bass, southern porgy Pacific halibut,
sculpin, and yelloweye rockfish) or repelled (eg,
squid, herring, mackerel, butterfish, and wolf eel) to
submersibles and divers. Nevertheless, as pointed out
by Uzmann et al. (1977), one can at least observe the
reactions of species to the submersible's presence,
giving the viewer the opportunity to evaluate poten-
tial sources of error. We have attempted to address
this problem by pooling counts for all species. While
admittedly this procedure may not remove all bias,
it is our feeling that in the absence of more quan-
titative information, little else can be done to im-
prove the data. Studies are now being implemented
to specifically evaluate the degree of attraction or
repulsion of different species to the Makalii.
Provided an awareness of these concerns, the
results presented here support the contention that
the catch of bottom fish/line-h is a suitable CPUE
statistic This conclusion is based on the data pre-
sented in Figure 7, where CPUE generally increases
with fish density and the regression intercept passes
close to the origin. Although the relationship is
statistically insignificant, this is likely due to small
sample size (n = 6). Moreover, differences in bottom
fish abundance between upcurrent and downcurrent
locations were shown to result largely from the con-
tagious dispersion of Pristipomoides filamentosus
along the eastern side of the atoll, where its primary
food resource first becomes available for consump-
tion.
The estimation of catchability for deep-sea hook-
and-line gear is a useful application of the dual sam-
pling program presented hera The results suggest
relatively great sensitivity of bottom fish stocks to
exploitation pressure, a finding consistent with pre-
vious and ongoing studies (Ralston 1984). If we use
q = 0.0215 ha/line-h as an estimate of catchability,
we conclude that 1 line-h of Townsend Cromwell fish-
ing effort removes about 2.2% of the bottom fish
inhabiting 1 ha of habitat. A similar finding was
reported by Polovina9, who estimated q from the
same vessel for a Mariana stock of bottom fish. Re-
movals such as this are not insubstantial and under-
score the importance of developing methods of stock
assessment which can be used early in the develop-
ment of a fishery and in the absence of conventional
data sources. A combination of surface platform
surveys with submersible ground-truthing is certain-
ly a promising assessment technique to pursue (Uz-
mann et al. 1977).
ACKNOWLEDGMENTS
We would like to thank the U.S. Army Corps of
Engineers Pacific Ocean Division, the U.S. Army
Toxic and Hazardous Materials Agency, and the Na-
tional Undersea Research Program at the Univer-
sity of Hawaii for making this study possible Special
thanks go to the staff of the Hawaii Undersea Re-
search Laboratory Program and the Makalii opera-
tions crew for help in coordinating the dive program
and in meeting our needs for logistical support.
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1980. An analysis of the Hawaiian offshore handline fishery:
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155
PATCHINESS AND NUTRITIONAL CONDITION OF ZOOPLANKTON
IN THE CALIFORNIA CURRENT
Stewart W. Willason, John Favuzzi, and James L. Cox1
ABSTRACT
Zooplankton and water samples were collected from 81 stations off the California coast in April 1981
during CalCOFI cruise 8104 aboard the RV David Starr Jordan. Abundance, weight (wet and dry),
digestive enzyme activity (laminarinase), and biochemical composition of three zooplankton species were
determined. The indices measured provided estimates of zooplankton nutritional history on time scales
of 1 day to 3 weeks.
Upwelling was taking place along the California coast, from Point Conception to San Francisco dur-
ing the study period. The resulting low surface temperatures were most evident south of San Francisco
and just north of Point Conception. Just south of these areas patches of high phytoplankton standing
crop (up to 14.7 mg chlorophyll a/m3) were found. The two herbivorous species, Euphausia pacifica and
Calanus pacificus, showed highest laminarinase activity in areas with the highest density of phytoplank-
ton: enzyne activity was particularly high in the waters off Point Conception. Zooplankters in the southern
and offshore regions of the sampling grid showed very low digestive enzyme activity. The larger size (weight)
and higher lipid content of C. pacificus near Point Conception and south of San Francisco in comparison
to animals in other parts of the California Current suggest that animals in these areas experience pro-
longed periods of better nutrition. Nematoscelis difficilis, which is not a herbivore, did not show these
patterns. This study illustrates the importance of upwelling regions, such as Point Conception, and shows
the large spatial variability of trophic interactions within the California Current System.
The nearshore, pelagic marine environment is ex-
tremely variable and heterogeneous. Spatial hetero-
geneity of physical conditions elicit behavioral or
physiological responses from marine organisms
which contribute to biological patchiness (Haurey et
al. 1978; Steele 1978). Patchiness of pelagic marine
organisms occurs on all temporal and spatial scales
(Haury et al. 1978); one of the most important of
these is the mesoscale (a few kilometers to 100's of
kilometers, and a few weeks to months). Mesoscale
processes, such as coastal upwelling, play a major
role in structuring the physical and biological en-
vironment at all scales (Haury 1982). Although up-
welling regions are very productive (eg., Ryther
1969), trophic interactions within these important
areas are poorly understood.
Along the California coast episodic upwelling takes
place during the spring and summer months (Reid
et al. 1958; Bernstein et al. 1977; Owen 1980; Lasker
et al. 1981; Parrish et al. 1981). Upwelling results
in mesoscale phytoplankton patchiness along the
coast and in the southward flowing California Cur-
rent (Owen 1974; Cox et al. 1982; Smith and Baker
1982; Pelaez and Guan 1982). It is thought that phy-
toplankton patchiness in this area influences the sur-
^arine Science Institute, University of California, Santa Bar-
bara, CA 93106.
vival and physiological condition of larval fish popula-
tions (Lasker 1975; Lasker and Smith 1977; Lasker
and Zweifel 1978; O'Connell 1980). In addition, nutri-
tion of herbivorous zooplankton (estimated by diges-
tive enzyme activity) is influenced by phytoplankton
patchiness (Cox et al. 1982; Cox et al. 1983; Willa-
son and Cox in press).
This study investigates the impact that mesoscale
and larger scale phytoplankton patchiness have on
zooplankton populations within the California Cur-
rent along the central and southern California coast.
Results of measurements of temperature, phyto-
plankton biomass, zooplankton abundance, and zoo-
plankton nutrition are presented. Nutritional status
was evaluated using intrinsic properties which reflect
previous feeding conditions. Short-term feeding his-
tory was estimated from measurements of the acti-
vity of the digestive enzyme, laminarinase Although
digestive enzyme levels of zooplankton do not always
provide a good measure of instantaneous digestive
or feeding rates (Hassett and Landry 1983; Head
et al. 1984; Willason and Cox in press), the level of
activity in field captured animals does give an indica-
tion of relative feeding history on the order of 1 to
5 d (Cox 1981; Cox and Willason 1981; Cox et al.
1983; Willason 1983). Longer term nutritional con-
dition was assessed from biochemical composition
and animal size (wet and dry weight) measurements.
Manuscript accepted April 1985.
FTSWRRV RTTT.T.F.TTN- VDT . RA NO 1 1 QRfi
/r* -/?4
157
FISHERIES BULLETIN: VOL. 84, NO. 1
Lipid content, size, and water content of a zooplank-
ton species reflect feeding history on the order of
1 to 3 wk (Omori 1970; Lee et al. 1970, 1971; Bam-
stedt 1975; Childress 1977; Boyd et al. 1978; Vidal
1980; Hakanson 1984). Spatial patterns derived from
these data are used to estimate relative differences
in feeding and nutritional condition of zooplankton
from different areas within the California Current.
An understanding of the interrelationships of these
variables in different areas may provide insights in-
to mechanisms which generate and maintain physical
and biological mesoscale features.
METHODS
Species Studied
Two euphausiid species, Euphausia pacifica Han-
sen and Nematoscelis difficilis Hansen, and the
copepod, Calanus pacificus Brodsky were chosen for
the present study because 1) all are common in the
California Current region (Fleminger 1964; Brinton
1967b), 2) all have been used in previous digestive
enzyme studies (Cox 1981; Cox and Willason 1981;
Hassett and Landry 1982, 1983; Cox et al. 1983;
Willason 1983; Willason and Cox in press), and 3)
a large base of information exists on the sizes,
feeding rates, and energetics of these zooplankters
(Brinton 1967a; Mullin and Brooks 1976; Vidal 1980;
Ross 1982; Cox et al. 1983; Torres and Childress
1983; Willason 1983; Hakanson 1984; Willason and
Cox in press). Euphausia pacifica, the most abun-
dant euphausiid in the California Current (Brinton
1967b; Brinton and Wyllie 1976; Youngbluth 1976),
and C. pacificus, the most abundant copepod along
the California coast (Fleminger 1964; Star and
Mullin 1981), are considered primarily herbivorous
(Mullin and Brooks 1976; Ross 1982; Willason and
Cox in press). By contrast, N. difficilis does not ap-
pear to be a herbivore (Nemoto 1967; Mauchline and
Fisher 1969; Willason and Cox in press).
Sample Collection
The sampling program was conducted off the Cali-
fornia coast from 7 to 27 April 1981 in conjunction
with the California Cooperative Fisheries Investiga-
tion (CalCOFI) survey. Zooplankton and water sam-
ples were collected from 81 stations during CalCOFI
cruise 8104 aboard RV David Starr Jordon. Figure
1 shows the stations sampled and the sampling se-
quence during the cruise. The grid covered an area
of about 270,000 km2; nearshore stations were
sometimes within 1 km of the coast and offshore
stations were located up to 300 km from the
coast.
Although the mean flow of the California Current
is south through the sampling grid at this time of
the year (Lynn et al. 1982), smaller regions within
the grid are often subjected to different hydro-
graphic influences. For example, the waters of the
offshore regions intergrade with the waters of the
Central Pacific Gyre (Bernstein et al. 1977); the
nearshore region south of Point Conception (the
Southern California Bight) is characterized by a
semipermanent, counterclockwise eddy and is hydro-
graphically distinct from the other areas of the grid
(Owen 1980); and the nearshore area adjacent to and
north of Point Conception is characterized by periods
of intense coastal upwelling during the spring and
summer months (Parrish et al. 1981). To compare
the biological and nutritional properties of zooplank-
ton in the different hydrographic regions, the sam-
pling grid was divided into four sections: southern
nearshore (I), northern nearshore (II), southern off-
shore (III), and northern offshore (IV) (Fig. 1).
Surface chlorophyll a concentration (depth of 2 m)
was used as an indicator of phytoplankton standing
crop. Previous studies have shown that there are
positive correlations between surface chlorophyll a,
integrated chlorophyll a, and primary production in
the waters of the California Current (Lorenzen 1970;
Hayward and Venrick 1982). Measurements of sur-
face chlorophyll a, therefore, give a relative approx-
imation of phytoplankton biomass within the sam-
pling grid.
Two replicate water samples (0.25 to 2.0 L) for
chlorophyll a analysis were taken at each of the 81
stations from a depth of about 2 m using the ship's
seawater pumping system. Each sample was filtered
through a 4.5 cm Whatmann GF/C filter; two drops
of a seawater-saturated MgC03 solution were add-
ed during filtrations. The filters were folded in half
and stored frozen in aluminum foil at -20°C. An
additional 15 water samples were taken for chloro-
phyll a analysis along the cruise track adjacent to
and immediately south of the Point Conception
region while the ship was under way. Measurements
of surface water temperature (±0.1°C) were also
taken at each station using a glass mercury thermo-
meter.
Paired bongo nets (designated net 1 and net 2) with
mouth openings of 0.396m2 and mesh openings of
505 ptm were used for the collection of zooplankton
samples. A General Oceanics2 flowmeter was mount-
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
158
WILLASON ET AL.: ZOOPLANKTON IN CALIFORNIA CURRENT
I Southern Nearshore
II Northern Nearshore
III Southern Offshore
IV Northern Offshore
San
Francisco
~&Sjii: Monterey Bay
II J
\ >
v oj £///. Point Conception
San
Diego
38c
36(
34°
32°
124<
122<
120°
118'
Figure 1.— Sampling grid. Open circles are day stations and closed circles are night stations.
Arrows show the sampling sequence The first station, adjacent to San Diego, was occupied on
7 April 1981. The last station, just north of San Francisco, was occupied on 27 April 1981.
ed inside the mouth of each net to measure the
volume of water filtered. An oblique net tow was
made to a depth of about 210 m at each station (bot-
tom depth permitting); each net filtered about 400
m3 of water. Ship speed during the net tows was 1.5
to 2.0 kn. Thirty-six stations were occupied at night
(after sunset and before sunrise) and 45 were oc-
cupied during the day.
The euphausiids, Euphausia pacifica and Nema-
toscelis difficilis, and the copepod, Calanus pacificus,
were separated from the catch of net 1 immediately
after collection. Adult euphausiids were sorted for
males and females and copepods sorted for females
and stage V copepodites. Specimens of E. pacifica
and N. difficilis were considered adults if they were
larger than 11 mm and 15 mm, respectively (Brin-
ton and Townsend 1981). Fifty undamaged animals
of each species and sex (or stage) were saved from
each net tow if adequate numbers were captured. For
C. pacificus, which were very abundant, 50 females
and stage V's were saved from 72 and 75 of the 81
stations, respectively. Two replicate groups of 50
females of C. pacificus were taken from 7 stations
and two replicate groups of 50 stage V copepodites
from 9 stations. After sorting, animals from each
net tow were wrapped in parafilm in groups (5 to
50 animals of each sex or stage) and frozen at -20°C
for biochemical analyses in the laboratory. Catches
from net 1 that could not be sorted on the ship (10
of the 81 stations sampled) were frozen whole at
-20°C and sorted in the laboratory after the cruise.
The entire catch of net 2 was preserved in Formalin
immediately after collection.
The abundances (numbers per 1,000 m3) of adult
euphausiids at each station were estimated by count-
ing all adults captured in net 1 and dividing by the
volume of water filtered. Copepod abundances (num-
bers per 1 m3) were estimated by counting all
159
FISHERIES BULLETIN: VOL. 84, NO. 1
females and stage V copepodites in triplicate aliquots
taken from the preserved catches of net 2.
Sample Analyses
All frozen samples were analyzed in the laboratory
within 6 wk of the time of collection. Plant pigments
were extracted from the filters in 90% acetone in
darkness at 4°C for 48 h. Chlorophyll a concentra-
tion was determined by the method of Strickland and
Parsons (1972) using a model 10-005 Turner Designs
fluorometer. The two chlorophyll a measurements
from each station were averaged.
Groups of frozen animals (separate species and
sexes) were thawed in the laboratory, blotted lightly
to remove excess water, and weighed (±0.01 mg).
Animals were then freeze-dried for 24 h at -50°C
and reweighed. Groups were then immediately
ground in cold (4°C) succinic acid buffer (pH 5.0)
using a Polytron grinder (for euphausiids) or a hand
glass tissue grinder (for copepods). Homogenates
were analyzed for total proteins by the Lowry
method using Sigma protein standard (Merchant et
al. 1964). Laminarinase activity (LA) of the homo-
genates was determined by the methods described
by Cox (1981) and Willason (1983). LA was expressed
as a function of the animal's wet weight: yg glucose
produced per gram wet weight per minute of incu-
bation. Copepod homogenates were also analyzed for
total lipids using stearic acid as the standard (Bligh
and Dyer 1959; Marsh and Weinstein 1966).
Data Analysis
Willason and Cox (in press) found that E. pacifica
exhibits a diel rhythm in enzyme activity associated
with feeding activity at night. Thus, to compare LA
of E. pacifica collected at different times of the day
from different localities, enzyme levels had to be
standardized with respect to the time of capture.
Calibration factors, which convert the LA of E.
pacifica collected at different times to a standardized
maximum value (between 0200 and 0800 h), were
derived from the results of the 24-h time-series col-
lections in Willason and Cox (in press). These fac-
tors are based on the average relative increases and
decreases of enzyme activity over a 24-h period
(Table 1). LA of AT. difficilis and C. pacificus do not
show diel changes (Cox et al. 1983; Willason and Cox
in press) and, therefore, were not standardized.
The data set for each station consists of surface
temperature, surface chlorophyll a, zooplankton
abundance, LA, individual wet and dry weights, pro-
tein content, and lipid content (copepods only). To
permit parametric statistical comparisons between
the various biological and physical properties and
between regions, chlorophyll a, zooplankton abun-
dance, and zooplankton LA were normalized by log
transformation. The log transformed values were
used for all parametric statistical tests. Zooplankton
wet weight, dry weight, protein content, and lipid
content were found to be normally distributed by
probit analysis and were not log transformed. Non-
transformed values from all data sets were used to
construct contour maps. The contour maps are in-
tended to show general trends and patchiness within
the sampling grid.
Table 1.— Correction factors for standard-
izing laminarinase activity (LA) of Euphausia
pacifica. These factors account for diel
changes in LA and are based on the time
of capture. They were derived from the 24-h
time-series collections of Willason and Cox'.
LA was standardized to the 0200-0800 time
period. LA of euphausiids captured during
other time periods was multiplied by the
corresponding factor.
Correction
factor
Time period
Females
Males
2000-0200
0200-0800
0800-1400
1400-2000
1.042
1.000
1.253
1.486
1.132
1.000
1.281
1.453
'Willason, S. W. and J. L. Cox. In press. Diel
feeding, laminarinase activity and phytoplankton
consumption by euphausiids. Biol. Oceanogr.
RESULTS
Surface Water Temperature and
Surface Chlorophyll a
Surface water temperatures along the California
coast during April 1981 ranged from 9.6° to 16.0°C.
The coldest water was located in the northern near-
shore region and the warmest was found in the
southern offshore region (Table 2, Fig. 2). Two small
areas showed very low surface water temperatures:
close to the shore along the central coast of Califor-
nia and just off San Francisco Bay (Fig. 2). A cold
water plume extended from Point Conception south
into the Southern California Bight.
Chlorophyll a concentrations showed greater than
100-fold variation between stations and were inverse-
ly correlated with surface water temperatures (r =
0.83, P < 0.001). Lowest values, 0.09 to 0.16 mg
chlorophyll a/m3, were found in the southern off-
shore region. Highest concentrations occurred in the
northern nearshore region (Table 2, Fig. 3). Within
160
WILLASON ET AL.: ZOOPLANKTON IN CALIFORNIA CURRENT
Table 2— Mean surface water temperature and mean surface chlorophyll a. Chlorophyll
a expressed as mg/m3. The numbers in parentheses are one standard deviation.
Southern
Nearshore (1)
Southern
Offshore (III)
Northern
Nearshore (II)
Northern
Offshore (IV)
Temperature (°C)
14.85 (0.72)
15.03 (0.49)
11.56 (0.82)*
13.68 (0.78)
Chlorophyll a
Log Chlorophyll a
0.659 (0.88)
-0.378 (0.38)
0.141 (0.04)
-0.883 (0.12)
5.110 (4.42)
0.555 (0.39)*
0.485 (0.29)
-0.404 (0.31)
No. of stations
27
12
25
17
indicates value(s) significantly different from those of other regions (P < 0.05, t-test).
Surface Temperature (°C)
9.0- 9.9
10.0-10.9
11.0-11.9
12.0-12.9
13.0-13.9
14.0-14.9
15.0-16.0
Figure 2 — Surface water temperatures
(°C) along the California coast. L
124c
122'
120c
118c
this region two areas of very high chlorophyll a (up
to 14.7 mg/m3) were found: near Point Conception
and just south of San Francisco Bay. These areas
were located just south of the areas of coldest sur-
face waters.
Euphausiid Distribution and Abundance
Euphausia pacifica adults were captured at 43 of
the 81 stations sampled and Nematoscelis difficilis
adults were captured at 38 stations. As there was
no significant difference between numbers of males
and females captured of either species (P > 0.3,
Wilcoxon test), the abundances shown in Figures 4
and 5 represent the sum of both sexes. Both the
number of specimens ofN. difficilis captured at each
station (P < 0.01, t-test) and the proportion of sta-
tions where individuals were caught (P < 0.01, x2
test) were greater at night. For E. pacifica, there
were no significant day-night differences in the num-
bers of animals captured (P > 0.2, £-test), however,
like N. difficilis, the proportion of stations where
individuals were captured was greater at night (P
< 0.05, x2 test). The day-night differences may
represent net avoidance by euphausiids or under-
sampling during the day because of vertical migra-
tion. Thus, the data presented in Figures 4 and 5
represent general trends and are intended to show
relative differences between areas. Because euphau-
siids were captured at only about one half of the sta-
tions, statistical comparisons were made only
between the north and south (i.e, nearshore and
161
FISHERIES BULLETIN: VOL. 84, NO. 1
Figure 3— Surface chlorophyll a. Ex-
pressed as mg chlorophyll a per m3.
Surface Chlorophyll a
mg/m3
> 7.0
3.5-7.0
1.3-3.4
0.4-1.2
< 0.4
San
£/;;.Diego
38c
36<
34<
32(
124c
122c
120c
118c
Euphausia pacifica
Abundance
San Adults/1000 m3
Francisco
> 1500
400-1500
40-399
< 40
None Captured
;;j. Point Conception
San
£:•;... Diego
J L
J L
38c
36°
34<
32<
Figure A— Euphausia pacifica abundance
Expressed as number of adults per
1,000 m3.
124<
122°
120°
118c
162
WILLASON ET AL.: ZOOPLANKTON IN CALIFORNIA CURRENT
offshore regions for the north and south were
combined).
Specimens of E. pacifica were captured in signifi-
cantly greater numbers north of Point Conception
(Table 3) and were rare or absent at most offshore
stations (regions III and IV). This species was espe-
cially abundant off Point Conception and just south
of Monterey Bay along the central coast (Fig. 4).
These two areas were located close to the areas of
highest chlorophyll a concentration. The abundance
of E. pacifica was significantly correlated with
chlorophyll a over the entire grid (Table 4).
The distribution of N. difficilis (Fig. 5) was quite
different from that of E. pacifica. This species was
captured at only 30% of the stations where E.
pacifica was found and was distributed farther off-
Table 3.— Mean abundance and laminarinase activity (LA) of Euphausia pacifica and Nematoscelis difficilis
in the north and south regions. Numbers in parentheses are one standard deviation. Log values were used
for statistical comparisons.
South Regions (I &
North (Regions (II & IV)
Males
Females
Males
Females
Euphausia pacifica
Abundance (No./1,000 m3)
Log abundance
LA
Log LA
No. of stations
Nematoscelis difficilis
Abundance (No./1,000 m3)
Log abundance
LA
Log LA
No. of stations
96.07 (100.4)
1.604 (0.623)*
122.5 (47.8)
2.058 (0.167)
16
13.71 (12.78)
1.001 (0.327)*
167.3 (87.5)
2.172 (0.237)*
16
96.41 (102.5)
1.647 (0.666)*
165.1 (59.9)
2.186 (0.183)
15
18.06 (16.07)
1.061 (0.461)*
208.6 (102.9)
2.270 (0.207)*
18
200.6 (234.4)
2.035 (0.551)
109.7 (68.9)
1 .965 (0.263)
27
55.11 (70.31)
1.530 (0.441)
104.4 (41.9)
1.992 (0.174)
20
270.2 (337.3)
2.119 (0.579)
153.2 (111.9)
2.099 (0.269)
27
75.17 (83.84)
1 .657 (0.453)
130.4 (55.1)
2.041 (0.191)
19
indicates value(s) significantly different between north and south (P < 0.05, f-test).
Figure 5.— Nematoscelis difficilis abun-
dance Expressed as number of
adults per 1,000 m3.
Nematoscelis difficilis
Abundance
Adults/1000 m3"
>250
50-250
10-49
<10
None
Captured
'///..Point Conception
San
V^.Diego
38<
36c
34<
32c
124°
122c
120c
118c
163
FISHERIES BULLETIN: VOL. 84, NO. 1
shore As with E. pacifica, both sexes of AT. difficilis
were found in significantly greater numbers in the
north (Table 3). The abundance of N. difficilis was
not correlated with surface chlorophyll a (Table 4).
Euphausiid Laminarinase Activity
Similar to the results of Willason (1983) and Willa-
son and Cox (in press), males of both euphausiid
species showed significantly less LA than females
(P < 0.01, both cases, Wilcoxon test). Males in this
study had about 70% (Euphausia pacifica) or 80%
(Nematoscelis difficilis) of the LA of females (Table
3). To simplify the presentation of the data on the
contour maps, LA values of males and females at
each station were averaged.
The values of LA for Euphausia pacifica within
the sampling grid ranged from 50 to 430. Euphau-
siids with the lowest LA values were found in off-
shore areas and in the nearshore area along the cen-
tral coast. Euphausia pacifica with the highest levels
of LA were found just south of San Francisco Bay
and adjacent to the south of Point Conception (Fig.
6). These areas overlapped with and extended just
south of the regions of highest surface chlorophyll
a. There was a positive correlation between LA of
E. pacifica and chlorophyll a over the entire grid
(Table 4).
Table 4— Correlations between chlorophyll a, zooplankton abundance, and laminarinase activity (LA) for
Euphausia pacifica, Nematocelis difficilis, and Calanus pacificus. For euphausiids, abundance and LA values
used in the analyses are the averages of males and females. Numbers in parentheses refer to the number
of samples used in regression analyses.
Correlation
coefficients
Correlation
E. pacifica
(43)
N.
difficilis
(38)
C.
pacificus
9(81)
C.
pacificus
V(81)
Chlorophyll a vs. abundance
Chlorophyll a vs. LA
LA vs. abundance
0.61
0.57
0.40
10.27
10.03
10.14
0.24
0.53
0.38
0.31
0.62
0.48
'Correlation coefficients which were not significant at the 95% level.
J L
Euphausia pacifica
Laminarinase
Activity
>300
200-300
100-199
< 100
None Captured
///.Point Conception
San
rv/;;;. Diego
J L
j i
38c
36°
34c
32e
Figure 6— Euphausia pacifica laminari-
nase activity (LA). Expressed as fig
glucose per gram wet weight per
minute
124<
122c
120c
118c
164
WILLASON ET. AL.: ZOOPLANKTON IN CALIFORNIA CURRENT
The values of LA for Nematoscelis difficilis were
in the same range as those of Euphausia pacifica
(50 to 400), but showed a different distributional pat-
tern (Fig. 7). Regions of highest activity were located
in three small areas: adjacent to San Diego, in the
Santa Barbara Channel (just south of Point Concep-
tion), and in an area about 150 km off Monterey Bay.
Both males and females of N. difficilis had signifi-
cantly higher levels of LA in the southern portion
of the grid (Table 3). LA of AT. difficilis was not corre-
lated with chlorophyll a (Table 4). Nematoscelis dif-
ficilis with high LA were often found in areas with
very low phytoplankton biomass and vice versa.
Euphausiid Size and Chemical
Composition
Mean wet and dry weights, water content, and pro-
tein content (expressed as percent dry weight and
percent wet weight) of Euphausia pacifica and
Nematoscelis difficilis are presented in Table 5.
Female E. pacifica and both sexes oiN. difficilis had
significantly higher wet and dry weights in the north.
The water content of both euphausiid species ranged
from 76.5 to 81.7% and was very similar between
species, sexes, and regions (Table 5). Protein content
was also very similar between species, sexes, and
regions. The protein values reported here (51 to 56%
of dry weight) are within the range of previously
reported values (Childress and Nygaard 1974).
Copepod Distribution and Abundance
Female and stage V copepodites of Calanus paci-
ficus were captured at all 81 stations sampled. There
were no significant differences between day and
night catches for either C. pacificus (P < 0.01, £-test).
For comparisons between regions, mean abundances
were calculated using both the log transformed and
nontransformed values (Table 6). The log transform-
ed values were used for statistical comparisons. The
overall abundances of females and stage V copepo-
dites were similar to one another in all regions (P
> 0.1, t-test, all cases). Both C. pacificus stages were
significantly more abundant in the two nearshore
regions (I and II) than in the two offshore regions
(III and IV) (Table 6). Figures 8 and 9 show that the
distributions of females and stage V C. pacificus
were patchy within regions. Copepods were particu-
larly abundant in the area close to and just south
of Point Conception. An extremely dense aggrega-
Figure 1 —Nematoscelis difficilis lami-
arinase activity (LA). Expressed as
fig glucose per gram wet weight
per minute.
Nematoscelis difficilis
Laminarinase Activity.
>300
200-300
100-199
<100
None
Captured
Point Conception
San
Diego
38c
36c
34c
32(
124<
122<
120'
118c
165
FISHERY BULLETIN: VOL. 84, NO. 1
Table 5.— Mean individual wet weight, dry weight, % water, and protein content of Euphausia pacifica and
Nematoscelis difficilis from the north and south. Numbers in parentheses are one standard deviation.
South (Regions 1 & III)
North (Regions II & IV)
Males
Females
Males
Females
Euphausia pacifica
Wet weight (mg)
31.01 (11.55)
32.57 (10.81)*
37.73 (11.24)
42.38 (12.11)*
Dry weight (mg)
6.48 (2.38)
6.75 (2.53)*
7.91 (2.57)
8.98 (2.41)*
% water
79.10
79.28
79.04
78.81
Protein (% dry wt)
54.57
56.16
52.62
52.26
Protein (% wet wt)
11.40
11.62
11.05
11.02
No. of stations
16
15
27
27
Nematoscelis difficilis
Wet weight (mg)
27.63 (7.07)*
34.73 (11.28)*
35.23 (7.26)*
43.59 (8.72)*
Dry weight (mg)
5.96 (2.21)
7.22 (2.49)*
7.43 (2.22)
9.19 (2.78)*
% water
78.43
79.22
78.82
78.94
Protein (% dry wt)
56.59
51.23
52.92
54.96
Protein (% wet wt)
12.22
10.65
11.17
11.58
No. of stations
16
18
20
19
indicates value(s) significantly different between north and south (P < 0.05, Mest).
Calanus pacificus <j>
Abundance
copepods/m3
San
:.. Diego
38c
36c
34c
32(
124°
122°
120c
118°
Figure 8.— Calanus pacificus females,
abundance Expressed as number of
copepods per m3.
tion of stage V C. pacificus (474 copepods/m3) was
found at the station adjacent to Point Conception.
The areas where C. pacificus showed the highest
abundances were located near regions of high chloro-
phyll a concentration. However, the abundances of
both C. pacificus stages were poorly correlated (al-
though significant at the 95% level) with chlorophyll
a over the entire grid (Table 4).
Copepod Laminarinase Activity
LA of female and stage V copepodites was much
higher than the levels of both euphausiid species
when expressed on a per weight basis. Like the
euphausiid results, there was large variability in the
LA of C. pacificus among stations. For example, LA
of stage V copepodites ranged from < 150 at offshore
166
WILLASON ET. AL.: ZOOPLANKTON IN CALIFORNIA CURRENT
Table 6. — Calanus pacificus. Mean abundance and laminarinase activity (LA) of stage V copepodites
and females from each region. Numbers in parentheses are one standard deviation. Log values were
used for statistical comparisons.
Southern
Nearshore (1)
Southern
Offshore (III)
Northern
Nearshore (I!)
Northern
Offshore (IV)
Stage V copepodites
Abundance (No./m3)
Log abundance
22.89 (32.11)
0.924 (0.681)*
1.70 (0.86)
0.175 (0.233)
26.07 (93.90)
0.571 (0.733)*
1.82
0.139
(1.44)
(0.299)
LA
Log LA
825.4 (455)
2.845 (0.272)
538.6 (254)
2.688 (0.201)
1,527.5 (792.1)
3.129 (0.231)*
933.2
2.891
(659.4)
(0.258)
Females
Abundance (No./m3)
Log abundance
14.21 (14.72)
0.807 (0.692)*
2.54 (2.21)
0.253 (0.411)
6.67 (10.79)
0.621 (0.400)*
3.05
0.343
(2.03)
(0.351)
LA
Log LA
927.6 (466.2)
2.913 (0.281)
635.2 (413.5)
2.734 (0.222)
1,272.9 (610.3)
3.072 (0.204)*
1,041.5 (547.5)
2.856 (0.261)
No. of stations
27
12
25
17
indicates value(s) significantly greater than those of other regions (P < 0.05, r-test).
41/
Figure 9— Calanus pacificus Stage V
copepodites, abundance Expressed
as number of copepods per m3.
Calanus pacificus V
Abundance -
copepods/m3
San
Diego
38c
36'
34c
32c
124c
122c
120c
118c
stations to 3,855 at the station adjacent to Point Con-
ception. LA of replicate groups of 50 copepods from
the same station were very similar indicating that
the variability was due to differences between sta-
tions (P < 0.05, ANOVA).
Calanus pacificus LA also showed large differ-
ences among the four hydrographic regions. Both
females and stage V copepodites from the northern
nearshore region (II) had significantly higher levels
of LA than copepods from the other regions (Table
6). Copepods in the southern offshore region had the
lowest levels. The contour maps of C. pacificus LA
show patches of copepods with high LA located ad-
jacent to and just south of Point Conception and off
Monterey Bay (Figs. 10, 11). These areas were
located near the regions of highest E. pacifica LA
(Fig. 6) and close to the regions of highest chloro-
phyll a (Fig. 3). There were significant positive cor-
167
FISHERY BULLETIN: VOL. 84. NO. 1
Figure 10— Calanus pacificus females,
laminarinase activity (LA). Expressed
as /jg glucose per gram wet weight
per minute
Calanus pacificus q
Laminarinase
Activity
>2000
1100-2000
500-1099
< 500
7/. Point Conception
San
.Diego
38'
36°
34c
32c
124<
122<
120c
118c
Calanus pacificus V
124c
Figure 11.— Calanus pacificus Stage V
copepodites, laminarinase activity
(LA) Expressed as ng glucose
per gram wet weight per minute
122c
120c
118'
168
WILLASON ET AL.: ZOOPLANKTON IN CALIFORNIA CURRENT
relations between the LA of both C. pacificus stages
and the concentration of chlorophyll a (Table 4).
Copepod Wet and Dry Weights
The largest female and stage V C. pacificus in
terms of weight were located in the northern near-
shore region and the smallest copepods were found
in the southern regions (Table 7). The average water
content of both C. pacificus stages from the four
regions was inversely related to the average dry
weights. Specimens of C. pacificus with the lowest
water content were found in the northern nearshore
region and those with highest water content were
located in the southern offshore region (Table 7).
Figures 12 and 13 show the distribution of wet
weights of C. pacificus females and stage V copepo-
dites, respectively. Since wet and dry weights were
highly correlated (r = 0.81 and 0.83, P < 0.001) only
wet weights are shown. Both figures show a band
of large copepods in the nearshore region along the
central coast. The figures also show the variation in
size of each stage between areas. Copepods (both
stages) in the "heavy band" along the central coast
were almost twice the weight of copepods at some
of the offshore and southern stations.
Copepod Protein and Lipid Content
Total protein content 0*g per copepod) of both C.
pacificus stages was highest in the northern near-
shore region and lowest in the two southern regions
(Table 7). This appears to reflect differences in cope-
pod size between regions as there were highly sig-
nificant correlations between the protein content and
the wet weight for both female (r = 0.82, P < 0.001)
and stage V C. pacificus (r = 0.69, P < 0.001). Pro-
tein content was not mapped since the patterns were
very similar to those of wet weight.
Protein content of C. pacificus, expressed as per-
cent of wet weight, was quite similar between re-
gions: 8.9 to 10.5% for stage V copepodites and 9.3
and 10.8% for females (Table 7). However, both
stages from the southern offshore region did show
slightly higher protein content when expressed as
percent dry weight. This probably reflects the high
water content of copepods from the southern off-
shore region.
The distributions of lipid content of female and
stage V C. pacificus were very patchy and showed
greater than fourfold variation between areas (Figs.
14, 15). Copepods with highest lipid values were
found in the area surrounding Point Conception and
off San Francisco Bay. Although copepod size (wet
weight) probably influenced the total lipid content
of C. pacificus to some extent, the variability of lipid
content cannot be attributed solely to weight. Lipid
content, unlike protein content, was poorly cor-
related with wet weight (r = 0.26 for females and
r = 0.38 for stage V copepodites).
Table 7. — Calanus pacificus. Mean wet weight, dry weight, percent water, protein content, and lipid content
for stage V copepodites and females from each region. Numbers in parentheses are one standard deviation.
Southern
Nearshore (1)
Southern
Offshore (III)
Northern
Nearshore (II)
Northern
Offshore (IV)
Stage V copepodites
Wet weight (^g)
471 (81)
447 (83)
555 (92)*
465 (95)
Dry weight fag)
98 (21)
88 (23)
125 (26)*
98 (25)
% water
79.20
80.31
77.54
78.89
Protein (^g/copepod)
Protein (% dry wt)
Protein (% wet wt)
41.88 (12.24)
44.12
8.89
44.82 (9.31)
49.25
10.03
52.15 (11.26)
42.75
9.40
48.58 (8.02)
48.10
10.45
Lipid (^g/copepod)
Lipid (°/o dry wt)
Lipid (% wet wt)
19.74 (7.82)
20.78
4.19
13.94 (4.96)
15.32
3.12
29.33 (7.72)*
24.04
5.28
15.74 (5.71)
15.58
3.38
Females
Wet weight (^g)
1,023 (170)
1,083 (160)
1,278 (180)*
1,125 (190)
Dry weight fag)
191 (47)
185 (38)
263 (40)*
225 (29)
% water
81.34
82.83
79.40
80.20
Protein (^g/copepod)
Protein (% dry wt)
Protein (% wet wt)
94.92 (22.71)
49.70
9.28
100.84 (24.84)
54.51
9.31
137.81 (26.40)*
52.74
10.78
115.62 (23.33)
51.38
10.28
Lipid (fjg/copepod)
Lipid (% dry wt)
Lipid (% wet wt)
26.71 (13.31)
13.81
2.61
21.96 (9.00)
11.69
2.03
35.27(11.47)
13.41
2.76
30.19 (10.21)
13.47
2.68
No. of stations
27
12
25
17
indicates value(s) significantly greater than those of other regions (P < 0.05, f-test).
169
FISHERY BULLETIN: VOL. 84, NO. 1
Figure 12— Calanus pacificus females.
Average individual wet weight in mg.
Calanus pacificus <j>
Individual Wet
Weight (mg)
1.34-1.54
1.14-1.33
0.94-1.13
0.74-0.93
//.Point Conception
San
Diego
38°
36°
34c
32'
124°
122'
120°
118°
Calanus pacificus V
San
Francisco
■i-t Monterey
": Bay
Individual Wet
Weight (mg)
0.57-0.68
0.48-0.56
0.39-0.47
0.27-0.38
///.Point Conception
San
Diego
38c
36c
34c
32<
124'
122'
Figure 13.— Calanus pacificus Stages V
copepodites. Average individual wet
weight in mg.
120<
118c
170
WILLASON ET AL.: ZOOPLANKTON IN CALIFORNIA CURRENT
Calanus pacificus °.
San
Francisco
::'. Monterey
HI Bay
Lipid
yiLg/copepod
> 40
30-40
20-29
10-19
4 Point Conception
San
£/.■;. Diego
38c
36c
34c
- 32c
Figure 14— Calanus pacificus females.
Average lipid content per copepod
in Hg-
124<
122'
120<
118c
Figure 15.— Calanus pacificus Stage V
copepodites. Average lipid content
per copepod in ytg.
Calanus pacificus V
* /] UJiHn|l PJf
W$r Lipid
'ml: Francisco ^.g/COpepod
V^m//.': Monterey
\).\};:i; Bay
III >30
20-30
10-19
<10
P
« y
r T T ffilTmlt- v/- Point Conception ~
1 ■ VI lnw::y ' •
J LLnulnllfT IfllliinilSi-'-. ••
< i,j yjj pi pjm
* ^i m n
;:::. San
)&::. Diego
3 l i R f
< in/ 4
« 4 LI |
» J-r-M-U
s 1 •
> /T |
s o
■ hh:;:;-'
1 1 1 1
o
1 1 1 1 1 1
38<
- 36c
34<
/••^ 32°
124c
122<
120°
118e
171
FISHERY BULLETIN: VOL. 84, NO. 1
Lipid content of female C. pacificus, expressed as
percent dry weight or percent wet weight, was lowest
in the southern offshore region, but was quite similar
between the other three regions (Table 7). Lipid con-
tent (percent dry or wet weight) of stage V copepo-
dites from the northern nearshore region was higher
than the other regions. This stage showed the lowest
lipid content in the southern offshore region (Table
7).
DISCUSSION
Upwelling was taking place along the California
coast during April 1981. The resulting coastal low
surface water temperatures were most evident in the
northern part of the sampling grid, especially just
north of Point Conception. An upwelling index calcu-
lated for this region during mid-April was higher
than the 20-yr mean (Howe et al. 1981). The cold-
water plume extending into the Southern Califor-
nia Bight (Fig. 2) is a common phenomenon that
occurs when cold, upwelled water from the Point
Conception region becomes entrained into the south-
ward flowing California Current (Reid et al. 1958;
Bernstein et al. 1977; Lasker et al. 1981). The distri-
bution of phy toplankton biomass (estimated by sur-
face chlorophyll a) was the most obvious biological
feature associated with coastal upwelling. Phyto-
plankton patchiness in turn influenced zooplankton
biomass and nutritional parameters. The following
discusses 1) the relationships between various biol-
ogical properties influenced by upwelling and 2)
the persistence and consequences of biological meso-
scale patchiness within the California Current
System.
The distributions and abundances of both euphau-
siid species were similar to previous reports (Brin-
ton 1962, 1967b, 1976, 1981; Brinton and Wyllie
1976; Youngbluth 1976). Euphausia pacifica is gen-
erally more abundant than Nematoscelis difficilis,
and the center of its distribution is located closer
to the coast. The abundance of E. pacifica within
the sampling grid was positively correlated with phy-
toplankton biomass, as has been noted by Young-
bluth (1976). Other herbivorous euphausiids (eg.,
Thysanoessa raschii and T. inermis) also show this
same relationship (Sameoto 1976).
The distribution and abundance of Calanus paci-
ficus stages were also similar to previous reports
(Fleminger 1964; Longhurst 1967). Both females and
stage V copepodites were most abundant close to the
coast near upwelling regions. In contrast to E. paci-
fica, abundances of the two C. pacificus stages show-
ed rather poor (but significant at 95% level) correla-
tions with phytoplankton biomass (r values of 0.24
and 0.31). This result was surprising since both
species are considered herbivores. The weak corre-
lations between C. pacificus abundance and phyto-
plankton standing crop probably resulted from
small-scale heterogeneity and poor mobility of the
C. pacificus population. Populations of C. pacificus
along the California coast show a great deal of small-
scale patchiness on the order of 10's to 100's of
meters (Mullin and Brooks 1976; Star and Mullin
1981; Cox et al. 1982). Grazing by copepods within
these patches can greatly reduce the local phyto-
plankton standing crop. When samples are taken on
scales of 1 km or less, a poor or inverse correlation
between phytoplankton and zooplankton biomass
results (Mackas and Boyd 1979; Star and Mullin
1981). Zooplankton samples in this study were col-
lected from net tows that covered distances of about
1 km or less. Thus, the poor correlations in the
present study confirm results of previous studies and
can be explained on the basis of the sampling
procedure
Laminarinase activity (LA) of C. pacificus and E.
pacifica was positively related to phytoplankton
standing crop. However, a strong relationship be-
tween these variables did not exist for either species
(correlation coefficients between 0.53 and 0.62).
These results were expected because, although most
studies agree that zooplankton digestive enzyme ac-
tivity and feeding rates are closely linked, enzyme
levels do not always represent instantaneous inges-
tion rates nor are they always related to the food en-
vironment at the time of collection (Head and Con-
over 1983; Hassett and Landry 1983; Head et al.
1984; Willason and Cox in press).
We propose three, non-exclusive explanations for
the observed weak correlations between LA and phy-
toplankton biomass. First, time lags of 1 to 7 d in
the response of zooplankton digestive enzymes to
changing food concentrations (Mayzaud and Poulet
1978; Cox and Willason 1981; Willason 1983) can in-
fluence the association between enzyme levels and
the food environment. Because the standing stock
of phytoplankton is often very patchy and can change
rapidly, especially in upwelling regions, zooplankters
are probably continually acclimating to new condi-
tions and an equilibrium may seldom be reached
between enzyme activity, feeding rates, and food
concentration.
Second, phytoplankton concentration may occa-
sionally be high in terms of chlorophyll a, but poor
in quality resulting in low consumption rates and low
digestive enzyme activity. Herbivorous zooplankton
feeding rates have been shown to be greatly de-
172
WILLASON ET AL.: ZOOPLANKTON IN CALIFORNIA CURRENT
pressed by the presence of unpalatable or toxic
phytoplankton (Fielder 1982).
Third, recent evidence indicates that zooplankton
digestive enzymes do not show a substrate-specific
response. Head and Conover (1983) found that LA
in C. hyperboreus was induced in animals which were
fed an algae that did not contain laminarin. Willa-
son (1983) found that levels of laminarinase in E.
pacifica increased when animals consumed small,
nonreactive charcoal particles. This increase in ac-
tivity, however, was less than that of animals given
phytoplankton as a food source Hence, some types
of nonphytoplankton food, such as detrital particles
or fecal pellets, may also elicit a positive digestive
enzyme response. However, since E. pacifica and C.
pacificus are primarily herbivorous and are found
close to the coast where phytoplankton is abundant,
LA of these zooplankters is probably, for the most
part, controlled by phytoplankton consumption.
Because of large-scale patchiness within the sam-
pling grid, relationships between the various biol-
ogical properties are much clearer when stations
were grouped and regions or mesoscale features
compared. Mesoscale patches (100 to 200 km) of C.
pacificus and E. pacifica with high LA values were
clearly associated with areas of highest phytoplank-
ton standing crop: south of San Francisco Bay and
particularly in the area adjacent to and just south
of Point Conception. Although laminarinase levels
may not always accurately represent the feeding con-
ditions at a single station (because of the reasons
stated above), large-scale comparisons indicate that
digestive enzyme levels of herbivorous zooplankton
are stongly influenced by overall food concentration
within an area. This suggests that animals near the
coastal upwelling regions were feeding at higher
rates than animals from other areas of the sampling
grid.
In contrast to E. pacifica, neither the abundance
nor the LA of N. difficilis were correlated with phy-
toplankton standing crop. These differences between
the two euphausiid species are due most likely to dif-
ferent feeding modes or different food preferences.
Nematoscelis difficilis, unlike E. pacifica and C. paci-
ficus, is probably not a herbivore Nemoto (1967) con-
cluded that its mouthparts were very different from
those of most herbivorous euphausiids, and Willason
and Cox (in press) found that phytoplankton was only
a small part of the diet of N. difficilis. What is
puzzling, however, are the high levels of LA we some-
times found in N. difficilis, a range of values similar
to those of E. pacifica. Laminarinase levels in N. dif-
ficilis are apparently controlled by consumption of
a food source other than phytoplankton. Since we
did not examine the gut contents of AT. difficilis nor
quantify potential food other than phytoplankton,
the type of food eaten by N. difficilis could not be
determined.
Based on the weight and biochemical composition
of C. pacificus, the areas of high feeding activity
along the California coast appear to have been per-
sistent for periods of at least 1 to 2 wk. Calanus
pacificus from the northern nearshore region and
from the area near Point Conception were heavier,
had a lower water content, and a higher lipid con-
tent than copepods from other areas. This indicates
that these copepods have had prolonged exposure to
better feeding conditions. The use of zooplankton
biochemical composition and weight as indices of
relative "physiological" or "nutritional" state has
been documented in laboratory experiments. Vidal
(1980) showed a direct relationship between food con-
centration and weight of adult and stage V C. paci-
ficus. Since C. pacificus completes a life cycle in
about 30 d (Vidal 1980; Huntley and Brooks 1982)
and has a fixed number of molts to maturity, 1 or
2 wk at higher food concentrations can have a large
impact on adult size The lipid content of a zooplank-
ton species represents an energy reserve and is an
excellent indicator of nutritional state Lipid content
increases in well-fed animals and decreases in
starved animals (Lee et al. 1970, 1971; Mayzaud
1976; Hakanson 1984). During periods of starvation,
crustaceans in the laboratory also show an increase
in water content (Hiller-Adams and Childress
1983).
Two field studies have shown that changes in food
quality and quantity can cause physiological or nutri-
tional changes in zooplankton populations (Omori
1970; Boyd et al. 1978). In both of these cases, zoo-
plankters were displaced from their optimal habitat
to areas of lower food concentration by currents or
eddies. The displaced zooplankters showed a lower
lipid content and a higher water content presumably
due to suboptimal nutrition. This may be what hap-
pened to individuals of C. pacificus in the offshore
areas of the California Current. These copepods
weighed less and were in poorer physiological con-
dition (high water content and low lipid content) than
C. pacificus located close to the upwelling regions.
Although the origins of these copepods are not
known, physical processes within the California Cur-
rent System such as eddy extensions (Bernstein et
al. 1977; Pelaez and Guan 1982; Haury 1984) or off-
shore surface transport mechanisms (Parrish et al.
1981) could displace zooplankters such as C. paci-
ficus to the food-poor offshore waters.
Because euphausiids were captured at only about
173
FISHERY BULLETIN: VOL. 84, NO. 1
one-half of the stations, comparisons of weight and
water content between specific regions were diffi-
cult. Although the average weight of adults of both
euphausiid species were greater in the northern area
(nearshore and offshore combined), water content
of both species was similar in all areas. The weight
and biochemical composition of adult euphausiids
may be less susceptible to short-term changes in food
concentration than copepods because of their larger
size and longer life cycle (>1 yr, Ross 1982).
Thus far, it is apparent that processes which oc-
cur in relatively small areas along the California
coast, in particular the area near Point Conception,
have a considerable influence on the nutritional state
of two common herbivorous zooplankters, E. paci-
fied, and C. pacificus. What are the long-term im-
plications of this mesoscale patchiness?
The regions of high phytoplankton standing crop
found in April 1981 appear to be relatively predict-
able from year to year. Although upwelling events
in these areas are episodic and seasonal, previous
studies have shown similar patterns. CalCOFI sur-
veys (Owen 1974) and recent satellite imagery (Smith
and Baker 1982; Pelaez and Guan 1982) indicate that
in past years Point Conception and the area off
Monterey Bay have consistently been regions of high
phytoplankton production during the spring and
summer months. This enhanced production has un-
doubtedly influenced zooplankton populations in pre-
ceding years in much the same way that was found
during the present study. Previous investigations
concerning zooplankton distributions and grazing ac-
tivity along the California coast support this conclu-
sion (Fleminger 1964; Brinton 1976, 1981; Cox et
al. 1982, 1983).
Although reproduction was not estimated, it is like-
ly that well-fed zooplankters in the California Cur-
rent produce more eggs than poorly fed animals.
This has clearly been demonstrated in the laboratory
for copepods (Marshall and Orr 1955; Checkley 1980)
and has been suggested for euphausiids (Brinton
1976). Larger individuals of a species also produce
more eggs (Brinton 1976; Nemoto et al. 1972; Ross
et al. 1982). Thus, the larger, better fed copepods
and euphausiids near Point Conception and off Mon-
terey Bay probably have a higher reproductive out-
put than animals from other areas. There is some
evidence which suggests that enhanced reproduction
of zooplankton takes place near Point Conception.
Arthur (1977) noted that the highest densities of
copepod nauplii in the Southern California Bight
were located in a cold-water upwelling plume extend-
ing south from Point Conception. In addition, eggs
and larvae of E. pacifica are more abundant in the
Southern California region following periods of up-
welling (Brinton 1976).
In summary, our results show that upwelling and
phytoplankton variability have a significant impact
on the herbivorous zooplankton in the California
Current. Not only did we find patchiness of zooplank-
ton abundances, but more importantly, zooplankton
nutritional states were also highly variable (i.e, meso-
scale and larger scale patchiness of trophic inter-
actions). Zooplankton in upwelling regions appear
to experience better feeding conditions for periods
of up to several weeks. Prolonged periods of better
feeding conditions in specific areas should influence
secondary production as well. This implies that the
relatively small, productive regions along the Cali-
fornia coast, south of San Francisco Bay and par-
ticularly the area near Point Conception, have a
disproportionally large impact on the biology of
marine organisms within the California Current
System.
ACKNOWLEDGMENTS
We thank M. Page, T Bailey, L. Haury, D. Morse,
and R. Trench for critical review of the manuscript.
We also thank P. Smith and the research staff at the
Southwest Fisheries Center in La Jolla for support
during CalCOFI cruise 8104 and for providing ac-
cess to preserved samples. This work was supported
by NSF grants OEC 79-9317 and OEC 81-09934 and
by the Marine Science Institute at the University of
California, Santa Barbara.
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176
RHIZOCEPHALAN INFECTION IN
BLUE KING CRABS, PARALITHODES PLATYPUS, FROM
OLGA BAY, KODIAK ISLAND, ALASKA
P. T. Johnson,1 R. A. Macintosh,2 and D. A. Somerton3
ABSTRACT
An isolated population of blue king crabs, Paralithod.es platypus, in Olga Bay, Kodiak Island, was sampled
quarterly during 1980-81. It was found to contain abnormal mature females with degenerate ovaries and/or
no sign of having extruded ova following molt. Histological studies of these females and of males and
females collected subsequently in April 1982 showed that rhizocephalan internas (roots) were present
in up to 50% of the population. Both males and females were infected, but male gonads and secondary
sexual characteristics were apparently unaffected. Presence of the rhizocephalan was strongly related
to ovarian abnormalities. Evidence suggests that infected females can molt, but do not extrude or retain
embryos. The Olga Bay rhizocephalan is not related to Briarosaccus callosus, which parasitizes several
species of Alaskan king crabs, including the blue king crab. Externas of the Olga Bay parasite were not
found. The possible relationship of this rhizocephalan to the genus Thompsonia, which has minute multi-
ple externa that might be missed during gross examination, and the possibility that the blue king crab
is an abnormal host that does not allow development of externas are discussed.
Molting, mating, and extrusion of ova occur annually
in red king crabs, Paralithodes camtschatica, and
biennially in blue king crabs, P. platypus. Because
embryos of both species hatch within about 1 yr,
empty embryo cases are carried on blue king crabs
in the second year (Powell and Nickerson 1965; Sasa-
kawa 1973, 1975; Somerton and Macintosh in press).
Somerton and Macintosh (1982)4 studied an isolated
population of blue king crabs in Olga Bay (Kodiak
Island, AK) and found abnormal females that were
of mature size but lacked external evidence of having
extruded eggs or that had apparently degenerate
ovaries. This paper reports results of gross and
histological examination of blue king crabs from the
aberrant Olga Bay population and from three ap-
parently normal eastern Bering Sea populations. A
rhizocephalan, which was found only in the Olga Bay
crabs, appears to be responsible for the abnormal
reproductive pattern.
Northeast Fisheries Center Oxford Laboratory, National Marine
Fisheries Service, NOAA, Oxford, MD 21654.
2Northwest and Alaska Fisheries Center Kodiak Laboratory, Na-
tional Marine Fisheries Service, NOAA, P.O. Box 1638, Kodiak, AK
99615.
3Northwest and Alaska Fisheries Center, National Marine
Fisheries Service, NOAA, 7600 Sand Point Way, N.E., Seattle, WA
98115.
4Somerton, D. A., and R. A. Macintosh. 1982. Aspects of the
life history of the blue king crab (Paralithodes platypus) in Alaska.
Document submitted to the annual meeting of the International
North Pacific Fisheries Commission, Tokyo, Japan, October
1982.
MATERIALS AND METHODS
Blue king crabs in Olga Bay were sampled quarter-
ly: spring (March-April 1980), summer (June 1980),
autumn (October 1980), and winter (January 1981).
Seasonal sample sizes ranged from 155 to 229 crabs,
and a total of 422 males and 337 females was ex-
amined. Both sexes were measured to the nearest
millimeter in carapace length (see Wallace et al.
1949, for measurement). Carapace lengths ranged
from 12 to 162 mm for males and 16 to 143 mm for
females. Data were taken on external egg clutches
of females by relative volume, color of embryos, and
presence or absence of eyespots on embryos. Pres-
ence or absence of empty embryo cases on non-
ovigerous females was also noted.
For the purposes of this paper, "oogonia" are stem
cells; "oocytes" are developing cells before full
maturity; and "ova" are cells that have completed
vitellogenesis, have a thick chorion, and are ready
for fertilization. "Embryo" refers to an external, fer-
tilized, and developing egg or ovum.
The entire ovary and a pleopod with attached em-
bryos or empty embryo cases (if present) were re-
moved from each female considered to be mature or
in the prepubertal stadium (>68 mm carapace length
(CL)). These were preserved in 10% freshwater (river
water) Formalin5 solution buffered with sodium
5Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Manuscript accepted April 1985.
FTSHF.RY RTTT.T.KTTN- VOT. 84 NO 1 1986.
177
FISHERY BULLETIN: VOL. 84. NO. 1
borate (10 g/L solution). The wet weight of preserved
ovaries was recorded to the nearest g and diameters
of a sample of oocytes/ova were recorded to the near-
est 0.1 mm using a stereomicroscope.
Because many of the ovaries appeared abnormal
and could not be classified easily by oogenetic stage,
histological examination was undertaken of ovaries
and pleopods from the largest sample, collected in
January 1981 (Table 1). To provide material for a
more detailed examination, the Olga Bay population
was sampled again in April 1982, and three ap-
parently normal Bering Sea populations of blue king
crabs were also sampled (Table 1). Except as in-
dicated, tissues taken in these collections included
portions of the central nervous system, gut, hepato-
pancreas, gills, eyestalks, epidermis, heart, anten-
nal gland, bladder, ovary, female pleopods, anterior
vas deferens, and, in some cases, testis and hemo-
poietic tissue
Except for the January samples from Olga Bay
(fixed in borate Formalin), all tissues were fixed in
Kelly's solution (containing zinc chloride rather than
mercuric chloride) for 3-4 d, washed 1-2 h in 50%
ethyl alcohol, and stored in 70% ethyl alcohol until
being processed by standard histological methods.
To provide a basis for comparison, ovaries and pleo-
pods of 1 1 female red king crabs collected at Olga
Bay, January 1981, and fixed in borate Formalin, and
tissues from two blue king crabs collected at Glacier
Bay, AK, infected with the rhizocephalan Brian-
saccus callosus, and fixed in Helly's solution, were
also prepared for histological examination.
RESULTS
Prevalence of the Rhizocephalan
The roots (internas) of a rhizocephalan were asso-
ciated with either or both the ovary and the pleopod
in 52% of the 104 blue king crab females taken from
Olga Bay in January 1981, and with various tissues
in 40% of the 15 females and 33% of the 15 males
taken from Olga Bay in April 1982 (Table 2). The
rhizocephalan was also found in 1 of the 11 red king
Table 1.— Origins of blue king crabs examined histologically.
Carapace length
Location
Date
Number of specimens
(mm)
Olga Bay
8-14 Jan. 1981
104 females (ovaries and pleopods)
69-136
Olga Bay
5-9 Apr. 1982
15 males
88-151
15 females
90-128
Pribilof Is.
25 June-3 July 1982
10 males
10 females (plus ovaries and
pleopods from an additional
83-155
10 females)
96-145
Pribilof Is.
21 Feb. 1983
10 females
113-137
St. Matthew I.
10-13 July 1983
17 males
68-158
9 females
61-129
St. Lawrence I.
5-11 Sept. 1982
5 males
85-106
5 females
79-104
Table 2.— Rhizocephalans in individual male and female blue king crabs, Olga Bay, Kodiak Island,
AK, April 1982.
Intensity of
infection
Degenerate
roots
Major areas parasitized (in tissue sections)
Sex
Nerve cord,
assoc. bladder
Bladder in
other areas
Gut
Gonad
Antennal
gland
Hepato-
pancreas
Female
±1
+2
+
+
+
+
+
+
+
+
+ 3
+
+
+
+ +
+
+
+
+ +
+
+
+
+
+
+
+ + +
+
+
+
+
+
+
Male
±
+
+
+
+
+
+
+
+
+
+
+
+ +
+
+
+
+
+
+
+ +
+
+
+
+
+
+
+
'± = light infection; + to + + +
2+ = parasite present.
3+ = present
medium to very heavy infection.
178
JOHNSON ET AL.: RHIZOCEPHALAN INFECTION IN BLUE KING CRABS
crab females taken from Olga Bay in January 1981.
Rhizocephalan externas were never detected. Rhizo-
cephalan tissue was not found in any of the 76 blue
king crabs collected from the Bering Sea and ex-
amined by us.
Data on females collected from Olga Bay in
January 1981 and April 1982 were combined and
then separated into various categories of reproduc-
tive condition, based on both histological condition
and reproductive features of the ovary and on ex-
ternal reproductive features. Females in all cate-
gories were further classified by the presence or
absence of rhizocephalan infection, as determined
histologically (Table 3).
The effect of the rhizocephalan on female repro-
duction was examined by testing the independence
of probable future reproductive success and rhizo-
cephalan presence Based on ovarian categories
(Table 3), probable future reproductive success was
judged as either successful (no degenerating gonadal
cells) or unsuccessful (ovary empty or ovary with
degenerate gonadal cells). Independence of probable
future success and rhizocephalan presence was re-
jected for both measures, implying that rhizo-
cephalan infestation significantly reduces the prob-
ability of future reproductive success (x2 = 16.81,
df = 1, P < 0.001 for empty ovary; x2 = 20.41, df
= 1, P < 0.001 for ovary with degenerate gonadal
cells).
Three of the external categories of females (Table
3) represent crabs at different times after extrusion
of ova. Embryos begin to develop eyes about 4 mo
after extrusion. Hatching occurs slightly more than
12 mo after extrusion. Following hatching, empty
embryo cases persist on the pleopod setae until the
crab molts again, usually slightly <12 mo later
(Somerton and Macintosh in press). Therefore, the
Table 3.— Prevalence of rhizocephalan infection in female blue
king crabs (>68 mm CL) collected in Olga Bay, Kodiak Island,
AK, January 1981 and April 1982.
Parasitized
Not
n
%
parasitized
Ovarian categories
Ovary empty
15
71
6
Ovary with gonadal cells1
With some degenerate cells
38
64
21
No degenerate cells
7
18
32
External categories
Clean pleopod setae
19
51
18
Ovigerous
Uneyed embryos
1
10
9
Eyed embryos
12
48
13
Previously ovigerous
27
59
19
(embryo cases)
'Oocytes and/or ova.
generalized time since extrusion for the uneyed,
eyed, and empty-embryo-case categories is 0-4 mo,
4-14 mo, and 14-24 mo, respectively. If parasitic at-
tacks are random and prevent successful extrusion
and embryo attachment, then prevalence of the
parasite should be low for females with uneyed em-
bryos and should increase with time Independence
between prevalence and time since extrusion (using
uneyed and empty-embryo-case categories) was re-
jected (x2 = 7.79, df = 1, P < 0.01).
Females are grasped by males and held in a "pre-
copulatory embrace" before molting and mating. Of
the 10 grasped females collected January 1981, 5
showed no evidence of previous reproductive activity,
and 5 had empty embryo cases. None were infected
with the rhizocephalan, although three of the
females with empty embryo cases had some degen-
erate gonadal cells.
Based on the April 1982 sample, which includes
males, independence between sex and rhizocephalan
presence was not rejected (x2 = 0.14, df = 1, P =
0.75). The rhizocephalan, therefore, does not appear
to discriminate by host sex.
Presence of the rhizocephalan apparently did not
affect the gonads of males. Both infected and non-
infected males had numerous spermatophores in the
anterior vas deferens. Spermatocytes, some of them
dividing, and developing and mature sperm were
present in the four crabs whose testes were sampled
(one parasitized and three nonparasitized). In the
field, we saw no males exhibiting female secondary
sexual characteristics.
Histological Observations
Rhizocephalan roots occupied the hemal spaces of
the pleopods, were associated with the exterior of
the ovary, and occasionally lay within internal hemal
spaces of the ovary of infected females collected in
January 1981. Roots were associated with various
tissues of males and females collected from Olga Bay
in April 1982 (Table 2). Hemal sinuses of the ovary
and those abutting the gut, the bladder, and the
thoracic ganglia were the most frequently invaded
sites. Roots lay within the glia of the thoracic ganglia
of one crab, but otherwise were confined to hemal
spaces and did not invade tissues.
Roots were cylindrical and surrounded by a PAS-
positive cuticle of variable thickness (Figs. 1, 3). Cells
within the roots usually had large vesicular nuclei,
and refractile spherules were sometimes present in
the cytoplasm. Usually the roots were tubular, with
a defined lumen, and those with large, empty lumens
often had a flattened epithelium. Loosely anasto-
179
1
J
■«
■-,:,/'..,
:g:'":"-' I
.
• <
Figure 1.— Olga Bay rhizocephalan: Cross sections of roots
with occluded lumens. PAS. C, cuticle; S, refractile cytoplasmic
spherules. Bar =10 ^m.
mosing cells filled the lumen of some tubules, and
a defined epithelium was not present in these (Fig.
2). Roots with narrow or occluded lumens often had
smaller, denser nuclei in the epithelium, or an addi-
tional interior layer or group of cells with small,
dense, or condensed nuclei (Fig. 2). The occluded
roots may represent the distal, growing portions of
the organism.
Intensity of infection varied (Table 3). In all of the
heavier infections and most of the medium ones, por-
tions of the roots were degenerate or necrotic (Fig.
3). Host hemocytes had aggregated in such areas and
often had encapsulated the degenerate roots. In
heavy infections with many degenerating and
necrotic roots, blackened areas, probably due to
melanin deposition in the roots, were visible with the
naked eye in the tissues. Sometimes hemocytes had
invaded the lumens of degenerate and necrotic roots,
and other roots had been reduced to amorphous
material surrounded by hemocytes (Fig. 3). In all
cases, roots of normal appearance were also pres-
ent in the same areas. In only one instance were nor-
mal roots surrounded by hemocytes (Fig. 2). Prob-
st
FISHERY BULLETIN: VOL. 84, NO. 1
n
!
0
ilp
*>" i
1
I
v
**
.
#
i
A
Figure 2— Olga Bay rhizocephalan: Normal roots, lying in an
area invaded by hemocytes. Note variable size of the lumen and
one tubule with a group of small, central nuclei and another
with anastomosing cells in the lumen (arrows). PAS. H, hemo-
cytes; T, tubular roots. Bar = 20 (jm.
ably the section had been cut just peripherally to a
large area of degenerating roots.
Ovaries of 88% (53/60) of parasitized females as
opposed to 46% (27/59) of normal females either con-
tained no oocytes or had some or all degenerate
oocytes (Fig. 4). Figure 5 shows a normal ovary with
previtellogenic oocytes. Grasped females all had nor-
mal oocytes that were in late vitellogenesis and en-
closed by a thick chorion. Of the 10 grasped females,
9 were in the premolt condition, and the 10th, a
precocious juvenile 77 mm CL, was in the intermolt.
None of the parasitized crabs were in advanced
premolt, although some were judged to be in early
premolt because the pleopod epidermis was thick-
ened, and occasionally a developing epicuticle was
present.
Excepting the ovary, tissues and organs appeared
normal in the parasitized crabs. Whether or not
there was reduced lipid storage in the hepatopan-
creas was not evident by histological examination of
the present series.
180
JOHNSON ET AL.: RHIZOCEPHALAN INFECTION IN BLUE KING CRABS
1
4 V / *
% — N,# ^ ^J||L<«
-
** -I .
u ; *. *
.0 * t
„• •
«
Figure 3— Olga Bay rhizocephalan: Degenerating and normal roots. PAS. N, normal tubule; C, cuticle;
D, tubules with sloughing epithelium; M, completely necrotic tubule; H. hemocytes. Bar = 0.05 mm.
4
,>'£#*, 4flWMHBfe*i/r'w
.
V
*
1 1
DISCUSSION
The presence of the rhizocephalan in female blue
king crabs appears to impair reproductive function.
Most parasitized crabs have empty ovaries or ovaries
that contain degenerate gonadal cells. We assume
that these traits are linked to reproductive failure,
although there are also unparasitized crabs within
each category. It is not unusual to find a few retained
ova— destined to be resorbed— in a normal post-
extrusion ovary. Therefore, these crabs are also a
source of degenerate gonadal cells. The 2-yr
reproductive cycle of the blue king crab might also
lead to presence of degenerate gonadal cells that had
been produced early in the cycle and had become
senescent. This speculation remains to be investi-
gated.
The increase in the incidence of infection over time
in postextrusion crabs also suggests reproductive im-
pairment. Not only is the prevalence very low (10%)
among females that had recently extruded (with
uneyed embryos), it is zero among grasped premolt
females that were presumably about to molt, mate,
Figure 4— Olga Bay rhizocephalan: Empty ovary of an infected
crab. Arrows point to roots of the parasite PAS. Bar = 0.2
mm.
181
FISHERY BULLETIN: VOL. 84, NO. 1
Figure 5.— Normal ovary with oogonia and previtellogenic
oocytes. PAS. Same scale as Fig. 4.
and extrude. These facts suggest that the rhizo-
cephalan might preclude mating and subsequent ex-
trusion and attachment of fertilized ova.
The external category of reproductive condition
we term "clean pleopod setae" would normally be
associated with immature crabs. In this study, it con-
tained both small females and females of mature size
(total size range 69-133 mm CL). The average size
at maturity of females in Alaskan populations lack-
ing the rhizocephalan ranges from 80 to 96 mm
(Somerton and Macintosh 1983). Crabs larger than
114 mm could reasonably be expected to be carry-
ing embryos or empty embryo cases, but 10 crabs
in the combined January-April sample (9 of which
had the rhizocephalan) were not. Two of the para-
sitized females were soft-shelled, suggesting that
molting can occur in parasitized females.
Presence of the rhizocephalan in male crabs from
Olga Bay apparently did not interfere with normal
gonadal function. Species of Sacculina and many
other rhizocephalans cause a varying degree of ex-
ternal feminization and gonadal dysfunction of their
male hosts (Reinhard 1956). For example, Thomp-
sonia mediterranea causes external appendages of
males of Callianassa truncata to approach the
female condition (Caroli 1931), but a species of
Thompsonia parasitizing Portunus pelagicus does
not affect males (Phang 1975). Briarosaccus callosus
parasitizes the blue, red, golden (Lithodes aequis-
pina), and deep-sea {Lithodes couesi) king crabs in
the Gulf of Alaska (McMullen and Yoshihara 1970;
Somerton 1981; Hawkes et al. 1985). Meyers6 found
testicular regression and broadening of the abdomen
in Briarosaccus-'mfected male blue king crabs from
Glacier Bay.
High prevalences of infection with rhizocephalans
have been reported previously in other decapod
species, so the high prevalence in blue king crabs of
Olga Bay is not surprising. McMullen and Yoshihara
(1970) found 14 of 21 golden king crabs, captured
near Kodiak Island, infected with B. callosus, and
Hawkes et al. (1985) reported 76% prevalence of the
same species in blue king crabs from Glacier Bay;
Phang (1975) reported prevalences between 24% and
68% of Thompsonia sp. in groups of Portunus pela-
gicus captured near Singapore; and Perry (1984) said
that sometimes over 50% of blue crabs sampled from
a single population in the Gulf of Mexico were in-
fected with Loxothylacus texanus.
Although nearly 800 blue king crabs were sampled
from Olga Bay at quarterly intervals, no rhizoceph-
alan externas were observed, and the one red king
crab female found infected with what appeared to
be the same rhizocephalan also lacked an externa.
Due to the absence of externas, the Olga Bay rhizo-
cephalan cannot be indentified with certainty. Its
roots are similar histologically to those of other rhi-
zocephalans [Thompsonia (Potts 1915); Sacculina
(Fischer 1927; Dornesco and Fischer-Piette 1931);
and Peltogaster and Gemmosaccus (Nielsen 1970)],
corresponding best with the roots of Thompsonia,
which have a thinner cuticle than the others (Potts
1915). Roots of the Olga Bay parasite differ
histologically in several ways from those of
Briarosaccus callosus. They are of lesser diameter,
have a thinner cuticle, lack large peripheral nuclei,
often have a large lumen and flattened epithelium,
and seldom have the cytoplasmic vacuoles (probably
representing lipid storage) that are common in the
B. callosus roots. (Compare Figures 1, 2, and 3 with
Figure 6.) The Olga Bay parasite and B. callosus also
differ in that the roots of B. callosus are a bright
green when fresh (Hawkes et al. 1985) and blue-
green when fixed in Helly's solution, whereas the
roots of the Olga Bay parasite are colorless.
6T. Meyers, Assistant Professor of Fisheries, School of Fisheries
and Science, University of Alaska, 11120 Glacier Highway, Juneau,
AK 99801, pers. commun. October 1984.
182
JOHNSON ET AL.: RHIZOCEPHALAN INFECTION IN BLUE KING CRABS
The lack of obvious externas on the parasitized
crabs is puzzling. One possibility is that externas are
produced but are inconspicuous and/or evanescent.
Most rhizocephalans produce easily detected exter-
nas that emerge from the venter of the abdomen.
Species of Thompsonia, however, produce multiple
small externas 1-4.5 mm long and no more than 1.1
mm in diameter. These externas occur on the ap-
pendages and venters of the thorax and abdomen,
depending on the species, and those of at least one
of the species are easily dislodged (Hafele 1911; Potts
1915; Phang 1975). If few and scattered externas
of the Thompsonia type were present, they could
have escaped notice on animals as large as the blue
king crabs investigated. The second possibility is that
externas are not developed in the blue king crab.
Host ranges of rhizocephalans are often broad, but
some of the host/parasite associations may be acci-
dental or not fully evolved. Sacculina carcini is
known to react differently in different species of
crabs. In Carcinus maenas multiple broods of lar-
vae are produced by S. carcini, but if the host is Por-
tunus holsatus, it breeds but once and then is shed,
which suggests that C. maenas is a natural host but
P. holsatus is an adventitious and not entirely com-
petent one (Baer 1951). Perhaps the Olga Bay para-
site is not a usual parasite of the blue king crab, and
although the interna develops extensively and causes
severe damage to female gonads, externas cannot
be produced in this species. The fact that some roots
of the parasite were degenerating or necrotic in most
infected crabs suggests that parasites do die within
the blue king crab, and that infections might be lost
before externas are formed.
ACKNOWLEDGMENTS
We are grateful to E. Munk, J. Bowerman, and R.
Otto of the Kodiak Laboratory for assistance with
fieldwork; to S. Meyers, also of the Kodiak staff, for
laboratory assistance; to G. Roe and C. Smith of the
Oxford Laboratory for preparing tissues for histo-
logical examination; to R. Otto for reviewing the
manuscript; to T R. Meyers, University of Alaska,
Juneau, for providing tissues of blue king crabs in-
fected with Briarosaccus callosus; and finally, to Bill
Pinnell and Morris Talifson of Olga Bay, without
whose logistic support and hospitality the fieldwork
would have been twice as difficult and infinitely less
enjoyabla
# #
A • c
■||:
c •
♦
i •<
• «
1|
»
FIGURE 6.— Briarosaccus callosus: Roots. Note lack of a central lumen and the very large, peripheral nuclei
(arrows). Feulgen. C, cuticle Bar =10 ^m.
183
FISHERY BULLETIN: VOL. 84, NO. 1
LITERATURE CITED
Baer, J. G.
1951. Ecology of animal parasites. Univ. Illinois Press, Ur-
bana, IL, 224 p.
Caroli, E.
1931. Azione modificatrice dei Bopiridi e dei Rizocefali sui
caratteri sessuali secondarii delle Callianasse Arch. Zool.
Ital. 16:316-322.
DORNESCO, G. T., AND E. FlSCHER-PlETTE.
1931. Donnees cytologiques sur les "racines" de la Sacculine,
Crustace parasite Bull. Histol. Appl. 8:213-221.
Fischer, E.
1927. Sur le tissu constituant les "racines" endoparasitaires
de la Sacculine C. R. Soc. Biol. 96:329-330.
Ha'fele, F.
1911. Anatomie und Entwicklung eines neuen Rhizocephalen:
Thompsonia japonica. Beitrage zur Naturgeschichte Osta-
siens. Abh. bayer. Akad. Wiss. Math.-phys. Kl., Suppl.-Bd.
2, Abh. 7, p. 1-25.
Hawkes, C. R., T. R. Meyers, and T. C. Shirley.
1985. Parasitism of the blue king crab, Paralithodes platypus,
by the rhizocephalan, Briarosaccus callosus. J. Invertebr.
Pathol. 45:252-253.
MCMULLEN, J. C, AND H. T. YOSHIHARA.
1970. An incidence of parasitism of deepwater king crab,
Lithodes aequispina, by the barnacle Briarosaccus callosus.
J. Fish. Res. Board Can. 27:818-821.
Nielsen, S.-O.
1970. The effects of the rhizocephalan parasites Peltogaster
paguri Rathke and Gemmosaccus sulcatus (Lilljeborg) on five
species of paguridan hosts (Crustacea Decapoda). Sarsia
42:17-32.
Perry, H. M.
1984. A profile of the blue crab fishery of the Gulf of Mexico.
Gulf States Mar. Fish. Comm., Spec Publ. 9, 80 p.
Phang, V. P. E.
1975. Studies on Thompsonia sp. a parasite of the edible swim-
ming crab Portunus pelagicus. Malay. Nat. J. 29:90-98.
Potts, F. A.
1915. On the rhizocephalan genus Thompsonia and its rela-
tion to the evolution of the group. Pap. Dep. Mar. Biol.
Carnegie Inst. Wash. 8:1-32.
Powell, G. C, and R. B. Nickerson.
1965. Reproduction of king crabs, Paralithodes camtschatica
(Tilesius). J. Fish. Res. Board Can. 22:101-111.
Reinhard, E. G.
1956. Parasitic castration of Crustacea. Exp. Parasitol. 5:
79-107.
Sasakawa, Y.
1973. Studies on blue king crab resources in the western Ber-
ing Sea. I. Spawning cycle [In Jpn.] Bull. Jpn. Soc. Sci.
Fish. 39:1031-1037. (Engl, transl. NOAA Lang. Serv.
Branch.)
1975. Studies on blue king crab resources in the Western Ber-
ing Sea. II. Verification of spawning cycle and growth by tag-
ging experiments. [In Jpn.] Bull. Jpn. Soc. Sci. Fish. 41:
937-940. (Engl, transl. NOAA Lang. Serv. Branch.)
Somerton, D. A.
1981. Contribution to the life history of the deep-sea king crab
Lithodes couesi, in the Gulf of Alaska. Fish. Bull., U.S. 79:
259-269.
Somerton, D. A., and R. A. Macintosh.
1983. The size at sexual maturity of blue king crab, Para-
lithodes platypus, in Alaska. Fish. Bull., U.S. 81:621-
628.
Somerton, D. A., and R. A. Macintosh.
In press. Reproductive biology of the blue king crab, Para-
lithodes platypus, in the eastern Bering Sea. J. Crustacean
Biol.
Wallace, M. M., C. J. Pertuit, and A. H. Hvatum.
1949. Contributions to the biology of the king crab Para-
lithodes camtschatica (Tilesius). U.S. Fish Wild. Serv., Fish.
Leafl. 340, 49 p.
184
NOTES
THE SEX RATIO AND GONAD INDICES OF
SWORDFISH, XIPHIAS GLADIUS,
CAUGHT OFF THE COAST OF
SOUTHERN CALIFORNIA IN 1978
In the tropical and subtropical Pacific, swordfish,
Xiphias gladius, about to spawn are found through-
out the year but are most abundant from March to
July (Palko et al. 1981). There is, however, little in-
formation on the reproductive potential of swordfish
during their summer and autumn migrations into
the Southern California Bight, a temperate region
encompasing the principal U.S. west coast swordfish
fishing grounds. In 1978 scientists from the South-
west Fisheries Center collected the gonads of sword-
fish harpooned in the Bight (from Point Conception
to the United States-Mexico border) in order to
determine sex ratios, gonad indices, and the repro-
ductive condition of these fish.
Methods
Ninety swordfish were sampled from 25 August
through 20 November 1978. After capture their
gonads were preserved in 10% Formalin1 and, in the
laboratory, were weighed to the nearest gram and
their sex determined visually. Ovarian sections used
in the histological analysis were obtained from seg-
ments removed from the centers of the ovaries. Seg-
ments were imbedded in Paraplast and 8 ^m sections
were cut, stained in iron hematoxylin, and counter-
stained in eosin.
Two gonad indices were calculated for each pair
of ovaries to permit comparisons with two existing
studies on the sexual maturity of Pacific swordfish.
The first (from Uchiyama and Shomura 1974) is
simply the percentage of the fresh weight of the
ovaries to the total weight of the fish:
GI = (W/L3) x 104
(2)
r,r WT-0 ^nn
GI = - x 100
WT-F
(1)
where GI = gonad index,
WT-0 = fresh weight of both ovaries, and
WT-F = fresh weight of whole fish.
The second index (from Kume and Joseph 1969) is
'Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
FISHERY BULLETIN: VOL. 84, NO. 1, 1986.
where GI = gonad index,
W = fresh weight of both ovaries in grams,
and
L = post-orbital fork length in centime-
ters.
Because the gonads used in this study were pre-
served, and thus subject to shrinkage and loss of
weight, it was necessary to estimate their fresh
weight using the relationship (from Uchiyama and
Shomura 1974):
Y = e
In X-0.155
0.969
(3)
where Y = estimated fresh weight of ovaries, and
X = weight of preserved ovaries.
The estimated weight loss due to preservation was
as high as 7%.
Results and Discussion
All 90 swordfish collected were mature with fork
lengths ranging from 133 to 218 cm. Of these, 23
(26%) were males and 67 (74%) were females for a
sex ratio of 0.34:1 (M:F). Although the proportion
of females varied among months, our sample sizes
were too small to demonstrate such variation.
Female swordfish in our sample all had gonad in-
dices that were considerably lower than those of com-
parable studies. Uchiyama and Shomura (1974) col-
lected 16 pairs of ovaries from swordfish caught near
Hawaii and found three pairs to be ripe These had
gonad indices (from Equation (1)) of 6.4, 8.4, and 9.8
whereas our highest value (from Equations (1) and
(3)) was 1.0. Kume and Joseph (1969) examined 362
pairs of ovaries from swordfish captured in the east-
ern Pacific (east of long. 130°W) and found two ripe
specimens whose gonad indices (from Equation (2))
were 10.8 and 11.1. By comparison, the highest from
our study (from Equations (2) and (3)) was 1.8. These
results indicate swordfish in the Southern Califor-
nia Bight during our sampling period were not
spawning.
A histological analysis was performed on a subset
of 16 pairs of ovaries from our sample Histological
analyses can be used to determine not only if a fish
185
is in spawning condition but, also, if it has recently
spawned (Hunter and Macewicz 1985). Ovaries from
our sample contained no mature oocytes and, in
addition, did not contain abundant atretic oocytes
indicative of the resorption process. Instead the
ovaries were in the regressed stage and contained
primary oocytes lining connective tissue septa. These
results indicate that the swordfish were reproduc-
tively inactive during the sampling period and for
at least a month or two before capture Although this
conclusion does not preclude the possibility of spawn-
ing early in the year, swordfish then are scarce Also
water temperatures favorable for spawning (Palko
et al. 1981) are not widespread in the summer and
autumn, and are virtually nonexistant the remainder
of the year.
Acknowledgments
The authors are indebted to the cooperating com-
mercial swordfish fishermen and the scientific
observers, particularly Dimitry Abramenkoff and
Lynn Shipley, who conducted field sampling. The
comments of Gary Sakagawa, Norm Bartoo, and
Pierre Kleiber were greatly appreciated.
Literature Cited
Hunter, J. R., and B. J. Macewicz.
1985. Rates of atresia in the ovary of captive and wild north-
ern anchovy, Engraulis mordax. Fish. Bull., U.S. 83:119-
1. •',<',.
Kume, S., and J. Joseph.
1969. Size composition and sexual maturity of billfish caught
by the Japanese longline fishery in the Pacific Ocean east
of 130 W. Bull. Far Seas Fish. Res. Lab. (Shimizu) 2:115-
162.
Palko, B. J., G. L. Beardsley, and W. J. Richards.
1981. Synopsis of the biology of the swordfish, Xiphias
gladius Linnaeus. U.S. Dep. Commer., NOAA Tech. Rep.
NMFS Circ. 441, 21 p.
UCHIYAMA, J. H., AND R. S. SHOMURA.
1974. Maturation and fecundity of swordfish, Xiphias gladius,
from Hawaiian waters. In R. S. Shomura and F. Williams
(editors), Proceedings of the International Billfish Sympo-
sium Kailua-Kona, Hawaii, 9-12 August, 1972. Part 2. Review
and contributed papers, p. 142-148. U.S. Dep. Commer.,
NOAA Tech. Rep. NMFS SSRF 675.
Earl C. Weber
Southwest Fisheries Center La Jolla Laboratory
National Marine Fisheries Service, NOAA
8604 La Jolla Shores Drive
La Jolla, CA 92038
Stephen R. Goldberg
Department of Biology
Whittier College
Whittier, CA 90608
GROWTH OF DOLPHINS, CORYPHAENA
HIPPURUS AND C. EQUISELIS, IN
HAWAIIAN WATERS AS DETERMINED BY
DAILY INCREMENTS ON OTOLITHS
The dolphin, Coryphaena hippurus, and pompano
dolphin, C. equiselis, are widely distributed pelagic
fishes in tropical and subtropical oceans (Beardsley
1967; Rose and Hassler 1968; Shcherbachev 1973).
In Hawaiian waters C. hippurus is caught through-
out the year, but its abundance fluctuates. Small fish
(<2.3 kg) are plentiful in summer and large fish
(13.6-18.1 kg) are more abundant from February to
April (Squire and Smith 1977). Coryphaena hippurus
is important to the commercial and recreational fish-
eries; C. equiselis, a smaller fish with a maximum
length of 74 cm (Herald 1961), is occasionally caught
by recreational fishermen. Although much is known
about the life history of C. hippurus in the Atlantic
(Palko et al. 1982), the biology of the Hawaiian
population has been only sketchily investigated. Lit-
tle is known about C. equiselis.
At least three age and growth studies on C. hippu-
rus have been reported. Annual marks on scales have
been used to age C. hippurus off Florida (Beards-
ley 1967) and North Carolina (Rose and Hassler
1968) in the western North Atlantic Ocean. Wang
(1979) used monthly modal progression of length-
frequency distributions to estimate the growth rate
of C. hippurus off eastern Taiwan in the western
Pacific Ocean. The estimated growth rates of C. hip-
purus off Florida and North Carolina differed slight-
ly, but the growth rate of C. hippurus in the western
Pacific Ocean was reported to be about twice as
great as those in the western North Atlantic Ocean.
The purpose of this study was to validate estimates
of age and growth of larval and juvenile C. hippurus
and C. equiselis based on microstructure of otoliths
(sagittae) from fish of known age reared in captivity.
Otoliths from wild specimens captured in Hawaiian
waters were also used as a source of age and growth
information and these data were fitted to the von
Bertalanffy growth model. Ages of cultured and cap-
tured wild specimens were estimated by enumer-
ating presumed daily increments on the sagitta
following Pannella (1971). The daily nature of the
increments was validated by counts from sagittae
of fish reared in captivity and whose age was known.
Knowledge of growth rates of both species of
dolphins are useful to mariculturists who would like
to compare the growth rates of wild and cultured
individuals. Information on the growth rate of C. hip-
purus can also be of use to managers of Hawaiian
fishery resources.
186
FISHERY BULLETIN: VOL. 84, NO. 1
Materials and Methods
Validation
Fertilized eggs of C. hippurus and C. equiselis were
obtained between January 1982 and February 1983
from captive broodstock held at the University of
Hawaii's Waikiki Aquarium (WA); the Kewalo Re-
search Facility (KRF) of the Southwest Fisheries
Center Honolulu Laboratory, National Marine Fish-
eries Service; and The Oceanic Institute, Waimanalo,
HI. Larvae of both species were reared at the WA
in 4,000 L circular fiber glass tanks with flow-
through water exchange and under shaded natural
light condition. Water temperature ranged between
23° and 27°C. Both species were fed an unlimited
supply (a density of 1-5/mL) of cultured copepod,
Euterpina acutifrons, and Artemia sp. until they
were large enough to accept chopped fish and squid
(about 30 d after hatching), which were then pro-
vided several times during the day. These fish were
fed to satiation. One 167-d-old and three 191-d-old
C. hippurus were reared at the KRF under similar
environmental conditions and feeding regime as at
the WA.1 These juvenile C. hippurus were trans-
ferred to 8 m diameter tanks when they were about
25 cm long.
One to three larvae of C. equiselis were sampled
on the day of hatching (D-0), and each day thereafter
(D-l, D-2, D-4, etc.). However, after the fourth day,
there were few survivors, so only a single specimen
was taken at intervals of 4 d from D-l 9. Three lar-
vae of C. hippurus were sampled on D-4 and single
specimens were sampled at various intervals or ob-
tained after accidental deaths for validating the
growth increments. Other larvae were sampled from
other batches on D-0, D-l, and D-2 for measure-
ments. Specimens were sampled around noon. Total
length of the larvae was measured under a micro-
scope with an ocular micrometer while the specimen
was alive or within an hour after death. To facilitate
measurement, each larva was put on a glass slide,
extended to its full length, and measured. For the
examination of otoliths, the larva on the slide was
immersed in 70% ethanol and allowed to fix for an
hour. The larva was then removed from the ethanol
bath, blotted, and mounted in Euparal,2 a water solu-
ble mounting medium, and covered with a cover slip.
Otoliths could be examined in the squashed whole
mount without extracting them.
After measuring the fork length of juvenile and
adult dolphins with a caliper to the nearest milli-
meter, otoliths were extracted, cleaned, and mounted
whole To extract the otoliths, the head was removed
from the body, and the flesh removed from the head
to expose the skull. With a saw or knife, most of the
supraoccipital and roof of the skull were removed.
After careful removal of the brain, the sagittae
(largest of the three otoliths) could be found in the
sacculi located anteriorly on the right and left sides
of the first vertebra at the caudal end of the brain
cavity. Under a dissecting microscope, the sagitta
was teased out of the sacculus, and extraneous
tissues were brushed away. The pair of sagittae was
then placed on a clean glass slide, permitted to dry,
and mounted in Euparal. Segments of monofilament
line slightly thicker than the sagittae were placed
on both sides of the sagittae to prevent the cover slip
from crushing it.
After clearing for a month, presumed daily incre-
ments on a sagitta were enumerated using a com-
pound binocular microscope with transmitted light
at 600 x magnification. Increments were counted
starting from the core out to the edge of the post-
rostrum, or from the core to the tip of the rostrum.
Usually, counts could not be made in a direct line
from the core to the edge of the rostrum or post-
rostrum of the sagitta; rather, a somewhat circuitous
route was taken from one area of the sagitta to
another by following a prominent growth increment.
Increments were also counted inward from the edge
to the core. Two independent age estimations were
made separately on the rostrum and postrostrum on
a sagitta to verify the age of fish. In some samples,
it was possible only to make a single age estimate
since the sagitta was incomplete, having just a
rostrum or postrostrum. The reader had no infor-
mation such as specimen size or previous counts to
prevent bias in the counting.
The arithmetic mean of 3-14 counts was used to
estimate a fish's age The number of counts from the
rostrum and postrostrum varied from as few as 3
for a larva to 14 for a sagitta of a juvenile The rela-
tionship between counts of otolith increments and
days was assessed for both species by regression
analysis.
'Thomas K. Kazama, Southwest Fisheries Center Honolulu
Laboratory, National Marine Fisheries Service, NOAA, Honolulu,
HI 96812, pers. commun. October 1984.
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Growth of Wild Specimens
Juveniles of both species were dip netted from
Kaneohe Bay, HI. Large juveniles and adults of both
species were obtained from private and chartered
187
sport fishing boats in Honolulu, and C. hippurus
specimens were also obtained from cruises of the
NOAA ship Townsend Cromwell to the Northwestern
Hawaiian Islands from October 1976 to September
1981. Fork lengths were measured to the nearest
millimeter with calipers. The extraction and slide
preparation of sagittae, and counting method were
the same as described for the validation experiments
above But before reading the sagittae of fish caught
in the wild, the sagitta of a known-age fish was re-
examined to review the difference between known
daily increments and subdaily increments. Concen-
tric daily increments, which consist of an inner light
band and an outer dark band, were distinguished
from subdaily increments by carefully focusing to
the plane of maximum clarity. The dark band of the
subdaily increment appeared less defined than the
dark band of daily increments. Misinterpretation and
counting subdaily increments as daily increments
could result in an overestimation of aga The mean
of 10-20 counts was used as the age estimate of older
fish.
Age estimates of wild fish were fitted to the von
Bertalanffy growth model using NLIN Procedure,
a nonlinear regression routine (SAS Institute 1982).
The three juvenile C. hippurus whose sex was un-
determined were added to both the male and female
groups when fitting the curves.
Results
Validation
Fertilized eggs of C. equiselis and C. hippurus
began to hatch after 48-50 h at 24°-25°C and all
hatched within 2 h. The larvae of both species were
4.0-4.6 mm TL and had two pairs of otoliths, the
sagitta and lapillus, at time of hatching. Otoliths of
C. equiselis and C. hippurus on D-0 ranged from 16
to 20 nm in diameter and consisted of the core and
primordium. An hour after hatching, the larvae were
from 5.2 to 5.4 mm TL but did not grow during the
next 3 d and even shrank from 0.1 to 0.2 mm. Oto-
liths of both species on D-l had a dark ring near the
edge which the otoliths of D-0 larvae did not have
and were 22-24 ^m in diameter. The sagittae of both
species on D-4 had four increments (Fig. 1) and were
now slightly larger than the lapillus. Sagittal
diameters were 29-36 fim for C. equiselis and 34-41
^m for C. hippurus.
Mean counts of growth increments on the sagit-
tae of 10 C. hippurus (Table 1) and 13 C. equiselis
Figure 1— Sagitta of a day-4 Coryphaena hippurus larva. Diameter of sagitta is 17 ^m.
188
Table 1. — Mean of counts on known age sagittae of Coryphaena
hippurus.
Table 2.— Mean counts on known age sagittae of Coryphaena
equiselis.
Mean
Total
Fork
Mean
Total
Fork
Known
increment
No. of
length
length
Known
increment
No. of
length
length
age
counts
SD
counts
(mm)
(mm)
age
counts
SD
counts
(mm)
(mm)
0
0
5.3
0
0
4.0
1
1
—
1
1
0.00
3
—
4
4
0.00
3
6.7
1
1
0.00
3
—
4
4
0.00
3
6.8
4
3
0.00
3
4.6
4
4
0.00
3
6.8
4
4
0.00
3
5.2
20
20.0
+ 1.26
5
—
19
19
0.00
3
14.2
35
33.6
+ 2.06
9
—
—
23
23.6
+ 2.23
8
23.0
47
45.2
+ 3.16
10
—
95.0
27
21.5
+ 1.59
14
25.2
167
166.8
+ 7.14
11
—
383.0
31
31.7
+ 1.38
7
—
29.5
191
190.3
+ 6.92
6
—
510.0
36
35.3
+ 2.45
10
—
48.0
191
191.0
+ 0.71
4
—
554.0
51
51.7
+ 2.13
13
—
82.0
191
192.8
+ 7.44
5
—
491.0
52
53.6
+ 4.81
14
—
72.0
63
63.3
+ 3.19
14
—
89.0
63
63.4
±8.59
13
—
112.0
(Table 2) were plotted against corresponding known
ages (Figs. 2, 3). The relationships of mean incre-
ment counts (7) to known age (X) were Y = -0.5295
+ 1.0035X(r = 0.999, P < 0.01) for 10 C. hippurus
and Y = -0.6986 + 1.0164X(r = 0.997, P < 0.01)
for 13 C. equiselis. These results demonstrated that
growth increments are formed daily, and validated
their use for aging wild fish up to 191 d for C. hip-
purus and 63 d for C. equiselis.
Growth of Wild Specimens
Because of sexual dimorphism, separate von Ber-
talanffy growth parameters were calculated for male
and female C. hippurus (Table 3). The male and
female von Bertalanffy growth curves and 18 age-
length relationships of C. hippurus are shown in
Table 3.— Von Bertalanffy growth parameters calculated from cap-
tured wild specimens of Coryphaena hippurus.
Sex
Number Parameter
Estimate
SE
Male
Female
10
fn
0.0790 yr
0.0305
K
1.1871
0.5218
i-oo
189.9301 cm FL
48.9702
'n
0.0731 yr
0.0126
K
1.4110
0.2454
L„
153.2676 cm FL
14.2168
200
DAYS
Figure 2— Validation of daily increments on sagittae of Cory-
phaena hippurus by relationship of known age (X) to mean incre-
ment count (Y) up to 191 d (r = 0.999).
FIGURE 3— Validation of daily increments on sagittae of Cory-
phaena equiselis by relationship of known age (X) to mean incre-
ment count (Y) up to 63 d (r = 0.997).
189
Figure 4. A single set of growth parameters (Table
4) was calculated for C. equiselis since the largest
specimen in the sample had just reached sexual
maturity, and the calculation of separate growth
curves by sex was not warranted. The von Berta-
lanffy growth curve and 13 age-length relationships
of C. equiselis are shown in Figure 5.
Discussion
Validation
A pair of otoliths was present at the time of hatch-
ing for both dolphins, and the first increment was
formed on the otoliths on D-l, identical to Kat-
suwonus pelamis, another tropical pelagic species
(Radtke 1983). The strong correlation of mean incre-
ment counts of sagittae to known age of fish
validated the use of growth increments in the aging
of C. equiselis up to 63 d and C. hippurus up to 191
d. Since regular incremental formation began on D-l,
no adjustment is required to the incremental counts
140
120
100
- 80
I
I-
o
z
Id
cc
O
60
40
20
/
^
MALES
/
/
/ t\ °
/ / FEMALES
//
/ /
Q IMMATURE (N =3)
o FEMALES (N =8)
A MALES (N =7)
^^= VALIDATED
— == UNVALIDATED
0 I 2 3 4 5 6 7 8 9 10 II 12 13 14 15
ESTIMATED AGE (MONTHS)
Figure 4— Von Bertalanffy growth curves of male and female Cory-
phaena hippurus in Hawaiian waters.
Table 4.— Von Bertalanffy growth parameters calculated
from captured wild specimens of Coryphaena equiselis.
Number
Parameter
Estimate
SE
13
K
0.0648 yr
2.1734
61.3914 cm FL
0.0131
0.9750
17.8000
of wild fish sagittae to estimate age Ideally, valida-
tion of daily increments should cover 1) the time
when the first daily increment is formed, 2) the
regularity in the formation of increments in all
stages of life, and 3) events such as spawning, migra-
tion, and periods of starvation which may affect the
regularity of increment formation. Having achieved
only part of these requirements, validation of daily
increments on otoliths should continue as older
known-age specimens become available, and the ef-
fects of spawning and starvation on increment for-
mation should also be examined.
Growth of Wild Specimens
The plot of age-length relationships of male C. hip-
purus showed that there was at least one extreme
variant. This 111.0 cm FL male greatly affected the
growth curve, resulting in a lower estimated L^ and
causing most of the male age estimates to fall below
the growth curve (Fig. 4). Thus, age-length relations
of wild C. hippurus should be examined further to
shed light on the extent of variation in size at given
ages. Additional age determinations might also im-
prove the confidence intervals of the von Bertalanffy
growth parameters.
Growth rates of C. hippurus to age 1 around
Hawaii appeared to be greater than those reported
from the western North Atlantic Ocean. Beardsley
(1967) reported a mean length of 72.5 cm in age
group 1 for C. hippurus off Florida. Rose and
Hassler (1968) reported a mean length of 65.3 cm
at the end of 1 yr for fish off North Carolina. Around
Hawaii male C. hippurus were estimated to attain
40
30
£ 20
cc
O
10
"l r
VALIDATED
2 3 4 5
ESTIMATED AGE (MONTHS)
Figure 5.— Von Bertalanffy growth curve of Coryphaena equiselis
in Hawaiian waters derived from 13 age estimates.
190
a length of about 126 cm at 1 yr and about 112 cm
for females. The slower growth rate of C. hippurus
in the western North Atlantic Ocean may be the
result of a decrease in feeding rate when water
temperature goes below 23.0°C and a cessation of
feeding at 18.0°C (Hassler and Hogarth 1977). Cory-
phaena hippurus feed throughout the year in Hawaii
and can be expected to grow continuously.
Wang (1979) used the monthly progression of
modes in length-frequency distributions to estimate
growth rates of about 10 cm/mo from February
through June for C. hippurus between 50 and 100
cm FL. This growth rate is similar to that found for
C. hippurus in Hawaiian waters.
Growth rates of captive C. hippurus were similar
to those of wild fish in Hawaiian waters. Beardsley
(1967) reported rapid growth rates of three captive
C. hippurus. These fish grew from about 35 to 125
cm in 7 to 8 mo.3 Soichi (1978) reported that 11 C.
hippurus 35-50 cm TL grew to a mean 123 cm TL
in 7-8 mo. Their observations also support our
estimates of rapid growth for C. hippurus around
Hawaii.
Coryphaena equiselis appeared to grow as rapid-
ly as C. hippurus during the first 4 mo, then grew
at a slower rate (Fig. 5). At about 4 mo, C. equiselis
reached sexual maturity. Coryphaena hippurus also
reached sexual maturity at 4-5 mo, but have been
observed to mature as early as 3 mo in captivity.
The daily regularity of increment formation has
been demonstrated from D-l to D-191 for C. hip-
purus and from D-l to D-63 for C. equiselis. So the
use of daily increment counts on the sagitta of wild
fish for estimating age has only been partially
validated for these dolphins. The age-length relation-
ships are valid for the first 6 mo for wild C. hippurus
and the first 2 mo for wild C. equiselis. Thus, the
von Bertalanffy growth curves calculated for wild
C. hippurus in Hawaiian waters should be viewed
with caution despite good agreement with several
other growth observations in the literature
Acknowledgments
Our thanks to Richard W. Brill, Richard E. Brock,
Leighton R. Taylor, and Jerry A. Wetherall for their
critical reviews of this manuscript. Carol Hopper
greatly assisted our sampling efforts for wild-caught
specimens and Thomas K. Kazama provided the
oldest known-age C. hippurus.
3 A length-weight relationship (Gibbs and Collette 1959) was used
to estimate lengths in centimeters from weights, given in pounds,
by Beardsley (1967).
Literature Cited
Beardsley, G. L., Jr.
1967. Age, growth, and reproduction of the dolphin, Cory-
phaena hippurus, in the Straits of Florida. Copeia 1967:
441-451.
Gibbs, R. H., Jr., and B. B. Collette.
1959. On the identification, distribution, and biology of the
dolphins, Coryphaena hippurus and C. equiselis. Bull. Mar.
Sci. Gulf Caribb. 9:117-152.
Hassler, W. W., and W. T. Hogarth.
1977. The growth and culture of dolphin, Coryphaena hip-
purus, in North Carolina. Aquaculture 12:115-122.
Herald, E. S.
1961. Living fishes of the world. Doubleday and Co., Inc.,
Garden City, NY, 304 p.
Palko, B. J., G. L. Beardsley, and W. J. Richards.
1982. Synopsis of the biological data on dolphin-fishes, Cory-
phaena hippurus Linnaeus and Coryphaena equiselis Lin-
neaus. U.S. Dep. Commer., NOAA Tech. Rep. NMFS Circ
443, 28 p. [Also FAO Fish. Synop. 130.]
Pannella, G.
1971. Fish otoliths: Daily growth layers and periodical pat-
terns. Science (Wash., D.C.) 173:1124-1127.
Radtke, R. L.
1983. Otolith formation and increment deposition in labora-
tory-reared skipjack tuna, Euthynnus pelamis, larvae. In E.
D. Prince and L. M. Pulos (editors), Proceedings of the Inter-
national Workshop on Age Determination of Oceanic Pelagic
Fishes: Tunas, Billfish.es, and Sharks, p. 99-103. U.S. Dep.
Commer., NOAA Tech. Rep. NMFS 8.
Rose, C. D., and W. W. Hassler.
1968. Age and growth of the dolphin, Coryphaena hippurus
(Linnaeus), in North Carolina waters. Trans. Am. Fish. Soc
97:271-276.
SAS Institute.
1982. SAS user's guide: Statistics. SAS Institute Inc., Cary,
NC, 584 p.
Shcherbachev, Yu. N.
1973. The biology and distribution of the dolphins (Pisces,
Coryphaenidae). [In Russ.] Vopr. Ikhtiol. 13:219-230.
(Engl, transl. in J. Ichthyol. 13:182-191.)
Soichi, M.
1978. Spawning behavior of the dolphin, Coryphaena hip-
purus, in the aquarium and its eggs and larvae [In Jpn.,
Engl, summ.] Jpn. J. Ichthyol. 24:290-294.
Squire, J. L., Jr., and S. E. Smith.
1977. Anglers' guide to the United States Pacific coast:
marine fish, fishing grounds & facilities. U.S. Dep. Commer.,
NOAA, NMFS, 139 p.
Wang, C H.
1979. A study of population dynamics of dolphin fish (Cory-
phaena hippurus) in waters adjacent to eastern Taiwan.
[In Chin., Engl, abstr.] Acta Oceanogr. Taiwan. 10:233-251.
James H. Uchiyama
Southwest Fisheries Center Honolulu Laboratory
National Marine Fisheries Service, NOAA
P.O. Box, 3830, Honolulu, HI 96812
Raymond K. Burch
Syd A. Kraul, Jr.
Waikiki Aquarium, University of Hawaii
2777 Kalakaua Avenue
Honolulu, HI 96815
191
SIZES OF WALLEYE POLLOCK,
THERAGRA CHALCOGRAMMA, CONSUMED
BY MARINE MAMMALS IN THE BERING SEA
In the Bering Sea at least 11 species of marine mam-
mals, 13 seabirds, and 10 fishes are known to feed
on walleye pollock, Theragra chalcogramma (Frost
and Lowry 1981a). Walleye pollock are a major food
of most pinnipeds, particularly in the southern Ber-
ing Sea (Lowry and Frost 1981), and are sometimes
eaten by several species of baleen and toothed whales
(Frost and Lowry 1981b).
In recent years, walleye pollock have been the prin-
cipal target species in the Bering Sea commercial
groundfish fishery. Annual catches have been as high
as 1,840,000 t in 1972 (Bakkala et al. 1981). While
there can be little doubt that both the fishery and
marine mammal predation affect pollock stocks and
perhaps also one another, the interactions are poorly
understood at present (Lowry et al.1; Swartzman and
Harr 1983).
An important aspect of marine mammal-fishery
interactions is the size composition of fishes eaten
in relation to that of the commercial catch. For ex-
ample, if a marine mammal consumes fishes smaller
than those taken by the fishery, the fishery would
be unlikely to influence availability of food to the
predator unless it affected recruitment. If marine
mammals and the fishery remove fishes of similar
sizes, competition would be expected (IUCN2).
Stomach contents of marine mammals seldom con-
tain intact fishes in a condition suitable for mea-
suring. However, the sagittal otoliths of species such
as walleye pollock are easily identified (Frost 1981),
and equations are available that estimate the length
and weight of fishes from otolith lengths (Frost and
Lowry 1981a). We present here information on the
sizes of walleye pollock consumed by marine mam-
mals in the Bering Sea, based on otoliths from
gastrointestinal tracts.
Methods
Specimens were collected during the months of
March to October 1975-81, at the locations shown
in Table 1. With the exception of a minke whale,
Balaenoptera acutorostrata, which was stranded on
shore, all specimens were from animals collected for
scientific purposes. Stomachs were removed and
opened, and the contents gently washed on a 1 mm
mesh sieve. Otoliths were sorted from other ingesta
and identified using the descriptions of Morrow
(1979) and Frost (1981). Since fresh walleye pollock
otoliths have fine lobulations around their perimeter
(Frost 1981) which disappear during digestion,
degraded otoliths were easily detected by compari-
'Lowry, L. F., K. J. Frost, D. G. Calkins, G. L. Swartzman, and
S. Hills. 1982. Feeding habits, food requirements, and status of
Bering Sea marine mammals. North Pac Fish. Manage Counc.
Doc. 19 and 19A, Anchorage, Alaska, Contract 81-4, 574 p.
2IUCN. 1981. Report of IUCN workshop on marine mammal-
fishery interactions, La Jolla, Calif., 30 March-2 April. IUCN,
Gland, Switzerland, 68 p.
Table 1. — Location and dates of capture of marine mammals from which otoliths of walleye pollock
were obtained.
No. of
No. of
otoliths
Species
Dates
Location
specimens
measured
Harbor seal,
13 Apr. 1979
Otter Island
4
23
Phoca vitulina richardsi
9 Oct. 1981
Port Heiden
1
12
Spotted seal,
6 May 1978
61°42.3N, 175°36.0W
1
11
Phoca largha
23 May 1978
63°25.8N, 173°05.6W
1
10
Ribbon seal,
19-20 Apr. 1976
57°20.1N-57°28.0N
5
256
Phoca fasciata
172°30.9W-173°07.5W
21-22 Mar. 1977
58°51.0N-58°56.0N
172°40.0W-173°08.0W
4
67
5-31 May 1978
61°23.0N-64°39.4N
169°07.0W-176°08.8W
10
145
Steller sea lion,
20 Mar. 1976
56°04.8N, 168°32.9W
1
274
Eumetopias jubatus
13 Apr. 1979
Otter Island
1
6
24 Mar.,
59°30.0N-60°11.5N
32
497
10-11 Apr. 1981
176°43.5W-179°55.0W
30 Mar.-4 Apr.
59°08.0N-60°13.0N
56
638
1981
165°45.0E-170°46.0E
Minke whale,
5 Aug. 1975
Unalaska Island
1
121
Balaenoptera acutorostrata
192
FISHERY BULLETIN: VOL. 84, NO. 1, 1986.
son with those taken from trawl-caught fishes. The
maximum length of nondegraded otoliths was
measured to the nearest 0.1 mm using vernier
calipers. When more than 20 otoliths occurred in a
single stomach, a subsample of 20 was measured.
Very few otoliths were found in the stomachs of
ribbon, Phocafasciata, and spotted, P. largha, seals.
For those species, additional otoliths were obtained
from small intestines which were split along their
entire length and examined for parasitological
studies. There was no significant difference between
sizes of otoliths obtained from stomachs and intes-
tines of ribbon seals (Frost and Lowry 1980). Too few
otoliths were retrieved from spotted seal stomachs
to test their sizes relative to otoliths from intestines.
However, otoliths from intestines were of the same
general size range and condition as those from
stomachs. We therefore pooled the measurements
of otoliths from stomachs and intestines.
The fork lengths and weights of walleye pollock
consumed were estimated from equations in Frost
and Lowry (1981a).
Results
We measured a total of 2,060 otoliths from 117 in-
dividual marine mammals belong to 5 species (Table
1). Most of the otoliths were from the stomachs and
small intestines of 19 ribbon seals and 90 Steller sea
lions, Eumetopias jubatus. Ribbon seals, spotted
seals, and a minke whale fed primarily on walleye
pollock <20 cm long (Table 2, Fig. 1). Harbor seals,
Phoca vitulina richardsi, fed on a wide size range
of pollock, including equal numbers of fishes 8-15 cm
and 20-35 cm long and a few individuals 45-56 cm
in length. Most pollock eaten by sea lions (76%) were
20 cm or longer. Young sea lions (<4 yr) collected
in 1981 (all were males) ate significantly smaller fish
(x = 22.4 cm, n = 37) than did older animals (x =
26.9 cm, n = 51; P < 0.005).
There were some differences in sizes of pollock
consumed at different localities and in different
years. The sizes of pollock eaten by harbor seals col-
lected at Otter Island in 1979 ranged from 10.3 to
56.3 cm (i = 31.8 cm), while those eaten by a seal
collected at Port Heiden in 1981 were all <12.6 cm
long (x = 10.6 cm). Two sea lions collected in 1976
and 1979 near the Pribilof Islands had eaten pollock
averaging 46.9 cm in length (range 18.4-61.4 cm),
while those collected in 1981 to the west had eaten
substantially smaller pollock averaging 25.2 cm in
length (range 8.3-64.2 cm). In Figure 1, the smaller
size mode corresponds to 1981 collections and the
larger mode to those from 1976 and 1979. In 1981
sea lions collected in the central Bering had eaten
larger pollock than those off the Kamchatka Penin-
sula (x = 26.8 cm vs. 23.5 cm; P < 0.001). This was
not attributable to different age or size composition
of the samples, since the difference was apparent
for older sea lions (>5 yr; x = 21.8 cm vs. 25.6 cm;
P < 0.01) as well as the samples as a whole, and the
mean age and standard length of all sea lions >5 yr
in the Kamchatka sample (x age = 9.1 yr, x SL =
297 cm, n = 27) was greater than that of the cen-
tral Bering sample (x age = 8.2 yr, x SL = 282 cm,
n = 25).
Discussion
Of the marine mammal species we examined, rib-
bon seals, spotted seals, and a minke whale ate
almost exclusively small pollock, whereas Steller sea
lions and harbor seals ate pollock of a wide range
of sizes. There are few other data available on the
sizes of pollock consumed by marine mammals in the
Bering Sea. Nemoto (1959) indicated that the length
of pollock eaten by fin whales, Balaenoptera physa-
lus, never exceeded 30 cm, while larger pollock were
sometimes eaten by humpback whales, Megaptera
navaeangliae. Fiscus et al. (1964) reported that in
1962 northern fur seals, Callorhinus ursinus, ate
mostly whole pollock <30-35 cm long. McAlister et
al.3 found intact pollock in fur seal stomachs collected
in the eastern Bering Sea, July- September 1974, to
range from 10 to 35 cm, with a mean length of 19.3
cm. Most specimens were between 16 and 21 cm
long. In 1981, Loughlin4 collected fur seals north of
Unalaska Island and found the average size of
pollock consumed to be 30.4 cm. Antonelis5 found
that bearded seals, Erignathus barbatus, collected
near St. Matthew Island in the central Bering Sea
had eaten only small pollock (x length = 8.2 cm).
It is unknown whether the consumption patterns
described above are a result of actual size selection
of prey or if they result from coincidental distribu-
tion of predators and prey size classes. The overall
density of pollock and distribution by age classes are
far from uniform in the southern Bering Sea (Smith
1981; Bakkala and Alton6). The sizes of fishes con-
3McAlister, W. B., G. A. Sanger, and M. A. Perez. 1976. Pre-
liminary estimates of pinniped-finfish relationships in the Bering
Sea. Unpubl. background paper, 19th meeting North Pac. Fur Seal
Comm., Moscow, 1976.
4T. R. Loughlin, National Marine Mammal Laboratory, 7600 Sand
Point Way N.E., Seattle, WA 98115, pers. commun. November 1983.
5G. Antonelis, National Marine Mammal Laboratory, 7600 Sand
Point Way N.E., Seattle, WA 98115, pers. commun. December 1983.
6Bakkala, R., and M. Alton. 1983. Evaluation of demersal trawl
survey data for assessing the condition of eastern Bering Sea
193
Table 2.— Summary of sizes of walleye pollock consumed by marine mammals in the Bering
Sea.
Size of walleye pollock consumed
Marine mammal
Fork
length
height of mean
1Mean weight of
species
Mean (cm)
Range (cm)
length fish (g)
8.6
fishes consumed (g)
Ribbon seal
11.2
6.5-34.4
11.2
Spotted seal
10.9
8.0-15.0
7.9
8.4
Harbor seal
24.5
8.2-56.3
83.8
174.3
Steller sea lion
29.3
8.2-64.2
140.5
204.3
Minke whale
14.5
11.8-17.5
18.3
18.7
'The weight of the mean length fish does not correspond to the mean weight of fishes consumed due
to the exponential nature of the length-weight relationship for fishes and the distribution of lengths of
fishes consumed.
sumed generally agree with the basic distribution
pattern for pollock in that sea lions collected near
the continental slope ate many large pollock, while
ribbon and spotted seals collected north of St. Mat-
thew Island ate almost entirely small pollock.
However, concurrent sampling of prey in stomachs
and those available in the environment suggest that
some selection does occur. Fur seals were found to
eat smaller pollock than those caught in otter trawls
taken nearby (x length = 30.4 cm in seals, 38.3 cm
in trawls), while sea lions appeared to select larger
fishes (x length = 29.9 cm in sea lions, 25.5 cm in
trawls) (Loughlin fn. 4). Such comparisons must be
interpreted with caution since demersal trawl
samples underestimate the abundance of young
pollock, most of which occur several meters off the
bottom (Traynor7).
Other information also indicates that marine mam-
mals sometimes select fishes of certain size classes.
The sizes of arctic cod, Boreogadus saida, caught in
otter trawls in the northern Bering Sea were com-
pared with the estimated lengths of fishes eaten by
spotted and ribbon seals collected in the same area
and time period (Frost and Lowry 1980; Bukhtiyarov
et al. 1984). While the distribution of trawl-caught
fishes was distinctly bimodal, seals ate predominant-
ly fishes of the larger size classes. Saffron cod,
Eleginus gracilis, eaten by adult white whales, Del-
phinapterus leucas, in the Kotzebue Sound region
of the southern Chukchi Sea were larger than those
eaten by younger animals collected at the same loca-
tion on the same dates (Seaman et al. 1982). We ob-
tained similar results in this study for young versus
old sea lions. Pitcher (1981) found that pollock eaten
by sea lions were significantly longer (x = 29.8 cm)
pollock. Unpubl. Rep., 43 p. Northwest and Alaska Fisheries
Center, NMFS, NOAA, Seattle, WA.
7Traynor, J. J. 1983. Midwater pollock (Theragra chalcogram-
ma) abundance estimation in the eastern Bering Sea. Unpubl.
Rep., 7 p. Northwest and Alaska Fisheries Center, NMFS NOAA
Seattle, WA.
194
than those eaten by harbor seals (x = 19.2 cm; P <
0.001) collected in the same general locations in the
Gulf of Alaska.
The factors involved in the apparent size selection
of prey are poorly known for marine mammals. A
strict relationship between the size of predators and
the size of their prey is not to be expected in such
behaviorally complex and morphologically diverse
animals. For example, the prey of ringed seals, Phoca
hispida, range in length from 1 cm (euphausiids) to
at least 121 cm (wolffish, Anarhichas sp.) (Frost and
Lowry 1981c). The largest animal we examined in
this study, a minke whale 7.3 m long, ate uniformly
small pollock. Age-related differences in sizes of
fishes eaten by sea lions and belukha whales are
more likely due to morphological and behavioral
development than to size relationships per se.
Although size may affect a sea lion's ability to catch
large pollock, and old sea lions are larger than young
ones (i SL = 212 cm for sea lions age 1-4 yr, n =
33 vs. x SL = 289 cm for those >5 yr, n = 52), the
size range of pollock eaten by both young and old
sea lions was similar. The largest pollock (64 cm)
represented in our samples was eaten by a 215 cm
long, 3-yr-old sea lion which indicates that physical
differences due strictly to predator size are not the
sole factor influencing preference for a particular
prey siza Aspects of feeding strategy, including size
selectivity, are the result of a complex and inter-
acting suite of morphological, physiological, and
behavioral adaptations which allow an organism to '
gather food in the most efficient manner (Schoener
1971).
Size-specific feeding may have important conse-
quences for predators. For example, the length of
1-yr-old pollock fluctuates markedly among years, as !
does the numerical abundance of the first year class.
In 1976 abundance was low (729 million individuals
in the NMFS Bering Sea survey area) and fishes
were small (x = 11.6 cm), while in 1974 abundance
was high (2,840 million individuals) and fishes were
SPOTTED SEALS <r, = 2>
FISH LENGTH Com)
HARBOR SEALS <" = 5)
FISH LENGTH Com)
MINKE WHALES
Cn = l)
ga
ea
in
I
^-
-J
C
D
U.
O
70
ea
5a
K
48
3a
I
3
z
za
IB
za 30 4a »
FISH LENGTH (cm)
ea ?a
Figure 1— Size distributions of walleye pollock eaten by five
species of marine mammals collected in the Bering Sea,
1975-81.
ia 2e
oe 7e
FISH LENGTH Com)
195
considerably larger (x = 15.9 cm) (Smith 1981). The
corresponding average individual weights can be
estimated as 9.5 and 23.7 g, giving an estimated
biomass of age 1 pollock about 10 times greater in
1974 than in 1976. Therefore, the total food available
to predators that specialize on small pollock can vary
markedly, as can the energy obtained from each fish
consumed. Lengths and population sizes of older
pollock also vary somewhat among years (Smith
1981); however, predators feeding on large pollock
will undoubtedly be exploiting several age classes.
Three species of marine mammals— harbor seals,
sea lions, and fur seals— consume age classes of
pollock that are also exploited by the commercial
fishery (Table 3). A major effect of the pollock fishery
has been a reduction in the abundance of older,
larger individuals (Pereyra et al.8). Major declines in
abundance of sea lions and fur seals in the eastern
Bering Sea have been reported since the 1950's
(Braham et al. 1980; Fowler 1982). Although the
evidence is equivocal, especially for the fur seal (see
Swartzman and Haar 1983), reduced food availability
due to expansion of the pollock fishery has been sug-
gested as a possible cause of the decline in popula-
tions. The present population status of other pollock-
eating marine mammals in the Bering Sea is not
known.
The sizes of fishes consumed by marine mammals
are obviously very important for determining the
nature and magnitude of marine mammal-fishery
interactions. It is particularly important to recognize
that because of different feeding strategies, changes
8Pereyra, W. T., J. E. Reeves, and R. G. Bakkala. 1976. Demer-
sal fish and shellfish resources of the eastern Bering Sea in the
baseline year 1976. Processed Rep., 619 p. Northwest and Alaska
Fisheries Center, NMFS, NOAA, Seattle, WA.
Table 3.— Age-class distribution of walleye pollock con-
sumed by marine mammals in the Bering Sea, and caught
in the commercial fishery in 1978, based on length-at-age
data from Smith (1981).
Percent of fishes in age class
Predator species 1 23456789 >10
Harbor seal 43 20 23 3 0 3 3 6
Spotted seal 100 —
Ribbon seal 98 1 1 —
Steller sea lion 21 40 14 3 5 6 4 2 2 3
Fur seal1 49 44 7 —
Minke whale 100 — — — —
Commercial
fishery2 2 20 40 18 20 (>5 yr old)
1from McAlister et al. 1976.
2from Smith 1981.
in fish stock characteristics caused by fishing may
benefit some marine mammal species while having
no effect or being detrimental to others.
Acknowledgments
Support for this study was provided by the U.S.
Bureau of Land Management Outer Continental
Shelf Environmental Assessment Program and the
Federal Aid in Wildlife Restoration Program. Num-
erous colleagues, particularly John J. Burns and
Larry M. Shults, assisted in the collection and
processing of specimens. We are particularly grateful
to Donald G. Calkins, Thomas R. Loughlin, and
George Antonelis for providing us unpublished in-
formation. Graphics and statistical analyses were
done by Jesse Venable Clifford H. Fiscus made help-
ful comments on an earlier draft of the manuscript.
We also thank two anonymous reviewers whose com-
ments substantially improved the manuscript.
Literature Cited
Bakkala, R., K. King, and W. Hirschberger.
1981. Commercial use and management of demersal fish. In
D. W. Hood and J. A. Calder (editors), The eastern Bering
Sea shelf: oceanography and resources, Vol. 2, p. 1015-1036.
U.S. Dep. Commer., Off. Mar. Pollut. Assessment, NOAA,
Rockville, MD.
Braham, H. W., R. D. Everitt, and D. J. Rugh.
1980. Northern sea lion population decline in the eastern
Aleutian Islands. J. Wild]. Manage 44:25-33.
Bukhtiyarov, Y. A., K. J. Frost, and L. F. Lowry.
1984. New information on foods of the spotted seal, Phoca
largha, in the Bering Sea in spring. In F. H. Fay and G. A.
Fedoseev (editors), Soviet-American cooperative research on
marine mammals, Vol. 1 - Pinnipeds, p. 55-59. U.S. Dep.
Commer., NOAA Tech. Rep. NMFS 12.
Fiscus, C. H., G. A. Baines, and F. Wilke.
1964. Pelagic fur seal investigations, Alaska waters, 1962.
U.S. Fish Wildl. Serv., Spec Sci. Rep. Fish. 475, 59 p.
Fowler, C. W.
1982. Interactions of northern fur seals and commercial fish-
eries. Trans. N. Am. Wildl. Nat. Resour. Conf. 47:278-292.
Frost, K. J.
1981. Descriptive key to the otoliths of gadid fishes of the Ber-
ing, Chukchi, and Beaufort Seas. Arctic 34:55-59.
Frost, K. J., and L. F. Lowry.
1980. Feeding of ribbon seals (Phoca fasciata) in the Bering
Sea in spring. Can. J. Zool. 58:1601-1607.
1981a. Trophic importance of some marine gadids in north-
ern Alaska and their body-otolith size relationships. Fish.
Bull., U.S. 79:187-192.
1981b. Foods and trophic relationships of cetaceans in the Ber-
ing Sea. In D. W. Hood and J. A. Calder (editors), The
eastern Bering Sea shelf: oceanography and resources, Vol.
2, p. 825-836. U.S. Dep. Commer., Off. Mar. Pollut. Assess-
ment, NOAA, Rockville, MD.
1981c Ringed, Baikal, and Caspian Seals. In S. H. Ridgway
and R. J. Harrison (editors), Handbook of marine mammals,
Vol. 2, Seals, p. 29-53. Acad. Press, N.Y.
196
Lowry, L. R, and K. J. Frost.
1981. Feeding and trophic relationships of phocid seals and
walruses in the eastern Bering Sea. In D. W. Hood and J.
A. Calder (editors), The eastern Bering Sea shelf: oceanog-
raphy and resources, Vol. 2, p. 813-824. U.S. Dep. Commer.,
Off. Mar. Pollut. Assessment, NOAA, Rockville, MD.
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.
Nemoto, T.
1959. Food of baleen whales with reference to whale move-
ments. Sci. Rep. Whales Res. Inst. 14:149-291.
Pitcher. K. W.
1981. Prey of the Steller sea lion, Eumetopias jubatus, in the
Gulf of Alaska. Fish. Bull., U.S. 79:467-472.
SCHOENER, T W.
1971. Theory of feeding strategies. Annu. Rev. Ecol. Syst.
2:369-404.
Seaman, G A., L. F Lowry, and K. J. Frost.
1982. Foods of belukha whales (Delphinapterus leucas) in
western Alaska. Cetology 44:1-19.
Smith, G. B.
1981. The biology of walleye pollock. In D. W. Hood and J.
A. Calder (editors), The eastern Bering Sea shelf: oceanog-
raphy and resources, Vol. 1, p. 527-551. U.S. Dep. Commer.,
Off. Mar. Pollut. Assessment, NOAA, Rockville, MD.
SWARTZMAN, G. L., AND R. T HAAR.
1983. Interactions between fur seal populations and fisheries
in the Bering Sea. Fish. Bull., U.S. 81:121-132.
Kathryn J. Frost
Lloyd F Lowry
Alaska Department of Fish and Game
1300 College Road
Fairbanks, AK 99701
OCCURRENCE OF SOME PARASITES AND
A COMMENSAL IN THE AMERICAN LOBSTER,
HOMARUS AMERICANUS, FROM
THE MID-ATLANTIC BIGHT1
Larvae of the nematode Ascarophis sp. were
reported by Uzmann (1967b) from American lobsters
collected from Hudson, Block, Veatch, and Corsair
Canyons on the edge of the continental shelf east
and south of southern New England (Fig. 1). Follow-
ing parasitological examinations of over 3,000 coastal
and offshore lobsters, Uzmann (1970) reported that
the nematode larvae were restricted almost ex-
clusively to offshore lobsters. Adult Ascarophis sp.
are intestinal parasites of fishes (Uspenskaya 1953).
Although coastal and offshore lobsters occur off
Contribution No. 1277, Virginia Institute of Marine Science,
Gloucester Point, VA 23062.
northern and central New Jersey, coastal lobsters
are scarce or absent south of Cape May NJ. There
is an active offshore commercial lobster fishery along
the edge of the continental shelf south to Norfolk
Canyon (Fig. 1).
Materials and Methods
To determine whether offshore lobsters in the Mid-
Atlantic Bight have larval Ascarophis sp., we ex-
amined the guts of 218 American lobsters, Homarus
americanus, collected from August 1975 through
March 1977. Lobsters from this region had not been
examined previously for parasites.
One hundred and ninety-seven of the lobsters ex-
amined were caught in lobster traps or trawl nets
by commercial and research vessels in Norfolk and
Washington Canyons and from the shelf and slope
between and adjacent to those canyons (areas III-V,
Fig. 1) at depths of 73-402 m. The remaining 21
lobsters were caught by trawl nets from research
vessels off the coasts of Delaware and New Jersey
at depths of 57-95 m (area VIII, Fig. 1).
The intestines and rectum were excised from live
lobsters on shipboard (70% of the samples) or in the
laboratory at the Virginia Institute of Marine
Science, split longitudinally, and fixed in 10%
Formalin2 or in Davidson's fixative No free parasites
were found in the gut contents. In the laboratory,
the gut was transferred to 35% glycerine in 70%
ethanol, and part of the ethanol evaporated in a 55° C
oven. Pieces of the gut were then laid open, pressed
between two 35 x 50 mm slides, and examined for
the presence of cysts. This procedure followed the
recommendation of J. R. Uzmann3.
Results
Thirty-nine American lobsters were infected with
larval Ascarophis sp., encapsulated in the anterior
wall of the rectum (Table 1). The proportion of infec-
tion in 218 lobsters (17.9%) from the Mid-Atlantic
Bight was similar to that reported by Uzmann
(1967b), when examined in a 2 x 2 contingency table
and using Yates' correction for continuity (Elliott
1971). Uzmann (1967b) reported 77 infections in 314
lobsters (24.5%) collected east and south of southern
New England. However, Boghen (1978) reported in-
fection in the gills of 82 out of 233 lobsters (35.2%)
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
3J. R. Uzmann, Northeast Fisheries Center Woods Hole Labora-
tory, National Marine Fisheries Service, NOAA, Woods Hole, MA
02543, pers. commun. June 1974.
FISHERY BULLETIN: VOL. 84, NO. 1, 1986.
197
Figure 1— Canyons and lobster sampling sites along the edge of the continental shelf, between Cape Hatteras and the
eastern edge of Georges Bank.
198
Table 1. — Prevalence of American lobsters infected with
nematodes, Ascarophis sp., in the Mid-Atlantic Bight, August 1975-
March 1977.
No.
lobsters
sampled
Prevalence of
(No. infected)
infection (%)
Sexes
Sexes
Date
Area'
M
F
combined
M F
combined
Aug., Sept.
III
26(1)
236(6)
63(7)
3.8 16.2
11.1
1975
Dec. 1975
III
18(3)
18(2)
36(5)
16.7 11.1
13.9
Jan. 1975
III
3(1)
16(5)
19(6)
33.3 31.3
31.6
Jan. 1976
IV
11(1)
13(1)
24(2)
9.1 7.7
8.3
Apr. 1976
III
6(3)
9(2)
15(5)
50.0 22.2
33.3
Apr. 1976
V
4(2)
16(4)
20(6)
50.0 25.0
30.0
July 1976
V
7(1)
5(2)
12(3)
14.3 40.0
25.0
Oct. 1976
V
3(0)
5(2)
8(2)
0.0 40.0
25.0
Nov. 1976
VIII
11(1)
6(2)
17(3)
9.1 33.3
17.6
Mar. 1977
VIII
2(0)
2(0)
4(0)
0.0 0.0
0.0
Total
91(13)
127(26)
218(39)
14.3 20.5
17.9
1 III. Norfolk Canyon and adjacent slope
IV. Between Norfolk and Washington Canyons
V. Washington Canyon
VIM. Between Wilmington and Hudson Canyons.
2One 86 mm female contained 33 acanthocephalan cysts, Corynosoma sp.
from Northumberland Strait, southern Gulf of St.
Lawrence That higher proportion of infection was
highly significantly different from that reported off
southern New England and in the Mid-Atlantic
Bight.
Mid-Atlantic Bight lobsters examined for parasites
ranged from 49 to 179 mm carapace length (CL)
(Table 2). Larval Ascarophis sp. were found in 13
(14.3%) of 91 male lobsters and in 26 (20.5%) of 127
female lobsters. No significant difference in preva-
lence of infection between males and females, when
size was ignored, could be demonstrated with a 2
x 2 contingency table analysis. This agrees with the
absence of sex specificity in the canyon lobsters
Table 2.— Numbers of American lobsters examined and prevalence
of infection by the larvae of the nematode Ascarophis sp. in the
Mid-Atlantic Bight.
Size
range,
No.
examined
No.
infected
Percent
of group
Percent
of total
No.
larvae,
CL mm
M
F
Sum
M
F
Sum
infected
infected
range
40-49
0
2
2
0
2
2
100.0
0.9
1-12
50-59
5
7
12
2
1
3
25.0
1.4
1-9
60-69
9
21
30
1
8
9
30.0
4.1
1-13
70-79
27
29
56
4
7
11
19.6
5.0
1-4
80-89
20
37
57
2
4
6
10.5
2.8
1-5
90-99
16
19
35
3
3
6
17.1
2.8
1-8
100-109
7
8
15
1
1
2
13.3
0.9
2-3
110-119
2
2
4
0
0
0
120-129
2
1
3
0
0
0
130-139
0
0
0
0
0
0
140-149
1
1
2
0
0
0
150-159
0
0
0
0
0
0
160-169
1
0
1
0
0
0
170-179
1
0
1
0
0
0
Total
91
127
218
13
26
39
17.9
110-149
5
4
9
0
0
0
150-179
2
0
2
0
0
0
reported by Uzmann (1967b) and also reported from
Northumberland Strait by Boghen (1978).
Almost one-half (46.3%) of all infections occurred
in the 60-79 mm size classes; intensity of infection
ranged from 1 to 13 (mean 3.0) (Table 2). None of
the 11 lobsters >110 mm CL contained parasites.
Boghen (1978) reported 51.3% infection in the
60-69.9 mm range When the occurrences of para-
sites in males and females are arranged in three size
groups, 40-59, 60-79 and 80-109 mm, and statistically
examined with a 2 x 3 contingency table, no depar-
ture from the expected 1:1 ratio was observed.
A single specimen of the commensal polychaete,
Histriobdella homari, was obtained from the gills
of a female lobster, 82 mm CL, caught in Norfolk
Canyon in June 1974. Gills of four other lobsters
were excised, placed in dilute seawater in specimen
bowls, and refrigerated overnight. The polychaete
was found in the sediment collected from one gill.
Because of the small number of lobster gills ex-
amined, an estimate of prevalence is inappropriate
Previously, Histriobdella was reported by Uzmann
(1967a) in the gills and by Simon (1968) in the gills
and bodies of New England lobsters, and by Boghen
(1978) in the branchial chamber and gills of lobsters
from Northumberland Straits.
One female lobster, 86 mm CL, caught in Norfolk
Canyon in August 1975, was infected with cysts of
an acanthocephalan, Corynosoma sp. Thirty-three
cysts were found in the intestinal wall and in the
mesenteries along the outside of the intestine Adult
Corynosoma sp. are parasites of mammals and
aquatic birds; crustaceans are first intermediate
hosts and fishes are second intermediate hosts
(Yamaguti 1963).
According to Uzmann (1970), Corynosoma sp. is
a discriminator of coastal lobster stocks. Therefore
its presence in a lobster taken in Norfolk Canyon
indicates that migration from inshore to offshore
waters occurs. Montreuil (1954) reported that the
acanthocephalan infections in lobsters from the
Magdalen Islands, Gulf of St. Lawrence, varied with
the sex of the lobster and by season: 20% of females
and 20% of males had cysts seemingly acquired
towards the end of summer and early fall. Boghen
(1978) attributed the absence of cysts in his North-
umberland Strait samples to the fact that the lob-
sters were collected before the end of summer.
Discussion
The variety of animal parasites and their inten-
sity of infection are small in the Mid-Atlantic Bight
lobsters. Differences in the occurrence and rates of
199
infection of Ascarophis and Corynosoma and of the
commensal Histriobdella reported from American
lobsters of the Mid-Atlantic Bight, southern New
England waters, and the Gulf of St. Lawrence, are
not large and could be attributed to differences in
sample sizes or season of sampling. Peculiarly, cysts
of the sporozoan Porospora sp. were not seen in Mid-
Atlantic Bight lobsters, but occurred in most lobsters
in the Gulf of St. Lawrence (Montreuil 1954; Boghen
1978) and were reported by Uzmann (1970) from
southern New England waters. Cysts of the trema-
tode Stichocotyle sp. were reported by Nickerson
(1895) from Penobscot Bay, ME, and from lobster
dealers in Boston, MA; by Linton (1940) from an un-
stated region, probably Woods Hole, MA; by Uzmann
(1970) from southern New England waters; and by
Montreuil (1954) from southern Nova Scotia or
southeastern New Brunswick. Nickerson (1895)
found the cysts only in the intestinal tract at the
union of the intestine and rectum.
Literature Cited
Boghen, A. D.
1978. A parasitological survey of the American lobster
Homarus americanus from the Northumberland Strait,
southern Gulf of St. Lawrence Can. J. Zool. 56:2460-2462.
Elliott, J. M.
1971. Some methods for the statistical analysis of samples of
benthic invertebrates. Freshw. Biol. Assoc, Sci. Pub. 25, 148
P-
Linton, E.
1940. Trematodes from fishes mainly from the Woods Hole
region, Massachusetts. Proa U.S. Natl. Mus. 88:1-172.
Montreuil, P.
1954. Parasitological investigations. Rapp. Ann. Stn. Biol.
Mar. Dep. Peches Quebec, Contrib. 50:69-73.
Nickerson, W. S.
1895. On Stichocotyle nephropsis Cunningham, a parasite of
the American lobster. Zool. Jahrb., Abt. Anat. Ontog. Tiere
8:447-480.
Simon, J. L.
1968. Incidence and behavior of Histriobdella homari (An-
nelida: Polychaeta), a commensal of the American lobster.
Bioscience 18:35-36.
Uspenskaya, A. B.
1953. The life cycle of nematodes of the genus Ascarophis van
Beneden (Nematodes - Spirurata). [In Russ.] Zool. Zh. 32:
828-832. (Translated by J. M. Moulton, Bowdoin College,
Brunswick, ME, 1966).
Uzmann, J. R.
1967a. Histriobdella homari (Annelida:Polychaeta) in the
American lobster, Homarus americanus. J. Parasitol. 53:
210-211.
1967b. Juvenile Ascarophis (Nematoda:Spiruroidea), in the
American lobster, Homarus americanus. J. Parasitol. 53:
218.
1970. Use of parasites in indentifying lobster stocks. (Abstr.)
In Section II, Proceedings of the Second International Con-
gress of Parasitology, p. 349. J. Parasitol. 56(4).
Yamaguti, S.
1963. Classification of the Acanthocephala. Systema Helmin-
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W. A. Van Engel
R. E. Harris, Jr.
D. E. Zwerner
Virginia Institute of Marine Science
School of Marine Science
College of William and Mary
Gloucester Point, VA 23062
RESILIENCE OF THE FISH ASSEMBLAGE
IN NEW ENGLAND TIDEPOOLS1
Factors regulating density and species composition
of tidepool fishes have been little studied, partic-
ularly in comparison to other elements of the inter-
tidal community (Gibson 1982). Twenty-two collec-
tions of fishes were made in two tidepools at the
Marine Science and Maritime Studies Center of
Northeastern University at Nahant, MA, during
summers from 1967 to 1985. Initially, the purpose
was simply to demonstrate to my summer class in
ichthyology the technique of collecting fishes with
rotenone. After several years, it became apparent
that there would be interest in examing long-term
effects of repeated poisoning of the same pools. The
purpose of this paper is to report the data from this
series of samples and to compare the resilience of
this New England tidepool fish fauna with studies
done in the Gulf of California (Thomson and Lehner
1976), the central California coast (Grossman 1982),
and South Africa (Beckley 1985). Unfortunately,
there are no other similar tidepools in the area, so
it was not possible to make control collections from
unsampled pools.
Methods
The same two tidepools were sampled each sum-
mer from 1967 to 1985. The tidepools are located
on the ocean side of East Point, in Broad Sound. The
higher pool is at about 2 m elevation and is about
1 m deep at high tide; the lower pool is slightly below
1 m elevation, contains extensive red and brown algal
growth, and is shallower. Average tidal amplitude is
slightly over 3 m. One collection was made each year
except for 1969, 1982, and 1983 when two collections
were made, spaced about 2 wk apart. Collections
'Contribution No. 134 from the Marine Science Institute, North-
eastern University, Nahant, MA 01908.
200
FISHERY BULLETIN: VOL. 84, NO. 1, 1986.
were made with rotenone (about 1 qt Noxfish2) at
low tide in August, except in 1983 and 1985, when
they were made in July and in 1984 when they were
made in September. Specimens were taken by dip
net from the pools by my students and me An at-
tempt was made to collect and then count and
measure (mm SL) all fishes. Sometimes I used a face
mask to find fishes at the bottom of the pool which
was closer to the ocean. Many invertebrates also
were killed, but no attempt was made to record num-
bers. The most abundant invertebrates in the 1984
collection were the green crab, Carcinus maenas
(Linnaeus), and the sea urchin, Strongylocentrotus
droebachiensis (Miiller). Also collected were amphi-
pods, Gammarellus angulosus (Rathke), Calliopius
laeviusculus (Kroyer), and Gammarus oceanicus
Segerstrale; isopods, Idotea baltica (Pallas); and scale
worms, Harmothoe imbricata (Linnaeus).
Results
Thirteen species of fishes were collected (Table 1).
The number of species per collection varied from 3
to 8 (x 5.3). One species, the rock gunnel, Pholis gun-
nellus (Linnaeus), was collected in all 22 samples.
Young cunner, Tautogolabrus adspersus (Walbaum),
were found in all but two collections. The grubby,
Myoxocephalus aenaeus (Mitchill), and the threespine
stickleback, Gasterosteus aculeatus Linnaeus, were
present in 17 and 15 collections, respectively. The
radiated shanny, Ulvaria subbifurcata (Storer), was
taken 12 times. The seasnail, Liparis atlanticus (Jor-
dan and Evermann), was taken in 10 collections, the
mummichog, Fundulus heteroclitus Linnaeus, in 8.
The American eel, Anguilla rostrata (LeSueur), was
taken four times; young lumpfish, Cyclpterus lum-
pus Linnaeus, three times. Four of the 13 species
were taken only once or twice: the Atlantic tomcod,
Microgadus tomcod (Walbaum); Atlantic silverside,
Menidia menidia (Linnaeus); ninespine stickleback,
Pungitius pungitius (Linnaeus); and northern
pipefish, Syngnathus fuscus Storer. I can detect no
long-term change in species composition or number
of individuals over the 19-yr period.
The number of specimens per sample varied from
17 to 1,850 (x 197.5), but the mean is distorted by
the 1,842 young (9-28 mm SL) Tautogolabrus adsper-
sus taken in sample 16. Deleting this number, the
figures are 17-343 (x 119.2). Thus, a "typical" sam-
ple would consist of 41 Pholis gunnellus, 49 young
Tautogolabrus adspersus, 12 Myoxocephalus aenaeus,
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
7 Gasterosteus aculeatus, and 2 Fundulus
heteroclitus. One other species might be present, 1
or 2 specimens of any of the other 8 species, most
likely Ulvaria subbifurcata or Liparis atlanticus.
There is great variation from collection to collec-
tion in numbers of specimens of the most abundant
4 species: 2-232 Pholis gunnellus; 2-1,842 Tauto-
golabrus adspersus; 1-127 Myoxocephalus aenaeus;
and 1-44 Gasterosteus aculeatus. Ulvaria subbifur-
cata, Liparus atlanticus, Cyclopterus lumpus, and
Fundulus heteroclitus showed much less variation,
1-12 per collection. The other 5 species were uncom-
mon, numbering 1-4 specimens.
Discussion
To evaluate short-term effects, comparisons can
be made between pairs of collections made in 1969,
1982, and 1983 at 2-3 wk intervals. The number of
species decreased from 8 to 6 in the 1969 pair and
from 7 to 5 in 1982, but the number increased from
3 to 5 in 1983. Four of the 8 species in the first sam-
ple in 1969, and 3 of the 7 species in the first sam-
ple in 1982, numbered only 1 or 2 specimens, as did
one of the species in the second sample of 1983.
Numbers of individuals were about the same in the
1969 pair of collections (over 50) and the 1983 pair
(74 and 86), but decreased (54 to 17) in the second
collection of the 1982 pair. Rapid recolonization of
the tidepools clearly takes place. Differences in thor-
oughness of collecting, plus apparent random varia-
tion in the 7 least commonly taken species, can
explain the few differences between the paired
collections.
Thomson and Lehner (1976) sampled a large tide-
pool in the Gulf of California 11 times over the period
1966-73. The period of time between sampling
ranged from 13 to 78 wk. Number of species ranged
from 16 to 26, total 50; number of individuals 435-
2,627, total 11,701. No decrease in number of species
or individuals over time is apparent from their data
(Thomson and Lehner 1970:table 1).
Grossman (1982) sampled a series of rocky tide-
pools with quinaldine at Dillon Beach in northern
California 15 times from January 1979 to May 1981.
The period of time between sampling ranged from
4 to 21 wk. Number of species per sample varied
from 9 to 18 (excluding the first sample, 12-18), total
29 species; number of individuals was 71-517 per
sample [not 520 as in Grossman's (1982) table 3],
total 2,853 individuals. The structure of this rocky
intertidal fish taxocene was persistent over 29 mo
through 15 defaunations (Grossman 1982:table 3).
Beckley (1985) sampled three South African pools
201
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203
with rotenone over a 2-yr period at intervals of 1 mo,
3 mo, and 6 mo. She found rapid recolonization but
with lower densities of recolonizers in winter than
in summer. During 26 monthly samples, only one of
the original species did not recolonize the pool, while
13 additional species were found. In Pool 2, which
was sampled in 3-mo intervals, 14 species were taken
in the initial sample, 7-12 in subsequent samples.
Three of the original 14 species failed to recolonize,
but 8 additional species were taken. During four
repeat visits to Pool 3, the number of species varied
between 9 and 14, all but 1 species recolonized the
pool, and 5 additional species were recorded.
My study and those of Thomson and Lehner
(1976), Grossman (1982), and Beckley (1985) indicate
great resilience of species of tidepool fishes in
tropical and temperate waters. Recolonization is
quite rapid, within a matter of weeks.
Acknowledgments
I thank the students and teaching assistants in my
ichthyology course for helping to collect the material.
James Dooley made the second 1982 collection. N.
W. Riser of the Marine Science and Maritime Studies
Center identified the invertebrates. Comments on
drafts of this note were provided by G. D. Grossman,
J. Randall, N. W. Riser, V. G. Springer, and A. B.
Williams.
Literature Cited
Beckley, L. E.
1985. Tidepool fishes: Recolonization after experimental elim-
ination. J. Exper. Mar. Biol. Ecol. 85:287-295.
Gibson, R. N.
1982. Recent studies on the biology of intertidal fishes.
Oceanogr. Mar. Biol. Ann. Rev. 20:363-414.
Grossman, G. D.
1982. Dynamics and organization of a rocky intertidal fish
assemblage: the persistence and resilience of taxocene struc-
ture Am. Nat. 119:611-637.
Thomson, D. A., and C. E. Lehner.
1976. Resilience of a rocky intertidal fish community in a
physically unstable environment. J. Exper. Mar. Biol. Ecol.
22:1-29.
Bruce B. Collette
Marine Science and
Maritime Studies Center,
Northeastern University,
Nahant, MA 01908
and
Systematics Laboratory,
National Marine Fisheries Service,
National Museum of Natural History,
Washington, DC 20560
PARASITES OF BENTHIC AMPHIPODS:
CILIATES
Benthic gammaridean amphipods were sampled dur-
ing a 2V2-yr period as a part of the Northeast Moni-
toring Program (NEMP) of the Northeast Fisheries
Center, National Marine Fisheries Service The am-
phipod survey was designed to determine the kinds
of parasites and pathological conditions occurring
in amphipod populations that live in and on the
sediments of the continental shelf from Maine to
North Carolina. Microsporidans of the sampled am-
phipods have been discussed by Johnson (1985), and
this paper presents and discusses data on host
distribution, prevalence, effects on the host, and
probable relationships, of ciliates parasitizing am-
phipods from the same samples.
Materials and Methods
Benthic amphipods were collected from 35 sta-
tions, mainly on the Georges Bank and Mid-Atlantic
Bight (Fig. 1). Amphipods were sampled during 11
cruises, July 1980-November 1982 (Table 1). Each
station was sampled from 1 to 10 times during the
survey. The 11 stations indicated by solid circles on
Figure 1 had the most consistent and numerous
populations of amphipods, were sampled at least five
times each, and yielded the majority of data
presented here A Smith-Mclntyre grab and occa-
sionally an epibenthic sled or scallop dredge were
used to obtain the samples. Up to 30 individuals of
each species present in a sample, and sometimes
more depending on numbers present, were prepared
for histological study. Details of collecting pro-
cedures and preparation of the amphipods for study
are given by Johnson (1985).
Results
Host and geographic distribution of ciliate infec-
tion is given in Table 1. Ciliate-infected amphipods
were taken in samples from at least one station on
every cruise There was no indication that prevalence
was influenced by the season of the year or location
of the positive stations. The majority of infected
specimens were Ampelisca agassizi (Judd), but
prevalence of ciliate infection was lower in A. agassizi
than in the other species found infected (Pontogeneia
inermis Kr0yer, Phoxocephalus holbolli Kr0yer, Har-
pinia propinqua Sars, and unidentified haustoriids)
(Table 2). In three instances, at station 33, cruise G;
station 48, cruise I; and station 57, cruise E, in-
dividuals ofH. propinqua or P. holbolli were infected
204
FISHERY BULLETIN: VOL. 84, NO. 1
50 100 150 200
KILOMETERS
68°
40-
36-
Figure 1.— Number designations and positions of Northeast Monitoring Program (NEMP) benthic stations where gammaridean am-
phipods were sampled during the survey.
but A. agassizi collected at the same times were not.
Except for A. agassizi, all the species with ciliate
infections were rare (Table 2). The most numerous
species collected, after A. agassizi, were Leptochei-
rus pinguis Stimpson, which made up 11% of the
total collected (2,655/24,244), and Unciola species
(probably all U. irrorata Say and U. inermis Shoe-
maker), which made up 10% of the total (2,356/
24,244). Despite their abundance, these species were
never found infected with ciliates. Considering all
amphipods sectioned and examined, overall
prevalence of ciliate infection was 0.6% (41/7,363).
Light infections consisted mainly of large ciliates.
Heavier infections had medium to small ciliates, but
205
Table 1.— Stations with ciliate-infected amphipods, by cruise and
host species.
Cruise1
Station
A
B
C
D
E
F
G
H
1
J K
20
P|2
3
23
AA*
AA
AA
—
—
AA
—
—
25
—
PH2
33
—
AA
AA
AA
AA
AA
HP2
—
—
35
—
AA
—
AA
—
—
—
AA
37
AA
38
—
—
AA
—
48
—
AA
—
—
HP
49
AA
50
AA
51
AA
AA
—
57
—
—
—
—
AA
PH
—
AA
AA
62
HAU2
—
—
—
—
78
—
—
HAU
'Dates of cruises: A, July 1980; B, Sept. 1980; C, Dec. 1980; D, Apr 1981;
E, July 1981; F, Aug. 1981; G, Nov. 1981; H, Jan. 1982; I, Mar 1982; J, Aug.
1982; K, Nov. 1982
2lnfected amphipods present at the station PI = Pontogeneia inermis, AA
= Ampelisca agassizi, PH = Phoxocephalus holbolli, HP = Harpinia propin-
qua, HAU = unidentified haustoriids.
3— = station sampled, no ciliate Infections found.
sometimes large forms were also present. The
largest ciliates were in the gill of a specimen of Pon-
togeneia inermis (Fig. 2). Measured in paraffin sec-
tions, they were about 17 ^m x 80 ^m. Large forms
in other infected amphipods were 16-20 jjm x 40-50
jim. The majority of small- and medium-sized ciliates
were 17-30 ^m in the greater dimension; none were
less than 14 fiin (Fig. 3). Ciliates were elongate-
spindle-shaped, with pointed or sharply rounded
ends in P. inermis, and oval to subspherical in the
other amphipods. The macronucleus of the large
ciliates in P. inermis was sometimes ribbonlike (Fig.
2), and macronuclei of the smaller ciliates in P. in-
ermis and those from the other amphipod species
were elongate cylinders or elongate ovals in section
(Fig. 3).
None of the infections showed recent evidence of
host reaction against the ciliates. The melanized
nodules and small hemocytic encapsulations occa-
sionally seen in infected amphipods did not contain
recognizable ciliates, and may have been due to other
causes.
Few pathological effects were visible in ciliate-
infected tissues. Two infected subadult males of A.
agassizi had karyorrhexis and probable lysis in the
transverse abdominal muscles, and one heavily in-
fected female of A. agassizi, which had a few early
embryos in the brood pouch, also had retained
necrotic, mature ova in the ovaries. All infected am-
phipods had material in the gut, indicating that
feeding was continuing. Hemocytes were present in
Figure 2 — Pontogeneia inermis: large and
small ciliates in the gill. L, large form; S, small
form. Bar = 10 /im.
>
.1
206
r
%
#
<
Figure 3.— Ampelisca agassizi: medium-sized
ciliates. The small, pale micronucleus is visible
close to the macronucleus in one of the ciliates
(arrow). Bar = 10^m.
light to medium infections, but essentially missing
in heavy infections. None of the ciliates were posi-
tioned in such a way that they appeared to have been
phagocytizing hemocytes or other cells at the time
of fixation. The granular inclusions commonly pres-
ent in the cytoplasm of the ciliates bore no resem-
blance to food vacuoles or phagocytized material.
Discussion
Two groups of ciliates contain species that para-
sitize crustaceans. Paranophrys, in crabs, lobsters,
and possibly isopods, and Parauronema, in penaeid
shrimp, belong in the class Oligohymenophora, order
Scuticociliatida (Corliss 1979). They are apparently
opportunistic parasites (Bang 1970; Sindermann
1977; Couch 1978; Armstrong et al. 1981; Hibbits
and Sparks 1983). The remaining parasites are
members of the class Kinetofragminophora, order
Apostomatida (Corliss 1979). Typical apostomes are
obligate commensals of aquatic crustaceans and have
a life cycle geared to their hosts' molting cycles
(Bradbury 1966, 1973), but some apostomes have
become internal parasites of various invertebrates,
including polychaetes, cephalopods, ophiurans,
coelenterates, ctenophores, and isopod, amphipod,
and decapod crustaceans (Corliss 1979).
Because specialized fixation and staining of whole
Table 2.— Species of amphipods infected by ciliates: proportion of the amphipod
population and prevalence of ciliate infection.
Species of amphipod
Percent prevalence
at positive stations
Proportion of the total
amphipods collected
Ampelisca agassizi
Harpinia propinqua
Haustoriidae spp.
Phoxocephalus holbolli
Pontogeneia inermis
3.8% (31/812)
18.2% (2/11)
5.4% (3/56)
9.5% (2/21)
10.3% (3/29)
54.3% (13,165/24,244)
0.6% (146/24,244)
0.9% (225/24,244)
0.5% (125/24,244)
0.7% (164/24,244)
207
ciliates is necessary for firm identification (Corliss
1979), the amphipod ciliates can be only provision-
ally assigned to a ciliate group, as is true in other
studies based on fixed and embedded material
(Sparks et al. 1982; Hibbits and Sparks 1983). On
the basis of similarities in hosts and morphology, the
amphipod ciliates discussed here are like the apos-
tome genus Collinia, whose members parasitize am-
phipods (Summers and Kidder 1936; de Puytorac
and Grain 1975). Like Collinia, size of individual
ciliates from the benthic amphipods varied greatly
and there was no indication that the ciliates were
phagocytic Paranophrys and Parauronema, on the
other hand, belong to a group that ingests particu-
late material. Paranophrys is known to ingest
hemocytes and other cells of its hosts, and does not
exhibit major size differences (Bang 1970; Sparks
et al. 1982; Hibbits and Sparks 1983). Provisionally,
the ciliates of benthic amphipods are being con-
sidered apostomes.
Whether more than one species of ciliate was in-
volved in the infections is uncertain, but probably
the ciliate of Pontogeneia inermis represented a
species apart from the others. Its very large forms
with the ribbonlike macronucleus were not dupli-
cated in other infections.
Although more A. agassizi were found infected
with ciliates than any other species of amphipod, this
was apparently because it was the most abundant
and widespread of the susceptible species sampled.
A. agassizi had the lowest overall prevalence of ciliate
infection and sometimes was not parasitized when
other species in the same samples were parasitized.
There are at least two possible explanations for the
odd host distribution of the amphipod ciliates. First,
the ciliates might be highly host specific, each am-
phipod species having its own species of ciliate Sec-
ond, the ciliates might be either primary parasites
of some other member(s) of the benthic community,
or incompletely adapted to a parasitic existence, and
thus only occasionally parasitizing the least resis-
tant species of the sampled amphipods. Unciola
species and Leptocheirus pinguis were often the
most abundant amphipods at certain stations, but
ciliates were never found in individuals of these
species, suggesting that they are resistant to ciliate
attack. Conversely, the relatively high prevalence of
ciliates in the rare species of amphipods could in-
dicate less resistance than is exhibited by most of
the species of amphipods sampled.
Presumably, infected amphipods would eventually
die of their ciliate infections because of the massive
loss of hemocytes. The infrequency of ciliate infec-
tion, except in certain rare species, indicates that
these parasites are not important in regulating the
general amphipod populations they infect.
Acknowledgments
Thanks are due the following: Frank Steimle and
Robert Reid of the Northeast Fisheries Center,
Sandy Hook Laboratory, and Linda Dorigatti, Gret-
chen Roe, and Sharon MacLean of the Oxford
Laboratory collected the amphipods; Ann Frame,
Sandy Hook Laboratory, provided advice and train-
ing in identification of amphipods; Linda Dorigatti
identified material from cruises A to C, and she,
Gretchen Roe, Dorothy Howard, and Cecelia Smith,
Histology Section, Oxford Laboratory, prepared the
specimens for histological examination.
Literature Cited
Armstrong, D. A., E. M. Burreson, and A. K. Sparks.
1981. A ciliate infection (Paranophrys sp.) in laboratory-held
Dungeness crabs, Cancer magister. J. Invertebr. Pathol.
37:201-209.
Bang, F. B.
1970. Disease mechanisms in crustacean and marine arthro-
pods. In S. F. Snieszko (editor), a Symposium on Diseases
of Fishes and Shellfishes, p. 383-404. Am. Fish. Soc, Wash.,
D.C., Spec Publ. No. 5.
Bradbury, P. C.
1966. The life cycle and morphology of the apostomatous
ciliate, Hyalophysa chattoni n.g., n. sp. J. Protozool. 13:
209-225.
1973. The fine structure of the cytostome of the apostomatous
ciliate Hyalophysa chattoni. J. Protozool. 20:405-414.
Corliss, J. O.
1979. The ciliated Protozoa. Characterization, classification
and guide to the literature 2d ed. Pergamon Press, Ox-
ford, 455 p.
Couch, J. A.
1978. Diseases, parasites, and toxic responses of commercial
penaeid shrimps of the Gulf of Mexico and South Atlantic
coasts of North America. Fish. Bull., U.S. 76:1-44.
de Puytorac, P., and J. Grain.
1975. Etude de la tomitogenese et de l'ultrastructure de Col-
linia orchestiae, cilie apostome sangnicole, endoparasite du
crustace Orchestia gammarella Pallas. Protistologica 11:
61-74.
Hibbits, J., and A. K. Sparks.
1983. Observations on the histopathology caused by a parasitic
ciliate (Paranophrys sp.?) in the isopod Gnorimosphaeroma
oregonensis. J. Invertebr. Pathol. 41:51-56.
Johnson, P. T.
1985. Parasites of benthic amphipods: microsporidans of
Ampelisca agassizi (Judd) and some other gammari-
deans. Fish. Bull., U.S. 83:497-505.
Puytorac, P. de, and J. Grain, See de Puytorac, P., and J.
Grain.
Sindermann, C. J.
1977. Ciliate disease of lobsters. In C. J. Sindermann (editor),
Disease diagnosis and control in North American marine
aquaculture, p. 181-183. Elsevier Sci. Publ. Co, Amsterdam.
208
Sparks, A. K., J. Hibbits, and J. C. Fegley.
1982. Observations on the histopathology of a systemic ciliate
(Paranophrys sp.?) disease in the Dungeness crab, Cancer
magister. J. Invertebr. Pathol. 39:219-228.
Summers, F. M., and G. W. Kidder.
1936. Tkxonomic and cytological studies on the ciliates asso-
ciated with the amphipod family Orchestiidae from the
Woods Hole district. II. The coelozoic astomatous parasites.
Arch. Protistenkd. 86:379-403.
Phyllis T. Johnson
Northeast Fisheries Center Oxford Laboratory
National Marine Fisheries Service, NOAA
Oxford, MD 21654
FECUNDITY OF THE PACIFIC HAKE,
MERLUCCIUS PRODUCTUS,
SPAWNING IN CANADIAN WATERS
Previous studies on the fecundity of Pacific hake,
Merluccius productus, have been concentrated on the
coastal stock in Baja California (MacGregor 1966,
1971; Ermakov et al. 1974), although large-scale
spawning events have been recorded as far north as
lat. 38°N, near San Francisco, CA (Stepanenko
1980). The present work was undertaken in conjunc-
tion with ichthyoplankton surveys, aimed at esti-
mating the released egg production and spawning
biomass of the Pacific hake stock resident in the
Strait of Georgia, a semi-closed marine basin in
British Columbia (Thomson 1981). The spawning
season extends from February through June, peaks
in early April, and is 90% complete by mid-May
(Mason et al. 1984).
In comparison with the coastal stock of some 1-2
million metric tons (t) (Bailey et al. 1982), this in-
shore stock, of about 140,000 t, is subject to modest
annual exploitation (1-500 t) and resides in a semi-
estuarine environment on the known northernmost
edge of the reproductive range. The coastal stock
undertakes a northward feeding migration after the
spring spawning and reaches the southwest coast of
Vancouver Island by late summer (Bailey et al. 1982).
There is no evidence of intermingling between these
two stocks, based on their distributional patterns.
The inshore stocks in the Strait of Georgia and Puget
Sound may undergo some exchange, possibly due to
surface transport of larvae produced in the central
Strait of Georgia (Mason et al. 1984). The Puget
Sound and coastal stocks have been identified as
genetically distinct by Utter and Hodgins (1971),
but the two inshore stocks in Puget Sound and
the Strait of Georgia have not been similarly com-
pared.
Histological analysis has indicated that only one
mode of oocytes developes in Georgia Strait hake.
However, like the Baja, California form and hake
species elsewhere, some Strait of Georgia hake show
evidence of ovarian resorption following spawning
(Foucher and Beamish 1980). The quantitative sig-
nificance of resorption relative to individual and
stock fecundities, or to their potential physiological
and environmental correlates have not yet been ex-
amined. This report considers the "apparent fecun-
dity" as an annual expression of reproductive poten-
tial applicable to the stock in the Strait of Georgia,
determines that fecundity, and concludes that
ovarian resorption is of minor consequence in the
stock.
Materials and Methods
The ovaries of 97 Pacific hake females 39-82 cm
FL were collected during late February and early
March of 1980 and 1981, 71 of which were collected
in 1981 (McFarlane et al. 1983). Unspawned females
were selected in maturity stages R2 and R (Foucher
and Beamish 1977) when the ovary is yellow and
opaque, has prominent blood vessels, and fills one-
third to one-half of the coelomic cavity. No ovaries
contained translucent oocytes which signify immi-
nent spawning. Fresh ovaries were preserved in 10%
formaldehyde solution. In the laboratory, the pre-
served ovaries were transferred to modified (Simp-
son 1951) Gilson's fluid for several months to allow
breakdown of connective tissue
Ovaries were then washed thoroughly in cold water
over a series of stainless steel screens of 40 jum and
larger aperture, and gently broken up by hand when
necessary to separate the hardened eggs from the
ovarian tissue The mesh size of the finest screen was
determined by the difficulty encountered in separ-
ating oocytes <40 ^m diameter from ovarian tissue
The cleaned eggs were then stored in 5% formal-
dehyde solution in preparation for analysis.
Eggs from a single ovary were transferred to a
20 L glass reservoir filled to either 10 or 15 L. While
the reservoir was being stirred vigorously with a
wooden paddle in a rotating figure-eight pattern, a
second worker extracted 50 1-2 mL volumetric sub-
samples using Stempel pipettes and transferred
them to petri dishes. Under the dissecting micro-
scope at 50 x magnification, all eggs in five subsam-
ples were sized and counted in 20 /urn intervals of
oocyte diameter. These results were then combined
to construct oocyte size-frequency histograms and
FISHERY BULLETIN: VOL. 84, NO. 1, 1986.
209
to allot proportions of the combined egg count to
the various size intervals. All eggs were counted in
the remaining 45 subsamples to provide with the
previous 5 subsamples, 50 counts of eggs per unit
volume The total number of eggs in the ovary was
calculated from the product of mean subsample
count per milliliter and the reservoir volume prior
to subsampling. The number of eggs in various size
categories was obtained by applying the appropri-
ate proportional value to the estimated total number
of eggs in the ovary. Subsample egg counts averaged
between 50 and 150 eggs, with the majority falling
within 75 and 100. Size-frequency histograms were
based on 250-750 sized eggs with the majority bas-
ed on 375-500 sized eggs. Initial procedural evalua-
tion indicated that 200 sized eggs was sufficient to
obtain a replicable size-frequency distribution.
Eighteen ovaries from postspawned females
were collected on 3 July 1981 and were similarly
processed.
Prespawning females collected in 1981 were ag-
ed by the otolith break and burn method (Chilton and
Beamish 1982).
Results and Discussion
Frequency Distributions of
Oocyte Diameter for Prespawners
Most of the 97 ovaries of prespawners examined
contained a pronounced bimodal distribution of
oocyte diameters with peaks at about 100 p*m and
between 500 and 600 ^m (Figs. 1-3). Oocytes <150
jjm in diameter contained no yolk materials and are
taken to constitute a reserve fund for subsequent
years (Foucher and Beamish 1980). Oocytes >150 ^m
diameter were undergoing vitellogenesis, and a few
ovaries contained nonhydrated oocytes reaching
700-750 nm diameter. Hydrated eggs were not seen
in these ovaries collected in early March and hydra-
tion probably does not occur in oocytes <700 /urn,
although hydrated oocytes from 350 to 950 /^m
diameter were found by Foucher and Beamish
(1980). This apparent discrepancy may reflect their
underestimation of oocyte diameters in histological
preparations of translucent oocytes due to the plane
of sectioning.
The unimodal distribution of yolked oocytes, also
reported for M. m. hubbsi in the Argentine Sea
(Christiansen and Cousseau 1971) does not comple-
ment the findings of MacGregor (1966, 1971). He
found that ovaries of prespawning coastal hake taken
off Baja California contained distinct groups of
"small" and "large" yolked oocytes, of which only the
latter were destined for release Furthermore, Er-
makov et al. (1974) reported 21% of the 93 female
Pacific hake taken off Baja California in 1972 had
unimodal, 55% bimodal, 18% trimodal, and 6%
quadrimodal oocyte distributions. Similarly, their
subsequent sample of 45 ovaries collected in the
Oregon-Washington region in late November contain-
ed 22% unimodal, 65% bimodal, and 6% trimodal
distributions, with major peaks at 200 and 600 /um
diameter. Nearly half of the ovaries collected and ex-
amined by Ermakov et al. (1974) did not contain a
bimodal distribution of yolked oocytes, although
these authors concluded that asynchronous develop-
ment of yolked oocytes indicated the probability of
multiple spawnings, most likely two batches within
the spawning season.
Estimates of Total Fecundity
Standard errors of mean egg counts for total
fecundity estimates of total fecundity (oocytes ^40
(jm diameter) ranged between 0.4 and 4.4% of the
means and were <3% in nearly 70% of the 97 ovaries
processed. The variability of the enumeration tech-
nique compares favorably with that reported by
Mason et al. (1983) in an analysis of the fecundity
of the sablefish, Anoplopoma fimbria, and with that
reported by Pitt (1963) on the fecundity of the
American plaice Hippoglossoides platessoides, using
Wiborg's whorling vessel (Wiborg 1951).
The estimates of total fecundity (oocytes ^40 ^m
diameter) increased with fork length according to
the equation F = 0.3081FL3-7605, [where FL = fork
length in centimeters]. The correlation coefficient
(r) for the regression was 0.93. An insignificant F
ratio from analysis of variance of slope and inter-
cept values allowed pooling of the 1980 and 1981
data.
The smallest and largest Pacific hake females in
the sample (39 and 82 cm FL) contained estimated
total oocyte complements of 202,100 and 3,009,900
oocytes >40 ^m, respectively. All 97 fecundity esti-
mates fell within the range of 165,700 and 3,108,000
oocytes ^40 \xm.
Estimates of Fecundity Within
Size Classes of Oocytes
The estimated number of oocytes with 20 \xm in-
tervals of diameter were summed within five inter-
vals and regressed against fork length to examine
the correlation coefficients (Table 1). Coefficients
declined progressively with increased oocyte
diameter, reflecting increasing variability among
210
18
16
14 -
12
10-
8 -
6-
4
2
0
18
16
14-
12
10-
8
6
4-
2-
0
18 -
Z
UJ 14-
o
UJ
IT
U.
I- 8-
2
O 6
<r
UJ 4.
0.
2.
0
18
16
14
12
10
8
6
4
2
0
18
16
14 -
12-
10
39 cm
39 cm
18-
16
14
12
10-
e
6
39cm
40cm
40cm
4 I cm
43cm
Mi|.i.iii.|iiipii ,
44 cm
o\^m
1 1 —
0 2 4 6 8 10
41 cm
JlLi LI
42 cm
43 cm
45cm
illinium
18-
16
14
12 -
10
8
6
4-
2
41 cm
18
16-
14
12"
10
jjyu
42 cm
Lil
18-
16
14
12
10
8
6
43cm
18
16
M-
12-
10-
8-
6-
4-
2
45cm
6 8 10
0 2 4 6
41 cm
1 n . 1 4ml
42 cm
Jipli
44 cm
I|IniI.i|IiIiI.I
46cm
0 2 4 6 8 10
OOCYTE DIAMETER t/*m x I0Z)
Figure 1— Representative frequency distributions of oocyte diameter from ovaries of Pacific hake 39-46 cm FL.
211
47cm
47cm
16-
14 -
12
10-
8
6
48cm
48cm
IB
16-
14
12-
IN
8-
6
4
2
49cm
1 lllllll illill
49cm
18
16
14'
12-
10-
8
6-
50 cm
51cm
Jii
ill
UIL
u
z
16
16-
51 cm
51cm
18
16
14-
12
10
52 cm
52 cm
1*41
18
16
14
12
10
8
6-
52 cm
JJMli
52 cm
53 cm
LJUli
53 cm
is
16-
12-
10
53 cm
ILlI
Ik
0 2 4 6
54 cm
miM> .
18
16
14
12-
10
8-
6-
54 cm
wJjLP
0 2 4 6 8 10
0 2 4 6 8 10
54cm
0 2 4 6 e 10
OOCYTE DIAMETER (Jim « I0Z)
Figure 2— Representative frequency distributions of oocyte diameter from ovaries of Pacific hake 47-54 cm FL.
212
12
10-
>-
o
o
cc
o
LL
56 cm
Uiliiii
59 cm
62 cm
69 cm
57 cm
60 cm
63 cm
Mkiliitu
70 cm
57 cm
illllll
61 cm
B
16
14-
12-
10
63 cm
70 cm
JJiUilil
58 cm
62 cm
llll llllllllll
65 cm
73 cm
llllllllllllllll,
18-
16
14-
12-
10
8
6-
74 cm
Mil I,
2 4 6
74 cm
i-
16-
14-
12
10
8-
6-
4
2
80 cm
111 llll
82 cm
llll
2 4 6
2 4 6 8 10
2 4 6 8 10
OOCYTE DIAMETER (jjm x I02 )
Figure 3.— Representative frequency distributions of oocyte diameter from ovaries of Pacific hake 56-82 cm FL.
213
Table 1.— Regression equations for oocytes of several size classes,
and some combinations of same, found in prespawned ovaries of
Pacific hake from the Strait of Georgia, B.C.
Oocyte
Regression
Correlation
diameter
Oocyte
equation
coefficient
G*m)
description
(F = aFLb)
(r)
40-780
all oocytes
F
= 0.3081 FL37605
0.93
40-180
unyolked reserve
F
= 0.0692FL3 9766
0.88
200-380
small, yolked
F
= 0.0446FL37097
0.86
400-580
medium, yolked
F
= 0.2078FL34174
0.71
600-780
large, yolked
F
= 0.0008FL4 6370
0.65
400-780
medium plus
large yolked
F
= 0.1872FL35640
0.75
200-780
all yolked
F
= 0.5501 FL33896
0.81
females in the number of maturing oocytes as their
maturity stage advanced towards hydration. This
may be both a reflection of the range in stage of
maturity among individual females at a common
time of collection, and variation among females in
the proportion of yolked oocytes destined for hydra-
tion and release
Apparent fecundity taken as the number of yolked
oocytes >200 /urn was best expressed by the equa-
tion Fa = 0.5501FL3-3896. The averaged female hake
in the Strait of Georgia stock (43.3 cm FL) contain-
ed an estimated 193,868 yolked oocytes >200 /urn and
had a relative apparent fecundity of 382.3 eggs/g.
In comparison, an uncommonly large female (80 cm
FL) could contain more than 1.5 million yolked
oocytes for a specific fecundity of 477 oocytes/g
(Table 2).
Pacific hake in the Strait of Georgia grow rapidly
to age 4, showing almost linear growth in length
(McFarlane et al. 1983). Thereafter, growth de-
creases rapidly and is accompanied by considerable
individual variation in annual growth. The largest
female in the sample (82 cm FL) was age 18 whereas
another female age 15 was only 49 cm FL. Not
surprisingly, age was weakly related to apparent
fecundity and wide individual differences in ap-
Table 2.— Total and relative (oocytes/g body weight) fecundity
estimates at fork length for unyolked (40-180 ^m diameter) and
yolked (200-780 /^m diameter) oocytes found in prespawned
ovaries of Pacific hake from the Strait of Georgia, B.C.
Fork
length
Unyolked oocytes
Yolked oocytes
% yolked
of
(cm)
Total
Relative
Total
Relative
unyolked
40
162,502
406
148,178
370
91.1
45
259,580
455
220,887
388
85.3
50
394,666
507
315,679
403
79.5
55
576,544
551
436,089
417
75.7
60
814,896
598
585,684
430
71.9
65
1,120,308
645
768,233
443
68.7
70
1,504,260
693
987,611
455
65.7
75
1,979,132
739
1,247,812
466
63.1
80
2,558,196
786
1 ,552,943
477
60.7
parent fecundity are evident within age classes
(Fig. 4).
Frequency Distributions of
Oocyte Diameter in Postspawners
Gonads of 276 adult Pacific hake, trawl-caught on
3 July 1981, were staged superficially for maturity
after Foucher and Beamish 1977. All gonads were
in postreproductive state The ovaries of 18 of 111
females retained for microscopic analysis were dis-
tributed within the various maturity states with
these results: spent (1), recovering (7), and resting
(10). Yolked oocytes (200-500 /mi) were found in 7
ovaries: spent (1), recovering (4), and resting (2).
Number of oocytes ^200 /mi, expressed as a percent-
age of the oocytes <200 pm (40-180 /mi) was <3%
in 6 of these fish, and 11% in the seventh, compared
with 85-90% in prespawned ovaries collected in
March (Table 2).
These results support previous conclusions that
not all yolked oocytes larger than 200 /mi diameter
are released, as suggested by Foucher and Beamish
(1980) and MacGregor (1966). They also suggest that
resorbtion in postspawned females probably does not
exceed about 5% of the yolked oocytes destined for
release
The female Pacific hake in the Strait of Georgia
appears to use progressively less of the reserve fund
of unyolked oocytes present during gonadal matura-
tion in subsequent spawnings (Table 2), although
relative and apparent fecundity increases with in-
creased fork length. This can be illustrated by com-
paring females <55 cm FL (Figs. 1, 2) with larger
females (Fig. 3). The number of reserve fund oocytes
in the size fraction 40-180 /mi increases at a faster
rate, almost doubling the relative fecundity for
reserve fund oocytes in this size fraction by 80 cm
FL than does production of larger oocytes. The
reserve fund may have several origins, and cyto-
logical evidence was presented by Foucher and
Beamish (1980) that the fund may be supplemented
by cells of follicular origin in the postspawned ovary.
Such a mechanism to increase potential fecundity
would appear to be rather redundant if significant
resorbtion of yolked oocytes commonly occurs.
Stock Differences in Fecundity and
Estimates of Spawning Stock
Methodological differences or lack of disclosure,
and lack of substantiated assessment of stock-
specific resorption following spawning, render it im-
possible to draw very useful comparisons of fecun-
214
LU
lu
180-
170
160-
150-
140
130-
S 120-
E
=«,
O
o
CVJ
co
CD
O
LU
LL
o
CO
Q
Z
<
co
D
O
I
LL
o
co
Z
LU
1 10 -
100-
90
80-
70
60-
50
40
30-
20
10-
•'° 9 0/<
• 10 »9
• 10 »I3
• 14
• 12 •
• 8
'-» -I?9
• 13 • •
•/•o
4»* §5^6 6 O
•^
3s*„
o
o o
o+^v-
0
40 44 48 52
56 60 64 68
FORK LENGTH (cm)
72
76
80 84
Figure 4— Estimated number of yolked oocytes >200 ^m diameter in 97 hake ovaries from the Strait of
Georgia, B.C., plotted against fork length of female hake Numbers adjacent to individual plots indicate
estimated age of female; open circles - 1980 females, closed circles - 1981 females.
215
dity between coastal and inshore stocks of Pacific
hake at this time Ermakov et al. (1974) excluded
oocytes <100 pirn diameter, thus excluding a large
fraction of unyolked oocytes constituting the reserve
fund. Their estimates of total fecundity (compar-
able fork length) are one-half to one-third of those
reported here for hake in the Strait of Georgia
(>40 mm) and are also lower than the present
estimates for apparent fecundity (oocytes ^200 ^m
diameter).
MacGregor (1966, 1971) counted advanced, yolked
oocytes (>600 /urn) only, premised on his assumption
that only these cells were destined for release On
the basis of relative fecundity (eggs per gram), for
yolked oocytes >580 fim diameter of comparable size
to MacGregor's "large, yolked" or "advanced"
oocytes, the female Pacific hake in the Strait of
Georgia are considerably less fecund (54-164 eggs/g)
over the fork length range of 40-80 cm than are Baja
California hake which averaged 216 eggs/g (MacGre-
gor 1971). However, the lack of distributional bi-
modality in the Canadian ovaries renders such a com-
parison unrealistic, for a common size threshold for
resorption, even if appropriate, cannot be applied
conveniently to individual ovaries.
We can state with reasonable certainty that re-
sorption of yolked oocytes is a common occurrence
in both coastal and inshore stocks of Pacific hake,
as has been found in other forms of Merluccius
(Hickling 1930; Christiansen 1971). The influence of
ovarian resorption on annual fecundity of stock and
on the magnitude of released egg production from
individual females remains unknown. It follows that
the application of existing fecundity information to
problems of assessing magnitude of Pacific hake
spawning stock from released egg production, as
determined through ichthyoplankton surveys, should
reflect these reservations.
For the Pacific hake stock in the Strait of Georgia,
British Columbia, resorption may not involve more
than 5-10% of the apparent fecundity. Hence spawn-
ing biomass estimates based on released egg pro-
duction and the apparent fecundity could be
rendered conservative by the observed extent of
resorption in this stock.
Acknowledgments
Staff of the Groundfish Program at Nanaimo are
thanked for collecting biological materials and
related statistics at sea, and for aging the female
Pacific hake used in the study (Aging Unit). Par-
ticular appreciation is extended to Susan Johnston
for her able assistance in the laboratory and to R.
Foucher for helpful discussion and comments on the
original draft.
Literature Cited
Bailey, K. M., R. C. Francis, and P. R. Stevens.
1982. The life history and fishery of Pacific whiting, Merluc-
cius productus. NOAA, NMFS, Proc Rep. 82-03, NWAFC,
Seattle, 81 p.
Chilton, D. E., and R. J. Beamish.
1982. Age determination for fishes studied by the Groundfish
Program at the Pacific Biological Station. Can. Spec Publ.
Fish. Aquat. Sci. 60, 102 p.
Christiansen, H. E.
1971. La reproduccion de la merluza en el Mar Argentino
(Merlucciidea, Merluccius merluccius hubbsi). 1. Descripci6n
histologica del ceclo del ovario de merluza (Reproduction of
the hake in the Argentine Sea. 1. Histological description of
the spawning cycle of the hake). Bol. Inst. Biol. Mar., Mar
del Plata 20:1-41. (Engl, transl., Can. Fish. Mar. Serv.,
Transl. Ser. 4003.)
Christiansen, H. E., and M. B. Cousseau.
1971. La reproduccion de la merluza en el Mar Argentino
(Merlucciidea, Merluccius merluccius hubbsi). 2. La
reproduccion de la merluza y su relaci6n con otros aspectos
biologicos de la especie (Reproduction of the hake in the
Argentine Sea. 2. Hake reproduction and its relationship with
other biological aspects of the species). Bol. Inst. Biol. Mar,
Mar del Plata 20:41-73. (Engl, transl., Can. Fish. Mar. Serv.,
Transl. Ser. 4003.)
Ermakov, J. K., V. A. Snytko, L. S. Kodolov, 1. 1. Serobaba, L.
A. Borets, and N. S. Fadeev.
1974. Biological characteristics and conditions of the stocks
of Pacific hake, sea perches, sablefishes, and walleye pollock
in 1972. Engl, transl., Can. Fish. Mar. Serv. Transl. Ser.
3066, 37 p.
Foucher, R. P., and R. J. Beamish.
1977. A review of oocyte development in fishes with special
reference to Pacific hake (Merluccius productus). Can. Fish.
Mar. Serv. Tech. Rep. 755, 16 p.
1980. Production of nonviable oocytes by Pacific hake (Merluc-
cius productus). Can. J. Fish. Aquat. Sci. 37:41-48.
Hickling, C. F.
1930. The natural history of the hake Part III. Seasonal
changes in the condition of the hake. Fish. Invest. Minist.
Agric. Fish. Food (G.B.), Ser. II, XII(l):l-78.
McFarlane, G. A., W. Shaw, and R. J. Beamish.
1983. Observations on the biology of Pacific hake, walleye
pollock, and spiny dogfish in the Strait of Georgia, February
20-May 2, and July 3, 1981. Can. MS Rep. Fish. Aquat. Sci.
1722, 109 p.
MacGregor, J. S.
1966. Fecundity of the Pacific hake, Merluccius productus
(Ayres). Calif. Fish Game 52:111-116.
1971. Additional data on the spawning of the haka Fish.
Bull., U.S. 69:581-585.
Mason, J. C, R. J. Beamish, and G. A. McFarlane.
1983. Sexual maturity, fecundity, spawning, and early life
history of sablefish (Anoplopoma fimbria) off the Pacific
coast of Canada. Can. J. Fish. Aquat. Sci. 40:2126-2134.
Mason, J. C, A. C. Phillips, and O. D. Kennedy.
1984. Estimating the spawning stocks of Pacific hake (Merluc-
cius productus) and walleye pollock (Theragra chalcogram-
ma) in the Strait of Georgia, B.C. from their released egg pro-
duction. Can. Tech. Rep. Fish. Aquat. Sci. 1289, 51 p.
216
Pitt, T. K.
1964. Fecundity of the American plaice, Hippoglossoides
platessoides (Fabr.) from Grand Bank and Newfoundland
areas. J. Fish. Res. Board Can. 21:597-612.
Simpson, A. C.
1951. The fecundity of the plaice Fish. Invest. Ministr. Agric
Fish. Food (GB), Ser. II, 17(5):l-27.
Stepanenko, M. A.
1980. Reproductive conditions and the assessment of the
spawning part of the Pacific hake, California anchovy, horse-
mackerel, and some other fish species in the California Cur-
rent Zone in 1979. Pac. Inst. Fish. Oceangr. (TINRO),
Manuscr. Rep., 29 p.
Thomson, R. E.
1981. Oceanography of the British Columbia coast. Can.
Spec Publ. Fish. Aquat. Sci. 56, 219 p.
Utter, F M., and H. 0. Hodgins.
1971. Biochemical polymorphisms in the Pacific hake (Merluc-
cius productus). Rapp. P.-v. Reun. Cons. int. Explor. Mer
161:87-89.
WlBORG, K. F
1951. The whirling vessel: An apparatus for the fractioning
of plankton samples. Rep. Norw. Fish. Mar. Invest. 9(13):
1-16.
J. C. Mason
Department of Fisheries and Oceans
Fisheries Research Branch
Pacific Biological Station
Nanaimo, British Columbia V9R 5K6, Canada
STRANDED ANIMALS AS INDICATORS OF
PREY UTILIZATION BY HARBOR SEALS,
PHOCA VITULINA CONCOLOR, IN
SOUTHERN NEW ENGLAND
Since Federal protection began in 1972, the New
England population of harbor seals, Phoca vitulina
concolor, has more than doubled (Gilbert and Stein
19811; Payne and Schneider 1984), increasing at a
site in southeastern Massachusetts at an average
rate of 11.9% per year (Payne and Schneider 1984).
One of the primary management concerns regarding
the New England seal population is the increasing
potential for conflict between commercial fisheries
and harbor seals (Prescott et al. 19802).
Seals have been shown to be significant consumers
Gilbert, J. R., and J. L. Stein. 1981. Harbor seal populations
and marine mammal fisheries interactions. National Marine Fish-
eries Service, NOAA, Northeast Fisheries Center, Contract No.
NA-80-FA-C-00029, Woods Hole, MA 02345, 55 p.
2Prescott, J. H., S. D. Kraus, and J. R. Gilbert. 1980. East
Coast/Gulf Coast Cetacean and Pinniped Workshop. Marine Mam-
mal Commission (MMC), Final Report, Contract 79/02. (Available
National Technical Information Service, Springfield, VA 22151 as
PB80-160104, 142 p.)
of marine production (Brodie and Pasche 1982) and
have been implicated as competitors for commer-
cially valuable fish stocks, impacting fisheries
through direct predation, gear damage, and en-
tanglement (Boulva and McLaren 1979; Everitt and
Beach 1982; Brown and Mate 1983). Despite the
significant increase in harbor seal abundance, only
anecdotal information exists on the diet of harbor
seals along the eastern United States, lb assess the
impact of this common predator on fish and squid,
information is required on the food species exploited.
In the past, seals were killed to facilitate quanti-
tative analysis of their stomach contents (Imler and
Sarber 1947; Spalding 1964; Boulva and McLaren
1979; Pitcher 1980a), although this procedure is im-
practical in New England. Two alternatives to this
method are the analysis of the stomachs of strand-
ed animals, and the examination of seal feces col-
lected on accessible haul-out sites (Pitcher 1980b;
Treacy and Crawford 1981; Brown and Mate 1983).
The first alternative for determining the food
habits of the southern New England seal population
was provided by the more than 500 harbor seals that
have been found stranded south of Maine since 1977.
The stranded seals were collected by the New
England Aquarium (NEA), Boston, MA. The major-
ity (59%) of the seals were collected between January
and March (Table 1) along the perimeter of Cape Cod
Bay, MA, primarily on the eastern side. This corre-
sponds to the time when the peak number of seals
occur south of Maine (Schneider and Payne 1983).
Most of the stranded seals (65%) came from one
year, 1980 (Table 1), when over 445 seals died of
acute pneumonia associated with influenza virus
(Geraci et al. 1982).
Upon necropsy at the NEA, most of the stomachs
and intestinal tracts of the stranded seals were found
to be empty. Only 63 stomachs contained food mat-
ter, and the contents from those were frozen for later
Table 1.— Monthly distribution of stranded P. v. concolor contain-
ing prey items examined 1977-83.
Month
1977
1978
1979
1980
1981
1982
1983
Total
Jan.
1
15
1
17
Feb.
7
2
1
10
Mar.
10
10
Apr.
1
1
May
1
1
1
2
1
6
June
1
2
1
4
July
1
1
Aug.
2
1
1
4
Sept.
3
2
5
Oct.
1
1
Nov.
1
1
Dec.
2
1
3
Totals
1
1
3
41
3
9
5
63
FISHERY BULLETIN: VOL. 84, NO. 1, 1986.
217
examination. In the fall of 1983, we pilot-tested the
analysis of stomach contents from stranded seals
using those 63 stomach samples as an indicator of
prey utilization. The objectives of this study were 1)
to identify prey items selected by seals in southern
New England and 2) to determine whether stomach
contents from stranded animals can provide accurate
information on the utilization of most kinds of prey.
Methods
The stomachs were thawed and the contents wash-
ed with water through a series of nested sieves (1.80,
1.00, and 0.50 mm2). Identifiable materials were
rough-sorted into fish and fish components, inverte-
brates and invertebrate components. Intact speci-
mens and cephalopod beaks were preserved in a 70%
ethanol-30% glycerin solution. Persistent prey hard
parts (primarily otoliths) were removed and stored
dry in glass vials.
Otoliths from the stomach samples were identified
against a reference collection at the National Marine
Fisheries Service, Northeast Fisheries Center
(NMFS/NEFC), Woods Hole, MA. Cephalopod beaks
were identified against a reference key (Clarke 1962).
To estimate the size of fish taken by harbor seals,
otoliths removed from the stomach samples were
measured under a dissecting microscope using ver-
nier calipers. Regression equations relating otolith
length to fish length (Frost and Lowry 1980; Brown
and Mate 1983) were calculated using measurements
obtained from the reference collection of fishes col-
lected in the Gulf of Maine, located at the NMFS/
NEFC. Fork lengths were estimated for four prey
species.
Results
Fifty-three stomachs (84%) held identifiable food
items (Table 2). Cephalopod beaks were recovered
from 35 stomachs, representing at least 168 in-
dividuals and 2 species. Thirty-three stomachs con-
tained beaks from the short-finned squid, Illex il-
lecebrossus, with a range of 1-22 beaks per stomach.
Beaks of the long-finned squid, Loligo pealei, were
found in two stomachs, ranging from 4 to 5 beaks
per stomach, and accounted for only 5% of the squid
recovered. The two species were not found together
in any of the stomachs. Twenty-nine stomachs con-
tained squid remains and no other type of prey. Six
stomachs contained both squid and fish remains.
Seventeen stomachs contained some fish remains,
including intact specimens, copious semidigested
flesh, and 121 free otoliths. In total, seven species
and five families were represented. Fourteen
stomachs held otoliths from only one species of fish,
while seven stomachs contained otoliths from more
than one fish species.
Four species of Gadidae comprised the majority
of all fish species found in the stomachs of the
stranded seals. A total of 86 otoliths in six stomachs
were recovered. Haddock, Melanogrammus aegle-
finus, was the most frequently found gadid (45
otoliths in four stomachs) with a maximum of 24
otoliths recovered from a single stomach. Silver hake,
Merluccius bilinearis, remains were found only
slightly less frequently (34 otoliths from three
stomachs). Pollock, Pollachius virens, otoliths were
found in one stomach (five otoliths), and two red
hake, Urophycis chuss, otoliths of equal length were
recovered from one stomach, presumably from a
single fish.
Fifteen free otoliths and three intact specimens
of American sand lance, Ammodytes americanus,
were recovered from two stomachs, and three
stomachs contained otoliths from members of the
flatfish family Pleuronectidae
Two stomachs contained shells: the Atlantic
mussel, Mytilus edulis, and the common slipper shell,
Crepidula fornicata.
The estimated mean fork length for the four gadid
prey species ranged from 170 to 340 mm (Table 3).
Regressions were not available to estimate the
lengths of the sand lance found in the stomachs;
however, studies on sand lance in Cape Cod Bay
found a mean size of 93 mm SL (Richards 1982).
Table 2. — Analysis of stomach contents from stranded harbor
seals, P. v. concolor in Southern New England, 1977-83.
Stomach {N
= 63)
Frequency
Min. no.
Species
N
%
animals
Cephalopoda:
Illex illecebrossus
33
58.4
159
Loligo pealei
2
3.7
9
Mytilidae:
Mytilus edulis
2
3.7
12
Calyptraeidae:
Crepidula fornicata
2
3.7
10
Clupeidae:
Clupea harengus
1
1.8
1
Gadidae:
Melanogrammus aeglefinus
4
5.6
23
Pollachius virens
1
1.8
3
Urophycis chuss
1
1.8
1
Merlucciidae:
Merluccius bilinearis
3
5.6
17
Ammodytidae:
Ammodytes americanus
2
3.7
11
Pleuronectidae:
Pseudopleuronectes americanus
3
5.6
10
Unidentified pisces
11
20.8
218
Table 3. — Estimated sizes of four fish prey species of harbor seals in Southern New
England, based on regression equations relating otolith length (OL) to fish fork length (FL).
Species
Regression
equation
Estimated prey size
(FL, mm)
r2
Range
Mean
Melanogrammus aeglefinus
Merluccius bilinearis
Pollachius virens
Urophycis chuss
FL = 3.4(OL) - 9.32 0.97 45 110-310 230
FL = 22.4(OL) - 1.44 0.98 34 30-460 170
FL = 4.9(OL) - 22.58 0.95 5 160-310 280
FL = 25.0(OL) + 0.63 0.96 2 340
Discussion
Analyzing stomach contents from stranded ani-
mals to determine prey preference or selection does
yield a partial list of prey species exploited; however,
several apparent biases prohibit the realization of ac-
curate quantitative results. Therefore, the utility of
this method is questionable
The limited number of stomachs containing food
was likely due to the weakened condition of seals
prior to stranding and their inability to obtain food.
The stomachs that did contain food all came from
stranded animals, and therefore may not reflect on
what a healthy seal was feeding. The stranded seals
were generally animals with debilitating conditions
like lungworm and heartworm, and may not have
been able to feed in usual feeding areas, or secure
usual prey, and thus were probably less selective
about prey items.
For example, the shells found in the two stomachs
may represent prey items desirable only to a disease-
weakened seal. The size and number of these shells
suggest that they were not ingested incidentally.
Comparing the stomach contents to a "condition
index", such as length vs. girth or blubber thick-
ness, might indicate whether the stranded animals
are less selective about prey species than healthy
ones.
The abundance of squid beaks found in the
stomachs suggests that squid are an important part
of the diet of harbor seals along coastal New
England; however, our own finding of squid beaks
in 56% of 63 stomachs may be inflated. Boulva and
McLaren (1979) found squid remains in 20.6% of 279
stomachs examined from eastern Canada, and Pit-
cher (1980b) similarly found cephalopod beaks in
21.1% of 351 harbar seals collected in the Gulf of
Alaska. Seals have been shown to retain, then re-
gurgitate, cephalopod beaks rather than pass them
through their digestive tract (Miller 19783; Pitcher
1980b). Retention of squid beaks will tend to over-
represent the utilization of squid as a prey species
(Pitcher 1980a). The retention of beaks during a
period of fasting prior to death may also account for
the large percentage (41%) of stomachs containing
squid beaks and no other type of prey remains.
Large fish may be underrepresented if the heads
(i.e, otoliths) are not eaten (Boulva and McLaren
1979; Brown and Mate 1983). Pitcher (1980b) sug-
gested that seals often fragment large fish while
eating them, usually discarding the head.
Finally, the relationship between the time when
prey was eaten and when the stomach was collected
may determine what types of prey remains will be
recovered (Frost and Lowry 1980; Pitcher 1980a;
Brown and Mate 1983). For example, the low num-
ber of sand lance otoliths found in the stomachs may
not accurately represent the importance of sand
lance as a prey species of harbor seals in southern
New England because otoliths of the size of the ones
recovered are very small and delicate and may not
remain for long in the seal stomachs once freed from
the skull (Smith and Gaskin 1974).
Thus, using only frequency of occurrence as a
measure of prey preference or selection may be mis-
leading by overemphasizing the importance of some
species. For example, based on number, cephalopods
were the major prey item; however fewer otoliths
representing fish of greater weight may show that
fish indeed are more improtant. The full importance
of fish or squid in the diet of seals can be accurately
described only if quantitative assessments such as
weight or volume of food items in the stomachs can
be determined (Rae 1973; Frost and Lowry 1980).
In summary, given a large sample of animals the
analysis of stomach contents from stranded seals
does provide information on the types of prey
selected. However, the analysis of stomach contents
from stranded seals greatly overemphasizes cephal-
opod remains while likely underrepresenting most
3Miller, L. K. 1978. Energetics of the northern fur seal in rela-
tion to climate and food resources of the Bering Sea. Marine Mam-
mal Commission, Final Report, Contract MM5AC025. (Available
National Technical Information Service, Springfield, VA 22151 as
PB-275 296, 32 p.)
219
species of fish prey due to an extended period of
fasting prior to stranding. We consider comparative
frequencies of selected prey to be too biased to be
useful in any ranking of prey items. Therefore, this
technique of analyzing prey utilization should be con-
sidered only if the examination of feces or the
stomach contents from seals that were healthy when
collected are not possible options.
Acknowledgments
We wish to thank all those from the New England
Aquarium, Marine Mammal Rescue and Release Pro-
gram, who helped collect the stranded animals. Paul
J. Boyle and Kevin D. Powers commented on previous
drafts of this manuscript. Research was conducted
with the New England Aquarium's Edgerton Re-
search Laboratory. This study was funded by Na-
tional Marine Fisheries Service/Northeast Fisheries
Center, Contract No. NA-82-FA-00007.
Literature Cited
Boulva, J., and I. A. McLaren.
1979. Biology of the harbor seal, Phoca vitulina, in Eastern
Canada. Fish. Res. Board Can., Bull. 200:1-24.
Brodie, P. F., and A. J. Pasche.
1982. Density-dependent condition and energetics of marine
mammal populations in multispecies fisheries management.
In M. C. Mercer (editor), Multispecies approaches to fisheries
management advice, p. 35-38. Can. Spec Publ. Fish. Aquat.
Sci. 59.
Brown, R. F, and B. R. Mate.
1983. Abundance, movements, and feeding habits of harbor
seals, Phoca vitulina, at Netarts and Tillamook Bays, Ore-
gon. Fish. Bull., U.S. 81:291-301.
Clarke, M. R.
1962. The identification of cephalopod "beaks" and the rela-
tionship between beak size and total body weight. Bull. Br.
Mus. (Nat. Hist), Zool. 8:421-480.
Everitt, R. D., and R. J. Beach.
1982. Marine mammal-fisheries interactions in Oregon and
Washington: An overview. In K. Sabol (editor), Transactions
of the North American Wildlife and Natural Research Con-
ference, p. 265-277. Wildl. Manage. Inst, Wash., DC.
Frost, K. J., and L. F. Lowry.
1980. Feeding of ribbon seals (Phoca fasciata) in the Bering
Sea in Spring. Can. J. Zool. 58:1601-1607.
Geraci, J. R., D. J. St. Aubin, I. K. Barker, R. G. Webster, V.
S. Hinshaw, W. J. Bean, H. L. Ruhnke, J. H. Prescott, G.
Early, A. S. Baker, S. Madoff, and R. T. Schooley.
1982. Mass mortality of harbor seals: pneumonia associated
with influenza A virus. Science 215:1129-1131.
Imler, R. H., and H. R. Sarber.
1947. Harbor seals and sea lions in Alaska. U.S. Fish. Wildl.
Serv., Spec. Sci. Rep. 28, 23 p.
Payne, P. M., and D. C. Schneider.
1 984. Yearly changes in abundance of harbor seals at a winter
haul-out site in Massachusetts. Fish. Bull., U.S. 82:440-442.
Pitcher, K. W.
1980a. Food of the harbor seal, Phoca vitulina richardsi, in
the Gulf of Alaska. Fish. Bull., U.S. 78:544-549.
1980b. Stomach contents and feces as indicators of harbor
seal, Phoca vitulina, foods in the Gulf of Alaska. Fish. Bull.,
U.S. 78:797-798.
Rae, B. B.
1973. Further observations on the food of seals. J. Zool.
(Lond.) 169:287-297.
Richards, S. W.
1982. Aspects of the biology of Ammodytes americanus from
the St. Lawrence River to Chesapeake Bay, 1972-75, in-
cluding a comparison of the Long Island Sound postlarvae
with Ammodytes dubius. J. Northwest Atl. Fish. Sci. 3:93-
104.
Schneider, D. C, and P. M. Payne.
1983. Factors affecting haul-out of harbor seals at a site in
southeastern Massachusetts. J. Mammal. 64:518-520.
Smith, G. J. D, and D. E. Gaskin.
1974. The diet of harbor porpoises (Phocoena phocoena (L.))
in coastal waters of eastern Canada, with special reference
to the Bay of Fundy Can. J. Zool. 52:777-782.
Spalding, D J.
1964. Comparative feeding habits of the fur seal, sea lion, and
harbour seal on the British Columbia coast. Fish. Res. Board
Can., Bull. 146, 52 p.
Treacy, S. D, and T W. Crawford.
1981. Retrieval of otoliths and statoliths from gastrointestinal
contents and scats of marine mammals. J. Wildl. Manage.
45:990-993.
Lawrence A. Selzer
Manomet Bird Observatory, Manomet, MA 0231*5
Greg Early
Patricia M. Fiorelli
New England Aquarium, Boston, MA 02110
P. Michael Payne
Manomet Bird Observatory, Manomet, MA 0231*5
Present address:
Boston University Marine Program, Woods Hole, MA 0231*5.
Robert Prescott
Massachusetts Audubon Society,
South Wellfleet, MA 02663
SCAVENGER FEEDING BY SUBADULT
STRIPED BASS, MORONE SAXATILIS,
BELOW A LOW-HEAD HYDROELECTRIC DAM1
A spawning run of striped bass, Morone saxatilis,
has not been found in the Connecticut River, but
subadults from other rivers were reported in the
lower 100 km of the river in the 1930's (Merriman
Contribution No. 84 of the Massachusetts Cooperative Fishery
Research Unit, which is supported by the U.S. Fish and Wildlife
Service, Massachusetts Division of Fisheries and Wildlife, Massa-
chusetts Division of Marine Fisheries, and the University of
Massachusetts.
220
FISHERY BULLETIN: VOL. 84, NO. 1, 1986.
1941). Subadults enter the river in the spring and
summer, often in enough abundance to support a
sport fishery in Connecticut (Moss 1960). No striped
bass were passed upstream in the two Holyoke Dam
fish lifts located at river km 140 from the initial
operation in 1955 until 1979, when 103 were lifted.
Each year from 1980 to 1984, 110-510 striped bass
have used the fish lifts (O'Leary 1985). In 1982,
83.5% of the fish were age II; 16.5% were age III;
and none were sexually mature (Warner 1983).
Because the striped bass did not migrate into the
river to spawn, they probably entered to feed. The
food of striped bass has been extensively studied,
but there is no published report about the food of
young fish that gather below a hydroelectric dam.
We studied the food of the striped bass that were
lifted at Holyoke Dam in 1982.
Methods
The stomachs of fish were removed and frozen, and
the contents were examined in the laboratory with
a dissecting microscope Stomach contents were
classified as small forage fish, body parts of large
fish (i.e., fish larger than the striped bass could eat
whole), insects, plant material, and empty. Body
parts were the scales, bones, flesh, and ovaries of
adult alosids (i.e, American shad, Alosa sapidissima,
and blueback herring, A. aestivalis), and pieces of
adult sea lamprey, Petromyzon marinus. The body
parts originated from the following sources: fish that
were injured or killed while attempting to pass the
dam or to use the fish lifts, American shad that were
discarded below the dam by sport fishermen, or
turbine-induced injuries or mortalities of fish that
passed through the hydropower turbine at the dam
(Bell and Kynard 1985).
When possible, small forage fish were identified
to species and measured for total length. Insects
were identified to order. We compared the frequency
of occurrence of the four foods eaten by striped bass
that were lifted early (25 May-14 June), when average
daily passage of adult alosids in the lifts was about
28,000, with the foods eaten by striped bass that
were lifted late (after 21 June), when the average
daily lift of alosids was about 3,000.
Results and Discussion
We examined 78 stomachs of striped bass— 65
(83%) contained food. Sixty-nine percent of the
stomachs with food contained the body parts of large
fish (Fig. la). Of the stomachs with the body parts
of large fish, 93% contained the scales of adult
alosids, with many containing over 20 scales; 16%
contained the body parts of adult sea lampreys.
Small forage fish were second in the frequency of
occurrence at 61%, and insects were third at 21%
(Fig. la). Elvers of the American eel, Anguilla
rostrata, (96 mm mean total length, range: 70-125
mm, N = 24) dominated the small forage fish
category, occurring in 58% of the stomachs that con-
tained forage fish. Elvers, migrating upstream from
the ocean, may be delayed and concentrated by
Holyoke Dam; perhaps striped bass follow the elvers
upriver— both species occur in the fish lifts at the
same time Cyprinids were identified in six of the
stomachs with forage fish. All had a 2,4-4,2 tooth
formula and were probably spottail shiners, Notropis
hudsonius, a commonly observed minnow. Insects in
stomachs were mayfly nymphs, order Ephemerop-
tera, but only one or two mayflys were found in any
stomach.
There was a significant difference in the frequency
of the four food groups in fish collected early and
late (x2 = 12.6, P < 0.01). Fish parts dominated the
stomach contents of early-lifted fish, whereas in late-
lifted fish 54% contained parts of large fish, but 77%
contained small forage fish (Fig. lb). Fifteen per-
cent of the stomachs of early-lifted fish were empty,
UJ
o
a: 100
UJ
a.
uu
(a )
80
60
40
20
n
m
FISH FORAGE
PARTS
FISH
INSECTS PLANTS
Figure 1— Percent occurrence of the four major foods in the
stomachs of striped bass passed by the Holyoke fish lifts a) in all
of 1982 and b) in fish sampled early (25 May-14 June, N = 39) and
late (after 21 June, N = 26) 1982.
221
and 19% of the stomachs of late-lifted fish were
empty.
Food of the striped bass at Holyoke Dam was
dominated by the body parts of adult American shad,
blueback herring, and sea lamprey when many in-
dividuals of these species were being lifted, and
dominated by forage fish and insects, when the
alosids and sea lampreys were scarce (Fig. lb). The
reduced incidence of feeding on the body parts of
large fish by striped bass lifted after 21 June was
probably the result of a dramatic reduction in the
availability of this food that occurred when the run
of anadromous alosids diminished.
Hollis (1952) found alosid scales in the stomachs
of adult striped bass captured below Conowingo Dam
on the Susquehanna River in Maryland, but he dis-
missed these as accidental. In our study, alosid body
parts occurred in stomachs too frequently to be ac-
cidental. Many authors consider the food that is
selected by striped bass to be directly related to the
availability (Hollis 1952; Thomas 1967; Schaefer
1970). During the run of anadromous fish at Holyoke
Dam, the most abundant food that is available for
striped bass is likely the body parts of dead or in-
jured American shad, blueback herring, and sea lam-
prey although we were not able to confirm this by
sampling below the dam. About 900,000 adult alosids
were passed upstream in the fish lifts in 1982, and
injuries and mortalities were commonly observed at
the dam and fish lifts. Subadult striped bass may
typically concentrate below hydroelectric dams and
feed on the parts of fish (anadromous or freshwater
species) that die or sustain injury while attempting
to move upstream or downstream of the dam.
Acknowledgments
This research was supported by Federal Aid Pro-
ject AFS-4-R-21 and Dingell- Johnson Project
5-29328 to the Massachusetts Division of Fisheries
and Wildlife and the Massachusetts Cooperative
Fishery Research Unit.
Literature Cited
Bell, C. E., and B. Kynard.
1985. Mortality of adult American shad passing through a
17-megawatt Kaplan turbine at a low-head hydroelectric dam.
North Am. J. Fish. Manage 5:33-38.
Hollis, E. H.
1952. Variations in the feeding habits of the striped bass, Roc-
cus saxatilis (Walbaum), in Chesapeake Bay. Bull. Bingham
Oceanogr. Collect, Yale Univ. 14:111-131.
Merriman, D.
1941. Studies on the striped bass (Roccus saxatilis) of the
Atlantic coast. U.S. Fish Wildl. Serv., Fish. Bull. 50:1-77.
Moss, D. D.
1960. A history of the Connecticut River and its fisheries.
Conn. Board Fish. Game, Hartford, 12 p.
O'Leary, J. O.
1985. Connecticut River anadromous fish investigations.
Mass. Coop. Fish. Res. Unit, Univ. Mass., D-J Proj. F-45-R-2
Rep., 19 p.
Schaefer, R. H.
1970. Feeding habits of striped bass from the surf waters of
Long Island. N.Y. Fish Game J. 17:1-17.
Thomas, J. L.
1967. The diet of juvenile and adult striped bass, Roccus sax-
atilis, in the Sacramento-San Joaquin River system. Calif.
Fish Game 53:49-62.
Warner, J. R
1983. Demography, food habits, and movements of striped
bass, Morone saxatilis Walbaum, in the Connecticut River,
Massachusetts. M.S. Thesis, Univ. Massachusetts, Amherst,
94 p.
John Warner
Boyd Kynard
Massachusetts Cooperative Fishery Research Unit
204 Holdsworth Hall
University of Massachusetts
Amherst, MA 01003
GENETIC CONFIRMATION OF SPECIFIC
DISTINCTION OF ARROWTOOTH FLOUNDER,
ATHERESTHES STOMIAS, AND
KAMCHATKA FLOUNDER., A. EVERMANNI
The uncertain taxonomic status of two morphologi-
cal types of Atheresthes (family Pleuronectidae) has
led to some problems in fisheries surveys and stock
assessments. Although data collection would be
simplified if these types were conspecific morphs,
a single classification would mask differences of
distribution and abundance if each type actually
represented a distinct species. Each type is described
as a separate species: arrowtooth flounder, A.
stomias, and Kamchatka flounder, A. evermanni,
based on morphological differences in gill raker
count, dorsal and anal fin rays, caudal vertebrae
number, eye-dorsal fin distance, and relative position
of the upper eye (Norman 1934; Wilimovsky et al.
1967). However, the differences are subtle, and both
types have generally been considered A. stomias in
fisheries surveys (e.g., Smith and Bakkala 1982).
Atheresthes stomias occurs in the eastern Bering
Sea and eastern North Pacific Ocean from about St.
Matthew Island, southward through the eastern Ber-
ing Sea and Gulf of Alaska, and along the North
American coast to central California (Hart 1973).
Atheresthes evermanni is distributed in the western
222
FISHERY BULLETIN: VOL. 84, NO. 1, 1986.
Bering Sea and western North Pacific Ocean from
the Anadyr Gulf, south along the Kamchatka Pen-
insula, through the Sea of Okhotsk, and to northern
Japan (Andriyashev 1939; Wilimovsky et al. 1967).
The geographic ranges of the two types overlap in
some areas of the Aleutian Islands and eastern Ber-
ing Sea.
Biochemical data have recently provided valuable
insights towards clarifying genetic relationships
among fishes. Findings have ranged from identify-
ing previously unknown species (eg., Shaklee et al.
1982) to grouping taxa previously considered distinct
(eg, Wishard et al. 1984). Biochemical data were
therefore used to clarify the taxonomic status of A.
stomias and A. evermanni through an electro-
phoretic examination of known individuals of both
types. The level of genetic difference observed in this
study is compared with that found between two
other groups of marine fishes of the Bering Sea and
the North Pacific Ocean.
Materials and Methods
Collections were made in the Bering Sea near
Unalaska Island by National Marine Fisheries Ser-
vice research vessels Oregon (lat. 53°45'N, long.
166°56'W, August 1980) and Miller Freeman (lat.
54°44'N, long. 166°29'W, February 1981). The 12
Kamchatka flounder (4 taken in 1980 and 8 in 1981)
included males and females with fork lengths
ranging from 24 to 43 cm. The 13 arrowtooth
flounder, taken only in 1981, also included both sexes
and ranged in fork lengths from 33 to 43 cm. Mor-
phological types were distinguished by the gill raker
counts and position of the upper eye In specimens
identified as Kamchatka flounder, the upper eye did
not reach the edge of the head and the mean total
gill raker count was 12.4. The upper eye of specimens
identified as arrowtooth flounder reached the edge
of the head, breaking the dorsal profile and the mean
total gill raker count was 15.3. Fish were frozen in-
tact at -20°C following collection and remained
frozen up to 30 mo until tissues were removed for
electrophoretic analysis.
Sample preparation and electrophoresis followed
methods given by Utter et al. (1974). Buffer systems
included 1) a discontinuous tris-citric acid (gel pH
8.2), lithium hydroxide-boric acid (tray pH 8.0) buf-
fer, described by Ridgway et al. (1970); 2) a tris-boric
acid - 0.004 M EDTA (pH 8.5) buffer, described by
Markert and Faulhaber (1965); and 3) an aminopro-
pylmorpholine-citric acid - 0.01 M EDTA (pH 6.5) buf-
fer, described by Clayton and Tretiak (1972).
Procedures of visualizing enzyme activities follow-
ing electrophoresis were those outlined by May et
al. (1979). We followed the criteria of Allendorf and
Utter (1979) for the inference of Mendelian inheri-
tance in the absence of breeding data. Genetic data
were collected from 22 protein systems (Table 1). A
system of nomenclature suggested by Allendorf and
Utter (1979) was used where the most common
allelic form of a locus was designated as 100, and
other allelic forms were assigned values based on
their mobility relative to the common form. Alleles
migrating cathodally were given negative values.
Phenotypic frequencies of the overall sample (all
specimens of both presumed species pooled together)
at each polymorphic locus were tested for expected
binomial (i.e, Hardy-Weinberg) distributions using a
G statistic for goodness of fit (Sokal and Rohlf 1969;
Goodenough 1978). Multiple allelic cases were col-
lapsed to two allelic classes to allow for small sam-
ple sizes. A contingency table analysis of allelic fre-
quencies testing the null hypothesis of no difference
between the two groups also used the G statistic,
Table 1.— Protein systems used in this study including tissues and
appropriate buffer systems for detection of suitable activity.
Enzyme
commission
Protein system
number
Tissues1
Buffed
Acid phosphatase (ACP)
3.1.3.2
M,L,H
1,2,3
Adenosine deaminase (ADA)
3.5.4.4
M,E
1
Alcohol dehydrogenase
(ADH)
1.1.1.1
L
3
Aldolase (ALD)
4.1.2.13
M
1,3
Aspartate aminotransferase
(AAT)
2.6.1.1
M
1,2
Creatine kinase (CK)
2.7.3.2
M
1,3
Esterase (EST)
3.1.1.1
L,H,E
3
General protein (GP)
M,E
2,3
Glucosephosphate isomerase
(GPI)
5.3.1.9
M,E
1
Glyceraldehydephosphate
dehydrogenase (GAP)
1.2.1.12
E,M
1,3
Glycerol-3-phosphate
dehydrogenase (G3P)
1.1.1.8
M
3
Glycylleucine peptidase (GL)
3.4.11
E,M
1,2
Isocitrate dehydrogenase
(IDH)
1.1.1.42
M,H,E
3
Lactate dehydrogenase (LDH)
1.1.1.27
M,E
3
Leucylglycylglycine peptidase
(LGG)
3.4.11
M
1
Malate dehydrogenase (MDH)
1.1.1.37
H.L.E.M
3
Malate dehydrogenase (ME)
(decarboxylating - NADP+)
1.1.1.40
M
2
Mannosephosphate
isomerase (MPI)
5.3.1.8
M
2
Phosphoglucomutase (PGM)
2.7.5.1
M
1
6-phosphogluconate
dehydrogenase (PGD)
1.1.1.44
M,E
3
Phosphoglycerate kinase
(PGK)
2.7.2.3
M
3
Superoxide dismutase (SOD)
1.15.1.1
M,H
1,3
1M = muscle, L = liver, H = heart, E = eye.
21 = discontinuous tris citrate, lithium borate; 2
EDTA; 3 = continuous amine citrate, EDTA.
continuous tris, borate,
223
with Yates correction for small sample sizes (Sokal
and Rohlf 1969). Nei's (1978) measure of genetic
distance for small sample sizes was calculated be-
tween the two groups.
Results and Discussions
Data were collected from 22 enzyme systems en-
coding the following 32 presumed loci (polymorphic
loci having one or more variant alleles are indicated
by *): AAT*, ACP-1, ACP-2*, ADA*, ADH*, ALD,
G3P-1*, G3P-2, CK-1, CK-2, EST, GAP-1*, GAP-2,
GL-1, GL-2, IDH*, LDH-1*, LDH-2, LDH-3, LGG*,
MDH-1, MDH-2, MDH-3, ME, PGD*, PGM-1,
PGM-2, GPI-1, GPI-2*, PGK*, MPI, SOD.
Allelic distributions for the 13 polymorphic loci
indicate considerable similarity for most of the
systems but some distinct differences as well, based
on the contingency analysis (Table 2). The nonsig-
nificant differences observed at nine of the loci are
not highly informative given the limited number of
individuals that were sampled.
However, the differences that were statistically sig-
nificant provide considerable information. The most
striking difference is at the ADH locus, where no
alleles were shared between the 12 arrowtooth and
the 10 Kamchatka flounders. These data alone con-
firm the genetic distinctness of the two types. The
allelic distribution between the two forms is almost
as distinct at the GAP-1 locus; a lesser, but signifi-
cant difference also exists at the ACP-2 locus. Gel
banding patterns observed for these three loci are
shown in Figure 1.
Not surprisingly, the genotypic frequencies at the
ADH and GAP-1 loci also deviated significantly (P
< 0.001) from the ratios of a binomial expansion of
allelic frequencies (Hardy-Weinberg equilibrium ex-
pected in a single, randomly mating population). This
difference resulted from excesses of homozygous and
deficits of heterozygous classes, a situation expected
in population mixtures (i.e., the Wahlund effect, see
Futuyma 1979).
The distinct genotypic distribution of the two
forms at the ADH and GAP-1 loci, coupled with their
sympatric occurrence and subtle but consistent mor-
phological identities, support their present tax-
onomic status as distinct congeneric species. How-
ever, the value of genetic distance observed, 0.052,
is rather low for distinct species suggesting recent
speciation (Avise 1976).
Recent genetic studies of two other pleuronectid
species sampled from the same geographic region
indicate only conspecific variation. The Alaska Pen-
insula separates two population groups of yellowfin
sole, Limanda aspera, at a mean genetic distance
of 0.005 (Grant et al. 1983). No significant differences
of allelic frequencies were detected in Pacific halibut,
Hippoglossus stenolepis, sampled in the Bering Sea
and the North Pacific Ocean (Grant et al. 1984).
These various outcomes among confamilial group-
ings undoubtedly reflect the past and present actions
of numerous variables; two major factors are differ-
ing capabilities for gene flow based on distinct life
history patterns, and differing times and degrees of
isolation imposed by glaciation events within the past
2 million years (discussed by Grant and Utter 1984).
Finally, the possibility of hybridization and intro-
gression between the two species of Atheresthes
should be examined through more extensive sam-
pling of these two forms over a broader geographic
range The distinct distribution of ADH alleles ex-
cluded a hybrid origin of any individuals in this study.
Table 2. — Observed number and (in parentheses) within group fre-
quency of alleles of 13 polymorphic loci in samples of arrowtooth
and Kamchatka flounder.
Allele
Observed alleles
(frequencies)
P1
Subunit
structure2
Locus
Arrowtooth
Kamchatka
AAT
92
100
106
2(0.100)
10(0.500)
8(0.400)
no data
d
ACP-2
100
109
20(0.769)
6(0.231)
22(1 .000)
0(0.000)
<0.05
m
ADA-1
100
108
24(0.923)
2(0.077)
19(0.792)
5(0.208)
ns
m
ADH
-100
-75
-13
24(1.000)
0(0.000)
0(0.000)
0(0.000)
1(0.050)
19(0.950)
<0.001
d
G3P-1
100
150
24(1.000)
0(0.000)
19(0.950)
1(0.050)
ns
d
GAP-1
13
70
100
0(0.000)
0(0.000)
26(1.000)
9(0.375)
12(0.500)
3(0.125)
<0.001
t
GPI-2
100
107
25(0.962)
1(0.038)
24(1.000)
0(0.000)
ns
d
IDH
70
100
0(0.000)
26(1.000)
3(0.125)
21(0.875)
ns
d
LDH-3
100
117
26(1 .000)
0(0.000)
22(0.917)
2(0.083)
ns
t
LGG
86
100
1(0.038)
25(0.962)
0(0.000)
22(1.000)
ns
d
PGD
75
100
4(0.154)
22(0.846)
0(0.000)
22(1.000)
ns
d
PGM-1
84
100
105
113
0(0.000)
23(0.885)
3(0.115)
0(0.000)
1(0.042)
22(0.916)
0(0.000)
1(0.042)
ns
m
PGK
100
133
26(1.000)
0(0.000)
19(0.950)
1(0.050)
ns
m
'Contingency tests of allelic frequencies using the G-statistic with Yates cor-
rection for small sample sizes, assuming all samples drawn from the same
population; ns = not significant.
2Protein subunit structure based on observed banding patterns of variants;
m = monomer, d = dimer, t = tetramer.
224
Literature Cited
'en
ACP-2
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CO
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00
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c
■-.
0)
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ea
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<u
he
J3
o
i-
ca
+j
en
rolro
I.
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C3
o J2
r^loo
ool<-
r~|r^
oo|oo
olo
o
o
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1939. Ocherk zoogeografii i proiskhozhdeniya fauny ryb Ber-
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waters). [In Russ.] Izd. Leningr. Gos. Univ., Leningr., 187
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1976. Genetic differentiation during speciation. In F. J. Ayala
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Clayton, J. W., and D. N. Tretiak.
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Carol L. Ranck
Northwest and Alaska Fisheries Center
National Marine Fisheries Service, NOAA
2725 Montlake Boulevard East
Seattle, WA 98112
Present address: Rufus Field Station
National Marine Fisheries Service, NOAA
P.O. Box 67, Rufus, OR 97050
Fred M. Utter
George B. Milner
Gary B. Smith
Northwest and Alaska Fisheries Center
National Marine Fisheries Service, NOAA
2725 Montlake Boulevard East
Seattle, WA 98112
226
ERRATA
Fishery Bulletin: Vol. 83, No. 1
Perez Farfante, Isabel. "The rock shrimp genus Sicyonia (Crustacea: Decapoda: Penaeoidea) in the
eastern Pacific," p. 1-79.
Page 4, figure legend was omitted and should be added as follows:
Figure 1— Lateral view of generalized Sicyonia showing terms used in description.
Fishery Bulletin: Vol. 83, No. 3
Lester, R. J. G., A. Barnes, and G. Habib. "Parasites of skipjack tuna, Katsuwonus pelamis: fishery
implications," p. 343-356.
Page 347; Table 2, No. 6, Syncoelium filiferum:
J should read 0.2 and K should read 6.9.
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Fishery Bulletin
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Notes
WEBER, EARL G, and STEPHEN R. GOLDBERG. The sex ratio and gonad indices
of swordfish, Xiphias gladius, caught off the coast of southern California in
iy / o loo
UCHIYAMA, JAMES H.( RAYMOND K. BURCH, and SYD A. KRAUL, JR. Growth
of dolphins, Coryphaena hippurus and C. equiselis, in Hawaiian waters as determined
by daily increments on otoliths 186
FROST, KATHRYN J., and LLOYD F. LOWRY. Sizes of walleye pollock, Theragra
chalcogramma, consumed by marine mammals in the Bering Sea 192
VAN ENGEL, W. A., R. E. HARRIS, JR., and D. E. ZWERNER. Occurrence of some
parasites and a commensal in the American lobster, Homarus americanus, from the
Mid-Atlantic Bight 197
COLLETTE, BRUCE B. Resilience of the fish assemblage in New England tide-
pools 200
JOHNSON, PHYLLIS T. Parasites of benthid amphipods: ciliates 204
MASON, J. C. Fecundity of the Pacific hake, Merluccius productus, spawning in
Canadian waters 209
SELZER, LAWRENCE A., GREG EARLY, PATRICIA M. FIORELLI, P. MICHAEL
PAYNE, and ROBERT PRESCOTT Stranded animals as indicators of prey utiliza-
tion by harbor seals, Phoca vitulina concolor, in southern New England 217
WARNER, JOHN, and BOYD KYNARD. Scavenger feeding by subadult striped bass,
Morone saxatilis, below a low-head hydroelectric dam 220
RANCK, CAROL L., FRED M. UTTER, GEORGE B. MILNER, and GARY B. SMITH.
Genetic confirmation of specific distinction of arrowtooth flounder, Atheresthes stomias,
and Kamchatka flounder, A. evermanni 222
* GPO 593-096
jr
**r.s o* ^
Fishery Bulletin
A
Vol. 84, No. 2
April 1986
HUMES, ARTHUR G. Copepodids and adults of Leptinogaster major (Williams, 1907),
a poecilostomatoid copepod living in My a armaria L. and other marine bivalve
mollusks 227
MYRICK, A. G, JR., A. A. HOHN, J. BARLOW, and P. A. SLOAN. Reproductive biology
of female spotted dolphins, Stenella attenuata, from the eastern tropical Pacific . . 247
SYKES, STEPHEN D., and LOUIS W. BOTSFORD. Chinook salmon, Oncorhynchus
tschawytscha, spawning escapement based on multiple mark-recapture of car-
casses 261
PAYNE, P. MICHAEL, JOHN R. NICOLAS, LORETTA O'BRIEN, and KEVIN D.
POWERS. The distribution of the humpback whale, Megaptera novaeangliae, on
Georges Bank and in the Gulf of Maine in relation to densities of the sand eel, Am-
modytes americanus 271
BAYER, RANGE D. Seabirds near an Oregon estuarine salmon hatchery in 1982 and
during the 1983 El Nino 279
WILKINS, MARK E. Development and evaluation of methodologies for assessing and
monitoring the abundance of widow rockfish, Sebastes entowelas 287
NELSON, WALTER R., and DEAN W AHRENHOLZ. Population and fishery charac-
teristics of gulf menhaden, Brevoortia patronus 311
HAWKES, CLAYTON, R., THEODORE R. MEYERS, and THOMAS C.
SHIRLEY. Length-weight relationships of blue, Paralithodes platypus, and golden,
Lithodes aequispina, king crabs parasitized by the rhizocephalan, Briarosaccus callosus
Boschma 327
DOHL, THOMAS P, MICHAEL L. BONNELL, and R. GLENN FORD. Distribution
and abundance of common dolphin, Delphinus delphis, in the Southern California Bight:
a quantitative assessment based upon aerial transect data 333
vKENNEY, ROBERT D, and HOWARD E. WINN. Cetacean high-use habitats of the
northeast United States continental shelf 345
CUMMINGS, WILLIAM C, PAUL 0. THOMPSON, and SAMUEL J. HA. Sounds from
Bryde, Balaenoptera edeni, and finback, B. physalus, whales in the Gulf of Califor-
nia 359
PEREZ, MICHAEL A., and ELIZABETH E. MOONEY. Increased food and energy
consumption of lactating northern fur seals, Callorhinus ursinus 371
BIGG, MICHAEL A. Arrival of northern fur seals, Callorhinus ursinus, on St. Paul
Island, Alaska 383
{Continued on back cover)
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Fishery Bulletin
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ment and Budget through 1 April 1986.
Fishery Bulletin
CONTENTS
Vol. 84, No. 2 April 1986
HUME S, ARTHUR G. Copepodids and adults of Leptinogaster major (Williams, 1907),
a poecilostomatoid copepod living in Mya arenaria L. and other marine bivalve
mollusks 227
MYRICK, A. G, JR., A. A. HOHN, J. BARLOW, and P. A. SLOAN. Reproductive biology
of female spotted dolphins, Stenella attenuata, from the eastern tropical Pacific . . 247
SYKES, STEPHEN D., and LOUIS W BOTSFORD. Chinook salmon, Oncorhynchus
tschawytscha, spawning escapement based on multiple mark-recapture of car-
casses 261
PAYNE, P. MICHAEL, JOHN R. NICOLAS, LORETTA O'BRIEN, and KEVIN D.
POWERS. The distribution of the humpback whale, Megaptera novaeangliae, on
Georges Bank and in the Gulf of Maine in relation to densities of the sand eel, Am-
modytes americanus 271
BAYER, RANGE D. Seabirds near an Oregon estuarine salmon hatchery in 1982 and
during the 1983 El Nino 279
WILKINS, MARK E. Development and evaluation of methodologies for assessing and
monitoring the abundance of widow rockfish, Sebastes entomelas 287
NELSON, WALTER R., and DEAN W. AHRENHOLZ. Population and fishery charac-
teristics of gulf menhaden, Brevoortia patronus 311
HAWKES, CLAYTON, R., THEODORE R. MEYERS, and THOMAS C.
SHIRLEY. Length-weight relationships of blue, Paralithodes platypus, and golden,
Lithodes aequispina, king crabs parasitized by the rhizocephalan, Briarosaccus callosus
Boschma 327
DOHL, THOMAS P., MICHAEL L. BONNELL, and R. GLENN FORD. Distribution
and abundance of common dolphin, Delphinus delphis, in the Southern California Bight:
a quantitative assessment based upon aerial transect data 333
KENNEY, ROBERT D, and HOWARD E. WINN. Cetacean high-use habitats of the
northeast United States continental shelf 345
CUMMINGS, WILLIAM C, PAUL 0. THOMPSON, and SAMUEL J. HA. Sounds from
Bryde, Balaenoptera edeni, and finback, B. physalus, whales in the Gulf of Califor-
nia 359
PEREZ, MICHAEL A., and ELIZABETH E. MOONEY Increased food and energy
consumption of lactating northern fur seals, Callorhinus ursinus 371
BIGG, MICHAEL A. Arrival of northern fur seals, Callorhinus ursinus, on St. Paul
Island, Alaska 383
(Continued on next page)
Seattle, Washington
1986
Marine Biological Laboratory
LIBRARY
JUL 31 1986
Woods 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
LO, NANCY C. H. Modeling life-stage-specific instantaneous mortality rates, an
application to northern anchovy, Engraulis mordax, eggs and larvae 395
SEN, A. R. Methodological problems in sampling commercial rockfish landings . . . 409
POLOVINA, JEFFREY J. A variable catchability version of the Leslie model with
application to an intensive fishing experiment on a multispecies stock 423
MATSUURA, YASUNOBU, and NELSON TAKUMI YONEDA. Early development
of the lophid anglerfish, Lophius gastrophysus 429
SQUIRES, DALE. Ex-vessel price linkages in the New England fishing industry . . 437
LEBER, KENNETH M., and HOLLY S. GREENING. Community studies in seagrass
meadows: A comparison of two methods for sampling macroinvertebrates and
fishes 443
Notes
OXENFORD, HAZEL A., and WAYNE HUNTE. A preliminary investigation of the
stock structure of the dolphin, Coryphaena hippurus, in the western central
Atlantic 451
FORWARD, RICHARD B., JR., BLANCA ROJAS de MENDIOLA, and RICHARD T.
BARBER. Effects of temperature on swimming speed of the dinoflagellate Gym-
nodinium splendens 460
GRAHAM, JEFFREY B., RICHARD H. ROSENBLATT, and DARCY L. GIBSON.
Morphology and possible swimming mode of a yellowfin tuna, Thunnus albacares, lack-
ing one pectoral fin 463
RATTY, F J., Y. C. SONG, and R. M. LAURS. Chromosomal analysis of albacore, Thun-
nus alalunga, and yellowfin, Thunnus albacares, and skipjack, Katsuwonus pelamis,
tuna 469
STIER, KATHLEEN, and BOYD KYNARD. Abundance, size, and sex ratio of adult
sea-run sea lamprey, Petromyzon marinus, in the Connecticut River 476
MASON, J. C, and A. C. PHILLIPS. An improved otter surface sampler 480
GROVE R, JILL J., and BORI L. OLLA. Morphological evidence for starvation and
prey size selection of sea-caught larval sablefish, Anoplopoma fimbria 484
Notices 490
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 ap-
proves, recommends or endorses any proprietary product or proprietary material
mentioned herein, or which has as its purpose an intent to cause directly or indirect-
ly the advertised product to be used or purchased because of this NMFS publication.
COPEPODIDS AND ADULTS OF
LEPTINOGASTER MAJOR (WILLIAMS, 1907), A POECILOSTOMATOID
COPEPOD LIVING IN MYA ARENAR1A L. AND
OTHER MARINE BIVALVE MOLLUSKS
Arthur G. Humes1
ABSTRACT
The five copepodid stages and adults of Leptinogaster major (Williams, 1907), a poecilostomatoid copepod
(family Clausidiidae) living in the mantle cavity of Mya arenaria L. and other marine bivalve mollusks
along the coast of eastern North America from Prince Edward Island, Canada, to Louisiana, are described.
Copepodid I is Saphirella-\ike in body form. In the adult female the maxilliped is present though much
reduced. Sexual differentiation first occurs in Copepodid IV, where the male and female maxillipeds are
differently formed.
The poecilostomatoid copepod Leptinogaster (=
Myocheres) major (Williams, 1907) has been reported
from the mantle cavity of various marine bivalve
mollusks along the eastern shore of North America,
from Prince Edward Island, Canada (J. C. Medcof
in correspondence with M. S. Wilson) to Louisiana
(Causey 1953). This copepod has undergone several
name changes, but it seems generally agreed now
that it properly belongs in the genus Leptinogaster
(see Bocquet and Stock 1958, and Table 1). The
seasonal population changes and host relationships
of this species have been described by Humes and
Cressey (1960), who listed as hosts Mya arenaria
L., Tagelus gibbus (Spengler), Venus mercenaria L.,
and Ensis directus (Conrad). Other hosts include
Mactra solidissima Dillwyn (reported by Williams
1907), Dosinia gibbus Reeve (reported by Pearse
Table 1.— Taxonomic history of Leptinogaster major (Williams, 1907).
Lichomolgus mayor Williams, 1907, p. 77, pi. Ill, 8 figs.; Sharpe 1910,
p. 408, placed in Lichomolgidae.
Myicola major, C. B. Wilson, 1932, p. 347, fig. 208, genus wrongly
assigned; Monod and Dollfus 1934, p. 316, placed in Clausiidae;
Deevey 1948, p. 22, 1960, p. 34; Sewell 1949, p. 156, placed in
Lichomolgidae; Causey 1953, p. 12.
Myicola spinosa Pearse, 1947, p. 5, figs. 26-31, placed in Myicolidae.
Myocheres major, M. S. Wilson, 1950, p. 299; M. S. Wilson and lllg
1955, p. 136, 138; Allen 1956, p. 62, placed tentatively in Licho-
molgidae; Bocquet and Stock 1957a, p. 213, 221, placed in
Clausidiidae; Humes and Cressey 1958, p. 932, 934, placed in
Clausidiidae; Bacescu and Por 1959, p. 20, placed in Clausi-
diidae; Humes and Cressey 1960, p. 307-325.
Leptinogaster major, Bocquet and Stock, 1958, p. 86-88, placed in
Clausidiidae; Gooding 1963, p. 132-136, pi. 17, figs. a-n.
aBoston University Marine Program, Marine Biological Labor-
atory, Woods Hole, MA 02543.
1947), and Pholas eostata L. (reported by Causey
1953). For a list of bivalve hosts and localities see
Table 2.
The copepodid development of Leptinogaster has
not been fully described. Bocquet and Stock (1958)
mentioned finding copepodids of Leptinogaster
histrio (Pelseneer 1929) and figured the maxillipeds
of an unknown stage (their fig. 3d, e); they also
reported a Copepodid V of Leptinogaster sp. and il-
Table 2.— Localities and hosts of Leptinogaster major.
Locality
Host(s)
Source
Ellerslie, Prince
Edward Island,
Can.
Bideford River,
Prince Edward
Island, Can.
Cotuit, MA
Marthas Vineyard,
MA
Wickford and
Matunuck, Rl
Delaware Bay
Beaufort, NC
Grand Isle, LA
Mya arenaria L.
Mya arenaria L.
Mya arenaria L.
Tagelus gibbus
(Spengler)
Venus mercenaria L.
Ensis directus
(Conrad)
in plankton
Mya arenaria L.
Venus mercenaria L.
Mactra solidissima
Dillwyn
in plankton
Tagelus gibbus
(Spengler)
Dosinia discus
Reeve
Venus mercanaria L.
Pholas eostata L.
J. C. Medcof in
correspondence
(23 May 1950)
with M. S. Wilson
J. C. Medcof in
correspondence
(31 July 1948) with
M. S. Wilson
Humes and
Cressey (1960)
Deevey (1948)
Williams (1907)
Deevey (1960)
Pearse (1947)
Causey (1953)
Manuscript accepted May 1985.
FISHERY BULLETIN: VOL. 85, NO. 2, 1986.
227
FISHERY BULLETIN: VOL. 84, NO. 2
lustrated its maxilliped (their fig. 6b, c). Gooding
(1963) described features of Copepodid I of Leptino-
gaster major.
Before her death Mildred S. Wilson had studied
specimens of Leptinogaster (= Myocheres) major
that had been sent to her from Rhode Island and
Prince Edward Island, and had prepared the first
draft of a redescription. She recognized the need for
a thorough redescription of this species whose
original description by Williams (1907) is very incom-
plete Although she wrote (1950) that a detailed
description of adults and developmental forms was
then in preparation, this study apparently was never
completed. In a letter to J. C. Medcof dated 24
August 1948 she stated that she had found two early
stages of Myocheres. Presumably descriptions of
these copepodids would have been part of her pro-
jected study if she had lived.
During the study by Humes and Cressey (1960) a
large number of Leptinogaster major (1,535) were
collected from Mya arenaria over a period of almost
2 yr at Cotuit, MA. The copepodids and adults
described below came from collections made during
the summer of 1957. All five copepodid stages,
distinguished on the basis of the number of body
segments, as well as adults, were obtained. This
paper deals with the detailed description of the ex-
ternal morphology of these immature stages and
adults.
Although the copepodids described here were not
obtained by rearing, it seems certain that the cope-
podids found in such large numbers are those of Lep-
tinogaster major. No other species of copepods oc-
curred in the Mya arenaria examined.
MATERIALS AND METHODS
The copepodids and adults described here were
selected from a pool of 305 copepodids and 195
adults found in 125 Mya arenaria during May-
September at Cotuit, MA. The successive Cope-
podids I-V and the adults were cleared in lactic acid
and sorted by size and external morphology into
their respective groups.
All measurements and dissections were made on
specimens cleared in lactic acid, following the
method of Humes and Gooding (1964). The body
length does not include the setae on the caudal rami.
The measurements of certain parts, such as the
length of the first antenna, maxilliped, and various
setae and claws, and the dimensions of leg 5, the
caudal ramus, and the urosomal segments, are based
on dissected specimens from which the drawings
were made, and may be considered representative
of nearly average body size Such measurements are
intended more to show relative changes in size dur-
ing successive instars rather than to represent ab-
solute size The drawings were made with the aid
of a camera lucida. The abbreviations used are as
follows: Al = first antenna, A2 = second antenna,
L = labrum, MD = mandible, MXX = first maxilla,
MX2 = second maxilla, P3 = leg 3, P4 = leg 4, and
P5 = leg 5.
DESCRIPTIONS
Copepodid I
Figures la-n, 2a-c
Size— Length 0.57 mm (0.45-0.60 mm) and
greatest width 0.17 mm (0.16-0.18 mm) based on 38
specimens.
Body form (Fig. la, b, c).— Saphirella-\\ke, with
cephalosome bluntly pointed anteriorly. Five body
segments including and posterior to segment bear-
ing leg 1. Anal segment with 4 groups of spines, 2
ventral groups and 2 ventrolateral groups (Fig.
Id).
Caudal ramus (Fig. le).— Relatively short, 36 x 18
/urn, ratio 2:1, with 6 setae. Outer lateral seta 18 ^m,
dorsal seta 20 ^m, 4 terminal setae from outer to
inner 23, 17, 39, and 176 pm, the last with minute
lateral spinules.
Rostrum (Fig. lf).—Broad ridge, prominent in
lateral view (Fig. lg).
First antenna (Fig. lh).— Five-segmented, 83 pm
long. Armature: 2, 2, 3 + 1 aesthete 2 + 1 aesthete
and 5 + 1 aesthete All setae smooth.
Second antenna (Fig. li).— Indistinctly 4-segment-
ed, last segment obscure First segment with 1 distal
seta. Second segment with 1 seta and group of small
spines. Third segment with outer row of spines and
2 slender inner setules, with outer stout curved seta
having expanded serrate distal half and 1 short in-
ner blunt seta. Fourth segment small and indistinctly
set off from third segment, with 1 blunt short seta,
1 long stout smooth seta, 1 slender smooth seta, and
1 long stout seta with prominent lateral setules.
Labrum (Fig. lj).— Broad, with ventral surface
bearing 2 medially interrupted rows of spines and
with posteroventral margin having row of small
228
HUMES: COPEPODIDS AND ADULTS OF LEPTINOGASTER MAJOR
Figure 1 .— Copepodid I of Leptinogaster major, a, dorsal (scale A); b, ventral (A); c, lateral (A); d, anal segment, ventral (B); e, caudal
ramus, dorsal (C); f, rostral area, ventral (D); g, rostral area, lateral (B); h, first antenna, dorsal (D); i, second antenna, dorsal (C);
j, labrum, in situ, ventral (C); k, mandible, ventral (C); 1, first maxilla, ventral (C); m, second maxilla, ventral (C); n, maxilliped, posterior
(C).
229
FISHERY BULLETIN: VOL. 84, NO. 2
spines, these spines becoming much larger at both
corners.
Mandible (Fig. Ik).— Simple form, small, about 42
(im long, with expanded base but slender distal por-
tion bearing 2 minute setae midway and having
minutely pectinate tip.
Paragnath — Minute smooth lobe.
First maxilla (Fig. 11).— Small lobe bearing 6 setae
Second maxilla (Fig. lm).— Two-segmented, large
first segment with 2 setae, small second segment
with 3 setae
Maxilliped (Fig. In).— Elongate, slender, 4-seg-
mented. First segment with 2 setae Elongate second
segment with 2 setae and 2 small setules. Small third
segment with 1 long seta having few prominent
lateral setules. Fourth segment bearing 3 setae near
midregion and extended beyond as setiform process
with few minute barbs near tip.
Leg 1 (Fig. 2a).— Both rami 1-segmented. Formula
for armature: coxa 0-0; basis 1-0; exopod 111,1,4; endo-
pod 1,5,1. Exopod with 3 outer spines having prom-
inent lateral spinules and terminal outer spine and
adjacent seta with outer denticulations.
Leg 2 (Fig. 2b).— Both rami 1-segmented. Arma-
ture: coxa 0-0; basis 1-0; exopod 111,1,3; endopod
111,2,1. Exopod spines with lateral spinules or den-
ticulations as in leg 1; endopod spines finely barbed.
Leg 3 (Fig. 2c).— Consisting of 2 setae 70 and 57
^m, with 2 very small spines near their insertions.
Legs 4, 5, and 6— Absent.
Copepodid II
Figures 2d-m, 3a-e
Size-Length 0.68 mm (0.59-0.72 mm) and
greatest width 0.19 mm (0.18-0.20 mm), based on 31
specimens.
Body form (Fig. 2d).— No longer Saphirella-Wke.
Suggesting form of later instars. Six body segments
including and posterior to segment bearing leg 1.
Segment bearing leg 4 ventrally with 2 transverse
rows of spines (Fig. 2e). Anal segment ventrally with
distal spines in addition to 4 groups of proximal
spines. Ventrolateral areas of cephalosome at level
of mouthparts with strip of small spinules (Fig. 3a).
Caudal ramus.— Similar to Copepodid I but few
small ventral spines distally
Rostrum (Fig. 2f).— Suggesting rounded form seen
in later instars.
First antenna (Fig. 2g).— Five-segmented, 107 /urn
long. Armature: 2, 3, 3 + 1 aesthete 2 + 1 aesthete,
and 6 + 1 aesthete
Second antenna (Fig. 2h).— Four-segmented. Third
segment with 2 strong recurved outer clawlike
spines. Small fourth segment with 4 smooth setae
2 middle setae curved.
Labrum (Fig. 2i).— Posteroventral margin sharply
pointed. No surficial or marginal ornamentation.
Mandible (Fig. 2j).— Elongate 43 ^m, distally with
3 elements, 2 helmet-shaped and 1 stoutly spiniform,
all with minute marginal barbs.
Paragnath.— As an adult (see Fig. 7f).
First maxilla (Fig. 2k).— Small lobe bearing 5 setae
Second maxilla (Fig. 21).— Two-segmented, its form
suggesting later instars. First segment expanded
with outer patch of small spines. Second segment
clawlike 30 ^m long, with 1 inner seta.
Maxilliped (Fig. 2m).— Delicately sclerotized and
weakly 4-segmented, length 40 ^m. Relative posi-
tions of maxillipeds and head appendages as in Fig-
ure 3a.
Leg 1 (Fig. 3b).— Both rami 2-segmented. Arma-
ture: coxa 0-0; basis 1-1; exopod 1-0; 111,5; endopod
0-1; 1,5.
Leg 2 (Fig. 3c).— Both rami 2-segmented. Arma-
ture: coxa 0-0; basis 1-0; exopod 1-0; 111,4; endopod
0-1; 111,3.
Leg 3 (Fig. 3d).— Both rami 1-segmented. Arma-
ture: coxa 0-0; basis 1-0; exopod 111,4; endopod 111,3.
Leg 4 (Fig. 3e).— Consisting of 2 setae 52 and 39
fim.
Legs 5 and 6.— Absent.
230
HUMES: COPEPODIDS AND ADULTS OF LEPTINOGASTER MAJOR
Figure 2— Copepodid I of Leptinogaster major, a-c: a, leg 1 and intercoxal plate, anterior (scale B); b, leg 2 and intercoxal plate, anterior
(B); c, leg 3, dorsal (B). Copepodid II of Leptinogaster major, d-m: d, dorsal (E); e, body posterior to leg 4, ventral (F); f, rostral
area, ventral (B); g, first antenna, dorsal (D); h, second antenna, anteromesial (C); i, labrum, ventral (D); j, mandible, ventral (G); k,
first maxilla, anterior (C); 1, second maxilla, posteroventral (C); m, maxilliped (C).
231
laSHEKY BULiLdSTlIN: VUL. 84, JNU. Z
Copepodid HI
Figures 3f-k, 4a-d
Size-Length 0.85 mm (0.72-0.95 mm) and
greatest width 0.24 mm (0.21-0.26 mm), based on 37
specimens.
Body form (Fig. 3f).— Spinules on ventral surface
of segment of leg 5 (Fig. 3g) continuous across seg-
ment. Seven body segments including and posterior
to segment bearing leg 1. (One specimen, 0.62 x 0.24
mm, with segments behind leg 4 telescoped as in
Figure 3h.)
First antenna (Fig. 3i).— Five-segmented, 145 ^m
long. Armature: 3, 10, 3 + 1 aesthete, 2 + 1 aesthete,
and 7 + 1 aesthete
Second antenna (Fig. 3j).— Similar to Copepodid
II but outermost seta on fourth segment longer and
recurved.
Maxilliped.— As in Copepodid II.
Leg 1 (Fig. 3k).— Both rami 2-segmented. Arma-
ture: coxa 0-0, basis 1-1; exopod 1-0; III, 5; endopod
0-1; 1,6.
Leg 2 (Fig. 4a).— Both rami 2-segmented. Arma-
ture: coxa 0-0; basis 1-0; exopod 1-0; 111,6; endopod
0-1; 111,4.
Leg 3 (Fig. 4b).— Both rami 2-segmented. Arma-
ture: coxa 0-0, basis 1-0; exopod 0-1; 11,5; endopod
0-1; 111,3.
Leg 4 (Fig. 4c).— Both rami 1-segmented. Arma-
ture: coxa 0-0; basis 1-0; exopod 11,4; endopod
111,3. (Distal outer seta on exopod somewhat spini-
form.)
Leg 5 (Fig. 4d).— Represented by 2 setae, 42 and
29 urn.
Leg 6.— Absent.
Copepodid IV, female
Figures 4e-k, 5a-c
Size— Length 1.19 mm (0.93-1.33 mm) and greatest
width 0.32 mm (0.28-0.35 mm), based on 42 speci-
mens.
Body form (Fig. 4e).— Eight body segments in-
cluding and posterior to segment bearing leg 1.
Spinules on ventral surface of segment bearing leg
5 and on anal segment (Fig. 4f) as in Copepodid
III.
First antenna (Fig. 4g).— Five-segmented, 179 ^m
long, but slight notch on posterior edge of second
segment suggesting division of segment. Armature:
4, 15, 4 + 1 aesthete, 2 + 1 aesthete, and 7 + 1
aesthete
Maxilliped (Fig. 4h).— Two-segmented, weakly
sclerotized, distal segment lobelike Relative position
of maxillipeds as in Figure 4i.
Leg 1— Both rami 2-segmented. Armature (as in
Copepodid III): coxa 0-0; basis 1-0; exopod 1-0; 111,5;
endopod 0-1; 1,6.
Leg 2 (Fig. 4j).— Both rami 2-segmented. Arma-
ture: coxa 0-0; basis 1-0; exopod 1-0; 111,6; endopod
0-1; 11,6. Distalmost outer seta on endopod somewhat
spiniform.
Leg 3 (Fig. 4k).— Both rami 2-segmented. Arma-
ture: coxa 0-0; basis 1-0; exopod 1-0; 111,6; endopod
0-1; 11,5. Distalmost outer seta on endopod somewhat
spiniform.
Leg 4 (Fig. 5a).— Both rami 2-segmented. Arma-
ture: coxa 0-0; basis 1-0; exopod 1-0; 111,5; endopod
0-1; 111,3.
Leg 5 (Fig. 5b).— Two-segmented, but first seg-
ment, armed with 1 seta, not clearly set off from
body; second segment oval, 60 x 30 ^m, bearing 3
spines and 1 seta, with few small spinules near in-
sertion of proximalmost and distalmost spines.
Leg 6 (Fig. 5c).— Represented by 1 seta 32 /im long,
with minute spinules near insertion.
Copepodid IV, male
Figure 5d-g
Size— Length 1.07 mm (0.90-1.19 mm) and greatest
width 0.28 mm (0.25-0.31 mm), based on 38 speci-
mens.
Body form— As in female, with same number of
body segments and similar arrangement of ventral
spinules (Fig. 5d).
232
HUMES: COPEPODIDS AND ADULTS OF LEPTINOGASTER MAJOR
Figure 3— Copepodid II of Leptinogaster major, a-e: a, cephalosome, ventral (scale F); b, leg 1 and intercoxal plate, anterior (B); c,
leg 2 and intercoxal plate, anterior (B); d, leg 3 and intercoxal plate, anterior (B); e, leg 4, ventral (B). Copepodid III of Leptinogaster
major, f-k: f, dorsal (E); g, body posterior to leg 4, ventral (A); h, posterior part of body showing telescoped segments, dorsal (A);
i, first antenna, ventral (B); j, second antenna, anteromesial (D); k, leg 1 and intercoxal plate, anterior (B).
233
FISHERY BULLETIN: VOL. 84, NO. 2
Figure 4— Copepodid III of Leptinogaster major, a-d: a, leg 2 and intercoxal plate, anterior (scale B); b, leg 3 and intercoxal plate,
anterior (B); c, leg 4 and intercoxal plate, anterior (B); d, leg 5, ventral (B). Copepodid IV of Leptinogaster major, female, e-k: e,
dorsal (H); f, urosome, ventral (E); g, first antenna, ventral (B); h, maxilliped, ventral (C); i, ventral region from second maxillae to
first pair of legs, showing maxillipeds (F); j, leg 2 and intercoxal plate, anterior (F); k, leg 3 and intercoxal plate, anterior (F).
234
HUMES: COPEPODIDS AND ADULTS OF LEPTINOGASTER MAJOR
Figure 5— Copepodid IV of Leptinogaster major, female a-c: a, leg 4 and intercoxal plate, anterior (scale F); b, leg 5, lateral (D); c,
leg 6, ventral (D); male, d-g: d, urosome, ventral (A); e, maxilliped, ventral (C); f, ventral region from second maxillae to first pair
of legs, showing maxillipeds (F); g, leg 5, dorsal (D). Copepodid V of Leptinogaster major, female, h-m: h, dorsal (H); i, urosome,
ventral (E); j, first antenna, posteroventral (B); k, maxilliped, ventral (C); 1, leg 4 and intercoxal plate, anterior (A); m, leg 5, dorsal (F).
235
Maxilliped (Fig. 5e).— Three-segmented, 50 ^m
long, with small pointed third segment weakly set
off from second segment and bearing 2 small se-
tae Relative position of maxillipeds as in Figure
5f.
Leg 5 (Fig. 5g).— Two-segmented. First segment
set off from body. Second segment 55 x 29 ^m. Ar-
mature similar to female.
Leg 6 (Fig. 5d).— Represented by single seta.
Copepodid V, female
Figures 5h-m, 6a-c
Size— Length 1.62 mm (1.42-1.87 mm) and greatest
width 0.41 mm (0.37-0.44 mm), based on 13 speci-
mens.
FISHERY BULLETIN: VOL. 84, NO. 2
Leg 6 (Fig. 5i).— Represented by 1 seta with minute
spinule near its insertion.
Copepodid V, male
Figure 6a-c
Size— Length 1.41 mm (1.22-1.57 mm) and greatest
width 0.34 mm (0.31-0.39 mm), based on 30 speci-
mens.
Body form.— As in female, with same number of
body segments. Similar arrangement of ventral spin-
nules on urosomal segments (Fig. 6a).
Maxilliped (Fig. 6b).— Four-segmented. First seg-
ment with 1 inner seta. Long second segment and
short third segment unarmed. Pointed fourth seg-
ment with 2 setae
Body form (Fig. 5h).— Nine body segments in-
cluding and posterior to segment bearing leg 1. Seg-
ment of leg 5 and more posterior segments as in
Figure 5i.
Caudal ramus (Fig. 5i).— Noticeably longer than in
preceding instars.
First antenna (Fig. 5j).— Incompletely 6-segment-
ed. Armature: 5, 15 + 9, 4 + 1 aesthete, 2 + 1
aesthete, and 7 + 1 aesthete
Maxilliped (Fig. 5k).— Reduced to slightly raised
lobe with 2 small setae
Leg 1.— Both rami 3-segmented. Armature (as in
adult): coxa 0-0; basis 1-1; exopod 1-0; 1-1; 111,5; endo-
pod 0-1, 0-1; 1,5.
Legs 2 and 3.— Both rami 3-segmented. Armature
(as in adult): coxa 0-0; basis 1-0; exopod 1-0; 1-1; 111,6;
endopod 0-1; 0-2; 111,3.
Leg 4 (Fig. 51).— Both rami 3-segmented. Arma-
ture: coxa 0-0, basis 1-0; exopod 1-0; 1-1; 111,5; endo-
pod 0-1; 0-1; 111,2. Distalmost spine on exopod more
slender than other exopod spines; outer of 2 terminal
spines on endopod only about one-half length of
inner terminal spine
Leg 5 (Fig. 5m).— Second segment 99 x 49 j^m.
Few outer spinules on first segment. Two groups of
spinules on inner side of second segment. Principal
armature as in Copepodid IV.
236
Legs 1-4.— Similar to those of female Endopod of
leg 2 (Fig. 6c) not showing sexual dimorphism.
Leg 5.— As in female; second segment 75 x 31 /^m.
Leg 6.— Represented by single seta with few very
small spinules near its insertion.
Adult Female
Figures 6d-m, 7a-l, 8a-e, 9a-j
Size-Length 2.18 mm (1.92-2.45 mm) and
greatest width 0.52 mm (0.47-0.56 mm), based on 10
specimens. Dorsoventral thickness at level of leg 1,
0.25 mm.
Body form (Fig. 6d, e).— Elongate and flattened
dorsoventrally. Nine body segments including and
posterior to segment bearing leg 1. Urosome 5-seg-
mented (Fig. 6f). Segment bearing leg 5 220 x 319
^m in dorsal view, smooth on dorsal surface, but ven-
tral surface with transverse groups of spines (Fig.
6g); dorsally this segment with posterodorsal hump
(Fig. 6e, h). Genital segment 270 x 264 ^m, wider
in anterior half than in posterior half. Three post-
genital segments from anterior to posterior 143 x
165, 143 x 160, and 200 x 143 /im. Genital areas
situated dorsolateral^, each area (Fig. 6i) bearing
2 very small setae about 16 fim long. Ventral sur-
faces of genital segment and first and second post-
genital segments smooth. Anal segment ventrally
with few small spines at postero-outer corners, with
row of 5 spines on each side distally, and with 2
HUMES: COPEPODIDS AND ADULTS OF LEPTINOGASTER MAJOR
Figure 6— Copepodid V of Leptinogaster major, male, a-c: a, urosome, ventral (scale E); b, maxilliped, ventral (D); c, endopod of leg
2, anterior (F). Adult female of Leptinogaster major, d-m: d, dorsal (I), e, lateral (I); f, urosome, dorsal (H); g, segment bearing
fifth pair of legs, ventral (A); h, segment bearing leg 5, lateral (E); i, genital area, dorsal (B); j, patch of spinules and sclerotized area
on side of cephalosome, ventral (E); k, caudal ramus, dorsal (F); 1, anal segment and caudal ramus, ventral (F); m, egg sac, ventral (E).
237
FISHERY BULLETIN: VOL. 84, NO. 2
Figure 7 — Adult female of Leptinogaster major: a, rostrum, ventral (scale F); b, first antenna, posteroventral (F); c, second antenna,
posteromesial (B); d, labrum, ventral (B); e, mandible, anteroventral (C); f, paragnath, ventral (D); g, first maxilla, anterior (D); h,
second maxilla, posterior (B); i, maxilliped, ventral (D); j, ventral region from second maxillae to first pair of legs, showing maxillipeds
(E); k, leg 1 and intercoxal plate, anterior (F); 1, inner spine on basis of leg 1, anterior (G).
238
HUMES: COPEPODIDS AND ADULTS OF LEPT1NOGASTER MAJOR
prominent groups of spines anteriorly. Cephalosome
ventrally with elongate oblique strip of small spines
between edge of body and region of mouthparts, and
with small elongate oval sclerotized area lateral to
level of maxillipeds (Fig. 6j).
Caudal ramus (Fig. 6k, 1).— Elongate, 221 ^m long,
greatest width 44 ^m, least width 35 pcra, ratio about
5.5:1. Outer lateral seta 50 ym. Dorsal seta 26 ^m.
Outermost terminal seta 52 ym. Innermost terminal
seta 26 \xm. Outer of 2 median terminal setae 130
\m\ and almost spinelike. Inner of 2 median terminal
seta 440 ^m, with extremely small lateral spinules.
Other setae smooth. Outer margin of ramus prox-
imal to outer lateral seta with 2 groups of spinules.
Distal end of ramus ventrally with patch of small
spines.
Egg sac (Fig. 6m).— Elongate, various sacs 693 x
209 ion, 781 x 242 ym, 860 x 220 ym (as in figure),
and 1,023 x 231 ym, average dimensions 839 x 226
ym; containing many small eggs with diameter 47-57
ym.
Rostrum (Fig. 7a).— Broad with weakly sclerotized
rounded posteroventral margin.
First antenna (Fig. 7b).— Six-segmented, 320 ^m
long. Lengths of segments (measured along their
posterior nonsetiferous margins): 29 (49 ym along
anterior margin), 88, 55, 26, 36, and 52 ^m, respec-
tively. Armature: 5, 15, 9, 4 + 1 aesthete, 2 + 1
aesthete, and 7 + 1 aesthete All setae smooth.
Second antenna (Fig. 7c).— Four-segmented. First
segment with distal seta. Second segment with distal
seta and crescentic row of small spines. Third seg-
ment with outer marginal row of spines and 2 large
recurved clawlike spines, 34 and 70 ym. Small fourth
segment 13 x 21 ^m, bearing 3 long recurved almost
clawlike setae and 1 smaller inner seta.
Labrum (Fig. 7d).— Posteroventral edge sharply
pointed medially. No surface ornamentation.
Mandible (Fig. 7e).— Elongate with distal end bear-
ing 2 helmet-shaped elements and 1 stout pectinate
spine.
Paragnath (Fig. 7f).— Small lobe with few distal
spinules.
First maxilla (Fig. 7g).— Small lobe bearing 5 se-
tae
Second maxilla (Fig. 7h).— Two-segmented. Large
first segment with patch of outer spinules (Fig. 7j).
Second segment clawlike and bearing 1 seta.
Maxilliped (Fig. 7i).— Reduced to 2 small setae
located as in Figure 7j.
Legs 1-4 (Figs. 7k, 8a, b, c).— Intercoxal plates with
2 groups of spines on distal (ventral) margin. Exo-
pods and endopods 3-segmented. Armature as
follows (Roman numerals indicating spines, Arabic
numerals representing setae):
Pj coxa 0-0 basis 1-1
coxa 0-0 basis 1-0
P3 coxa
0-0 basis 1-0
exp
1-0;
M;
111,5
enp
0-1;
0-1;
1,5
exp
1-0;
I-l;
111,6
enp
0-1;
0-2;
111,3
exp
1-0;
i-l;
111,6
enp
0-1;
0-2;
111,3
exp
1-0;
i-l;
111,5
enp
0-1;
0-1;
111,2
coxa 0-0 basis 1-0
Leg 1 (Fig. 7k).— Coxa with 2 groups of outer
spines. Basis with row of small spines between bases
of rami and another row near large inner spine This
inner spine delicately barbed (Fig. 71) and 33 ym
long; smaller spines near its base 7.5 ^m. First seg-
ment of endopod with outer margin having hairlike
setules along proximal half but small spines along
distal half.
Leg 2 (Fig. 8a).— Basis without inner spine First
segment of endopod with hairlike setules along outer
margin.
Leg 3 (Fig. 8b).— Fine ornamentation resembling
that of leg 2.
Leg 4 (Fig. 8c).— Coxa with only 1 group of outer
spines.
Leg 5 (Fig. 8d).— Two-segmented. First segment
130 x 125 ym, with distal outer seta and group of
spines. Second segment elongate, 161 x 68 ^m, with
2 outer smooth spines, 52 and 55 ^m, distal smooth
seta 70 ym, and terminal finely barbed spine 147 ym.
These 3 spines with small spines near their inser-
tions. Two groups of small spines on inner side of
segment.
Leg 6 (Fig. 6i).— Probably represented by 2 setae
on genital area.
Color— Living specimens in transmitted light with
opaque gray body, eye red.
239
FISHERY BULLETIN: VOL. 84, NO. 2
Figure 8— Adult female of Leptinogaster major, a-d: a, leg 2 and intercoxal plate, anterior (scale F); b, leg 3 and intercoxal plate, anterior
(F); c, leg 4 and intercoxal plate, anterior (F); d, leg 5, lateral (A). Adult male of Leptinogaster major: e, dorsal (I).
240
HUMES: COPEPODIDS AND ADULTS OF LEPTINOGASTER MAJOR
Adult Male
Figures 8e, 9a-j
Size-Length 1.82 mm (1.70-2.04 mm) and
greatest width 0.43 mm (0.40-0.47 mm), based on 10
specimens.
Body form (Fig. 8e).— Similar to female but 10
body segments including and posterior to segment
of leg 1. Urosome (Fig. 9a) 6-segmented. Segment
of leg 5 135 x 236 ^m in dorsal view, with spines
on ventral surface as in female Four postgenital
segments from anterior to posterior 140 x 166, 135
x 143, 113 x 128, and 151 x 109 (im. Anal segment
with spines as in female Cephalosome ventrally with
outer strip of small spines and small sclerotized area
as in female
Caudal ramus (Fig. 9a).— As in female but dimen-
sions 174 x 38 /um, ratio 4.6:1.
Rostrum, first antenna, second antenna, labrum,
mandible, paragnath, first maxilla, and second max-
illa as in female
Maxilliped (Fig. 9b).— Four-segmented. First seg-
ment with 1 inner smooth seta 50 fim. Elongate
second segment with 2 inner setae and 2 groups of
short spines. Small third segment unarmed. Claw
208 pm, proximal part representing fourth segment
bearing 3 setae Concave margin of claw stri-
ated.
Legs 1-4.— With segmentation and armature as in
female, and ornamentation as in that sex except for
endopod of leg 2.
Figure 9— Adult male of Leptinogaster major: a, urosome, dorsal (scale H); b, maxilliped, posterior (B); c, endopod of leg 2, anterior
(F); d, second segment of endopod of right leg, anterior (B); e, second segment of endopod of left leg (same individual as in d), anterior
Q3); f, second segment of endopod of leg 2, anterior (B); g, leg 5, dorsal (B); h, leg 5, ventrolateral (B); i, leg 6, ventral (F); j, sperma-
tophore, attached to female, ventral (A).
241
FISHERY BULLETIN: VOL. 84, NO. 2
Leg 2 (Fig. 9c).— Endopod showing sexual dimor-
phism in having variable nodose outer margin on
second segment (Fig. 9d, e, f). Number of nodes from
4-6, and not always same in 1 individual, as in Fig.
9d, e
Leg 5 (Fig. 9g, h).— Resembling that of female
Second segment in 2 individuals 101 x 47 /mi (Fig.
9g) with 4 major elements from proximal to distal
45, 42, 80, and 78 /mi, and 86 x 42 Mm (Fig. 9h) with
elements 22, 26, 65, and 73 /mi.
Leg 6 (Fig. 9i).— Represented by single smooth seta
49 /mi and adjacent group of small spines on corner
of genital area.
Spermatophore (Fig. 9j).— Elongate, approximately
220 x 78 /mi without neck.
Color— As in female
DISCUSSION
This study permits certain observations to made
concerning the postnaupliar development of Leptino-
gaster major. A summary of these is given in Table 3.
1) All five copepodid stages are present in the
mantle cavity of My a arenaria.
2) The presence of Copepodid I in Mya suggests
that either the last nauplius molts outside the clam
and then enters, or that this nauplius enters the clam
and then molts.
3) Copepodid I is SaphirellaAike in body form;
Copepodid II and later copepodids have a body form
more like the adult.
4) The number of body segments increases from
5 in Copepodid I to 9 in the adult female and 10 in
the adult mala
5) The armature of the caudal ramus remains
unchanged from Copepodid I onward, but the caudal
ramus lengthens in successive copepodid stages and
in the adults.
6) The first antenna is slow in reaching final
form, being 5-segmented in Copepodid I and not
reaching its fully 6-segmented condition until the
adult.
7) The second antenna has an indistinct fourth
segment in Copepodid I, but is clearly 4-segmented
thereafter.
8) The labrum of Copepodid I is broad and or-
namented with spines, but in Copepodid II and
subsequently it is pointed and smooth.
9) The mandible of Copepodid I is a simple
blade, but in Copepodid II and succeeding stages
there are 3 terminal elements as in the adult.
10) The first maxilla of Copepodid I is similar to
that of Copepodid II and following stages.
11) The second maxilla has terminal setae in
Copepodid I but a terminal claw thereafter.
12) The maxilliped in Copepodid I is elongate and
4-segmented with long setae but in Copepodid II and
Copepodid III it is small with 4 weak unarmed seg-
ments. From this point on, the maxilliped in the
female shows further reduction, while in the male
it undergoes enlargement and specialization. In the
female of Copepodid IV it is minute 2-segmented,
and unarmed; in Copepodid V and in the adult it is
reduced to 2 small setae In the male of Copepodid
IV the maxilliped is 3-segmented, pointed, with 2
setae; in Copepodid V it is 4-segmented, pointed,
with 3 setae; in the adult male it is 4-segmented with
a long terminal claw.
13) The full complement of 4 biramous 3-seg-
mented legs is not reached until Copepodid V
14) The inner spine on the basis of the endopod
of leg 1 first appears in Copepodid II.
15) Leg 5 is absent in Copepodid I and Copepodid
II, is represented by 2 setae in Copepodid III, and
abruptly becomes 2-segmented with full armature
in Copepodid IV
16) Sexual dimorphism in legs 1-4 occurs only in
the endopod of leg 2 in the adult male
17) Sexual differentiation during copepodid
development first occurs in Copepodid IV, where
the male and female maxillipeds are differently
formed.
The maxilliped in the adult female is said to be
absent in Leptinogaster histrio (Bocquet and Stock
1958; Bacescu and Por 1959), in the genus Myocheres
(Wilson 1950), in Leptinogaster inflata (Allen 1956),
in Leptinogaster scobina (Humes and Cressey 1958),
and in Leptinogaster dentata (Humes and Cressey
1958). The maxilliped has now been traced through-
out copepodid development, and it is apparent that
a remnant of this appendage exists in the adult
female of L. major.
This discovery prompted a reexamination of adult
females of two species of Leptinogaster, L. scobina
and L. dentata. In both the maxilliped is represented
by two very small setae, as in L. major. It is not sur-
prising that these setae were overlooked, since they
are very minute and readily seen only in well-cleared
specimens.
Although the remaining species of Leptinogaster,
L. histrio (Pelseneer, 1929), L. pholadis (Pelseneer,
1929), L. inflata (Allen, 1956), and a new species con-
242
HUMES: COPEPODIDS AND ADULTS OF LEPTINOGASTER MAJOR
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243
FISHERY BULLETIN: VOL. 84, NO. 2
tained in Gooding's thesis (1963) have not been re-
examined, it appears likely that the presence of a
very reduced maxilliped in the adult female is a
generic character in Leptinogaster.
Gooding (1963:218-220) discussed the generic
status ofSaphirella T. Scott, 1894, pointing out that
species of Saphirella may represent Copepodid I
stages of clausidiids. In his thorough description of
Copepodid I of Leptinogaster a significant difference
seems to be in the body length, which Gooding gave
as 0.45 mm, while in this study the length is 0.57
mm (0.45-0.60 mm).
Although the genus Leptinogaster has been assign-
ed to various families (Table 1), its presently agreed
location appears to be in the Clausidiidae Embleton,
1901, along with Clausidium Kossmann, 1874, Con-
chyliurus Bocquet and Stock, 1957a, Giardella
Canu, 1888, Hemieyclops Boeck, 1873, Hersiliodes
Canu, 1888, and Hippomolgus G.O. Sars, 1917.
[According to the phylogenetic analysis of Ho (1984),
the genus Myzomolgus Bocquet and Stock, 1957b,
should be removed from the Clausidiidae and placed
close to the Catiniidae Bocquet and Stock, 1957b.]
The family Clausidiidae, containing seven genera of
certain status, shows several features: first anten-
na 6- or 7-segmented; second antenna 4-segmented
with third segment having in some cases prehensile
elements and fourth segment without a strong claw;
mandible with spine (or spinelike process) and 2 or
3 accessory elements (setae, spines); labrum with
rounded margin, mostly entire without median in-
dentation, except triangular in Leptinogaster; first
maxilla often with 2 lobes, but with 1 lobe having
2 groups of setae in Leptinogaster and 1 lobe with
a few setae in Clausidium; maxilliped in female
mostly 2-, 3-, or 4-segmented, but in Leptinogaster
reduced to 2 setae; maxilliped in male 2- or 3-seg-
mented plus claw (in Hippomolgus male unknown);
legs 1-4 biramous and 3-segmented (endopod of leg
1 bearing suckers in Clausidium); leg 5 2-segmented
(though in some first segment not clearly separated
from body).
Leptinogaster falls within this concept of the
family Clausidiidae Neighboring families have fun-
damentally different features, e.g., the Clausiidae
(first antenna 3-6 segmented; legs 1-4 showing
various degrees of reduction (as characterized by
Wilson and Illg (1955)), the Myicolidae (3-segmented
second antenna with strong terminal claw, max-
illiped in female a small unarmed lobe), and the
Ergasilidae (second antenna with a strong terminal
claw, maxilliped often absent in female, legs 1-4 with
some reduction). More information on the develop-
mental stages of the members of these families
would contribute greatly to understanding their
interrelationships.
ACKNOWLEDGMENTS
I thank Roger F. Cressey who aided in the collec-
tion of the copepods from Mya at Cotuit in 1957 and
who provided M. S. Wilson's notes and correspon-
dence concerning Leptinogaster (= Myocheres) ma-
jor which are in the custody of the National Museum
of Natural History, Smithsonian Institution. I thank
also Geoffrey A. Boxshall, British Museum (Natural
History), and Paul L. Illg, University of Washington,
for helpful suggestions.
LITERATURE CITED
Allen, J. A.
1956. Myocheres inflata a new species of parasitic copepod
from the Bahamas. J. Parasitol. 42:60-67.
B&CESCU, M., AND F. POR.
1959. Cyclopoide comensale (Clausidiide si Clausiide) din
Marea Neagra si descrierea unui gen nou, Pontoclausia gen.
nov. In Omagiu lui Traian Savalescu cu prilejul implinirii a
70 e ani, p. 11-30. Acad. Rep. Pop. Rom.
Bocquet, C, and J. H. Stock.
1957a. Copepodes parasites d'invertebres des cotes de France
I. Sur deux genres de la famille des Clausidiidae, commen-
saux de mollusques: Hersiliodes Canu et Conchyliurus nov.
gen. Proa K. Ned. Akad. Wet, Ser. C Biol. Med. Sci. 60:
212-222.
1957b. Copepodes parasites d'invertebres des cotes de France
IVa. Le double parasitisme de Sipunculus nudus L. par
Myzomolgus stupendus. nov. gen., nov. sp., et Catinia plana
nov. gen., nov. sp., copepodes cyclopoi'des tres remarquables.
Proa K. Ned. Akad. Wet, Ser. C Biol. Med. Sci. 60:410-
431.
1958. Copepodes parasites d'invertebres des cotes de la Man-
che, IV. Sur les trois genres synonymes de copepodes
cyclopoi'des, Leptinogaster Pelseneer, Strongylopleura
Pelseneer et Myocheres Wilson (Clausidiidae). Arch. Zool.
Exp. Gen. 96:71-89.
Boeck, A.
1873. Nye Slaegter og Arter af Saltvands-Copepoder. Forh.
Vidensk.-Selsk. Christiania (1872), p. 35-60.
Canu, E.
1888. Les copepodes marins du Boulonnais. III. Les Her-
siliidae, famille nouvelle de copepodes commensaux. Bull.
Sci. Fr. Belg. 19:402-432.
Causey, D.
1953. Parasitic Copepoda from Grand Isle, Louisiana Occas.
Pap. Mar. Lab., La. State Univ. No. 7, 18 p.
Deevey, G. B.
1948. The zooplankton of Tisbury Great Pond. Bull. Bingham
Oceanogr. Collect, Yale Univ. 12:1-44.
1960. The zooplankton of the surface waters of the Delaware
Bay region. Bull. Bingham Oceanogr. Collect, Yale Univ.
17:5-53.
Embleton, A. L.
1901. Goidelia japonica - a new entozoic copepod from Japan,
associated with an infusorian (Trichodina). Trans. Linn. Soa
Lond. 2d Ser., Zool. 28:211-228.
244
HUMES: COPEPODIDS AND ADULTS OF LEPTINOGASTER MAJOR
Gooding, R. U.
1963. External morphology and classification of marine
poecilostome copepods belonging to the families Clausidiidae,
Clausiidae, Nereicolidae, Eunicicolidae, Synaptiphilidae,
Catiniidae, Anomopsyllidae, and Echiurophilidae. Ph.D.
Thesis, Univ. Washington, Seattle, 247 p.
Ho, J.-S.
1984. New family of poecilostomatoid copepods (Spiophani-
colidae) parasitic on polychaetes from southern California,
with a phylogenetic analysis of nereicoliform families. J.
Crustacean Biol. 4:134-146.
Humes, A. G., and R. F. Cressey.
1958. Copepod parasites of mollusks in West Africa. Bull.
Inst. Ft. Afr. Noire 20(A):92 1-942.
1960. Seasonal population changes and host relationships of
Myocheres major (Williams), a cyclopoid copepod from pelecy-
pods. Crustaceana 1:307-325.
Humes, A. G, and R. U. Gooding.
1964. A method for studying the external anatomy of cope-
pods. Crustaceana 6:238-240.
Kossmann, R.
1874. Ueber Clausidium testudo, einen neuen Copepoden,
nebst Bemerkungen uber das System der halbparasitischen
Copepoden. Verh. Phys.-Med. Ges. Wurzburg, n.f. 7:280-293.
Monod, T., and R.-Ph. Dollfus.
1934. Des copepodes parasites de mollusques (deuxieme sup-
plement). Ann. Parasitol. Hum. Comp. 12:309-321.
Pearse, A. S.
1947. Parasitic copepods from Beaufort, North Carolina. J.
Elisha Mitchell Sci. Soc. 63:1-16.
Pelseneer, P.
1929. Copepodes parasites de mollusques. Ann. Soc R. Zool.
Belg. (1928) 59:33-49.
Sars, G. O.
1917. An account of the Crustacea of Norway with short
descriptions and figures of all the species. In Vol. VI Cope-
poda Cyclopoida Parts XI and XII Clausidiidae,
Lichomolgidae (part), p. 141-172. Bergen Museum, Bergen.
Scott, T.
1894. Report on Entomostraca from the Gulf of Guinea, col-
lected by John Rattray, B.Sc Trans. Linn. Soc Lond. 2d
Ser., Zool. 6:1-161.
Sewell, R. B. S.
1949. The littoral and semi-parasitic Cyclopoida, the Monstril-
loida and Notodelphyoida. Sci. Rep. John Murray Exped.
9(2):17-199.
Sharpe, R. W.
1910. Notes on the marine Copepoda and Cladocera of Woods
Hole and adjacent regions, including a synopsis of the genera
of the Harpacticoida. Proc. U.S. Nat. Mus. 38:405-436.
Williams, L. W
1907. A list of the Rhode Island Copepoda, Phyllopoda, and
Ostracoda, with new species of Copepoda In Thirty-seventh
Annual Report of the Commissioners of Inland Fisheries of
Rhode Island, p. 69-79. Spec. Pap. 30.
Wilson, C. B.
1932. The copepods of the Woods Hole region Massachusetts.
U.S. Nat. Mus. Bull. 158, 635 p.
Wilson, M. S.
1950. A new genus proposed for Lichomolgus major Williams
(Copepoda, Cyclopoida). J. Wash. Acad. Sci. 40:298-299.
Wilson, M. S., and P. L. Illg.
1955. The family Clausiidae (Copepoda, Cyclopoida). Proa
Biol. Soc. Wash. 68:129-141.
245
REPRODUCTIVE BIOLOGY OF
FEMALE SPOTTED DOLPHINS, STENELLA ATTENUATA,
FROM THE EASTERN TROPICAL PACIFIC
A. C. Myrick, Jr., A. A. Hohn, J. Barlow, and
P. A. Sloan1
ABSTRACT
Reproductive parameters were estimated from about 4,700 female spotted dolphins collected in the eastern
tropical Pacific from 1973 to 1981. From this sample, specimens for which ages were estimated were
divided into two subsets and were used to estimate age-specific rates for the northern offshore stock
of this species. The youngest sexually mature individual was 10 years old; the oldest immature was 17
years; the youngest and oldest pregnant individuals were 10 and 35 years, respectively. There was high
individual variability in the accumulation of corpora with age; the ovulation rate appears to slow abruptly
after the eighth ovulation. Average age at attainment of sexual maturity (ASM) for all years ranged
from 10.7 to 12.2 years (x = 11.4 years) for two sets of age estimates; no significant temporal change
in ASM was detected. Correlation between color phase and state of sexual maturity suggests that color
phase may be a good indicator of maturity for this stock. The average annual pregnancy rate was about
0.33; this rate did not change significantly with age. The calving interval was 3.03 years (SE = 0.205).
The lactation period was 1.66 years, but there was a significant increase noted in the percent lactating
from 1973 to 1981. A low percentage of postreproductive females was found in the sample (0.4%) in-
dicating that reproductive senescence is of little importance in reproductive rates of this stock.
Purse seine operations of the yellowfin tuna fishery
in the eastern tropical Pacific Ocean (ETP) have
caused high mortality of the spotted dolphin,
Stenella attenuata (Perrin 1969a, 1970). Estimated
incidental kills for the northern offshore stock of
spotted dolphins were between 100,000 and 400,000
annually throughout the 1960's and early 1970's
(Smith 1983). Since 1968, research efforts by the Na-
tional Marine Fisheries Service (NMFS) have
focused on assessing the biological consequences of
the large incidental kill of this and other affected
dolphins using specimens and data collected by
NMFS observers aboard U.S. tuna seiners. Perrin
et al. (1976) presented the first comprehensive
description of spotted dolphin life history and
reproduction for specimens from the ETP. The ac-
cumulation of thousands of additional specimens, the
sharp decline in dolphin mortality (Smith 1983; Ham-
mond and Tsai 1983), and the improvements made
in estimating age since that study (Myrick et al.
1983) have made a new analysis necessary.
The purpose of this paper is to estimate the
reproductive parameters of the female spotted
dolphin, based on analyses which include more data
and a better age estimating method than previous
1 Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA 92038.
studies. Reproductive features of the male spotted
dolphin (Hohn et al. 1985) and temporal trends in
reproduction in the northern offshore stock (Barlow
1985) are discussed in separate papers.
MATERIALS AND METHODS
Samples
The specimens were analyzed as three samples.
The "overall" sample contained about 4,700 speci-
mens that had been collected from 1973 through
1981. A second sample for which ages were esti-
mated contained 580 specimens selected randomly
from more than 3,500 specimens collected in 1973
through most of 1978 (the 1973-78 aged sample). The
randomly chosen 1973-78 aged sample did not in-
clude any of the specimens studied by Perrin et al.
(1976). The third sample (the 1981 aged sample) was
composed of 226 specimens which had been collected
in 1981 and for which ages were estimated. It in-
cluded almost all specimens for which ovaries and
teeth were collected in that year. The two aged sam-
ples, referred to collectively as the aged sample, are
subsets of the overall sample In several analyses the
1973-78 aged sample was divided into 1973-74 and
1975-78 subsamples in an effort to detect possible
temporal changes in reproductive rates. Only the
Manuscript accepted June 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
247
FISHERY BULLETIN: VOL. 84, NO. 2
northern offshore stock of spotted dolphins (as de-
fined by Smith 1983) is treated in this analysis. The
geographic boundary used to divide it from a south-
ern stock is lat. 1°S (Henderson et al. 1980).
Life History Data
Data and specimens were collected by biological
technicians aboard tuna purse seine vessels in the
ETP. Biological data used in this analysis are body
length, color phase, reproductive condition (preg-
nant, lactating, or resting), and corpora counts for
each specimen (see Perrin et al. [1976] for a descrip-
tion of collection and examination procedures).
Although there is no certainty that all ovarian cor-
pora persist for life in all delphinids (Perrin and
Re illy 1984), corpora counts were used with age to
estimate ovulation rates. Counts included corpora
albicantia (CAs), corpora lutea (CLs), and in some
cases corpora atretica (atretic follicles). Only
specimens that had both ovaries examined were in-
cluded in the ovulation rate analyses.
Age Estimates
Ages were estimated for about 800 specimens
(from 1973 to 1978 and 1981 samples) by counting
growth layer groups (GLGs, Perrin and Myrick 1980)
in the dentine and cementum of decalcified and
hematoxylin-stained thin sections (Myrick et al.
1983). Tooth readings were made independently by
two readers (A. C. Myrick and A. A. Hohn), without
referring to field or laboratory data on size or repro-
ductive condition. For the 1973-78 sample, a tooth
of each specimen was read at least three times by
each reader. Age estimates by each reader were sig-
nificantly different (Reilly et al. 1983). To minimize
the differences, the mean of the multiple age esti-
mates by each reader was calculated and the average
of the two means was used as the estimate of a
specimen's aga For the 1981 sample a tooth from
each specimen was read once by each reader after
calibration tests showed that differences in estimates
between readers were acceptably small (Reilly et al.
1983). An average of these two readings was used
for specimen age.
We consider the method we used to estimate ages
improved over that used by Perrin et al. (1976)
because
1) the preparation technique we used provides
superior resolution of GLGs (Myrick et al. 1983);
2) the new method of reading utilizes GLGs in
the cementum as well as in dentine and allows a more
accurate estimate of maximum age for adults
(Myrick et al. 1983; see also Kasuya 1976);
3) calibration of GLGs in tetracycline-labeled
teeth of Hawaiian spinner dolphins, Stenella longi-
rostris (Myrick et al. 1984), has provided a basis for
interpreting dental layering within an absolute-time
framework (Myrick et al. 1983; Myrick et al. 1984).
Perrin et al. (1976) used the term tooth layers in lieu
of known time units.
RESULTS AND DISCUSSION
Composition of Samples
Chi-square (contingency) tests were used to evalu-
ate whether fractions of mature, pregnant, and lac-
tating females in the 1973-78 aged sample were a
representative subset of the overall sample for those
years. For all three tests, differences were not sig-
nificant (P > 0.05).
Reproductive statistics showed some differences
between years (Table 1). Chi-square tests were
carried out for homogeneity between 1973-74 and
Table 1.— Number of sexually mature, pregnant only, lactating only, simultaneously pregnant and
lactating, and "resting" female spotted dolphins, and the proportion of the sample pregnant or
lactating in the aged and overall samples. The proportion pregnant and proportion lactating in-
clude the simultaneously pregnant and lactating specimens.
Number
Proportion
Years
Sexually
mature
Pregnant
only
Lactating
only
Pregnant
and
lacting
Resting
Pregnant
Lactating
Aged
1973-74
188
57
87
7
38
0.34
0.50
1975-78
205
48
100
13
44
0.30
0.55
1981
149
34
86
9
17
0.29
0.64
Total
542
139
273
29
99
0.31
0.56
Aged and unaged
1973-81
2,979
780
1,480
151
568
0.31
0.55
248
MYRICK ET AL.: REPRODUCTIVE BIOLOGY OF SPOTTED DOLPHINS
1981 aged samples and between 1975-78 and 1981
aged samples for numbers of specimens pregnant,
lactating, and resting. These tests revealed signifi-
cant differences (1973-74 vs. 1981: xl = 7.46, P =
0.024; 75-78 vs. 1981: xl = 6.16, P = 0.046.). These
differences are the result of an increase in the
relative frequency of lactating females (see section
on Lactation Period). There were no differences in
percent pregnant during this time (see also Barlow
1985).
Ovulation Rate
Individual Variability
Perrin et al. (1976) found high variability in the
number of corpora (corpora atretica included) for a
given age (in tooth layers). Nevertheless, by fitting
a power curve to the average number of corpora as
a function of average reproductive age, they deter-
mined that the average ovulation rate slowed
abruptly from about "four during the first layer, [to]
two during the second, and about one per layer there-
after" (Perrin et al. 1976, p. 261).
The sexually mature specimens in the combined
aged samples were used in our study to plot average
frequency of corpora (corpora atretica excluded) on
estimated age (Fig. 1). Regressions for the 1973-74
sample and for the 1981 sample are not significant-
ly different; when the samples are pooled, the
resulting slope is 0.61 corpora/yr. A plot of number
of corpora on age for all individuals (n = 542) in
mature age classes (10 through 38 yr old) for all aged
specimens (Fig. 2) showed a significant slope (P <
0.0001) but a low correlation (r2 = 0.397), indicating
high individual variability. For example, the sample
included 12- and 13-yr-olds with 7 or 8 corpora, and
21-yr-olds with 4 or fewer corpora. A 38-yr-old had
only 1 1 corpora (Table 2). These results support those
of Sergeant (1962), Brodie (1971), Kasuya et al.
(1974), and Perrin et al. (1976), that great individual
variation occurs in ovulation rates among odonto-
cetes.
Table 2. — Summary of age-related reproductive
statistics for female spotted dolphins taken in
1973-78 and 1981.
Estimated
age
Variable
(years)
Range of ages with no corpora
0-17
Oldest with one corpus
23
Youngest with one corpus
10
Youngest pregnant
10
Oldest pregnant
35
Average age pregnant
18
Oldest simultaneously
pregnant and lactating
29
Oldest lactating
36
Youngest lactating
10
Oldest
38
Changes in Rate
Ovulation rate apparently decreases with repro-
ductive age If ovulation and mortality rates were
Figure 1— Linear regression of number of cor-
pora on estimated age as gross estimates of
ovulation rates in female spotted dolphins.
Points represent averages for 1-yr age classes
(1973-78 samples = closed circles; 1981 sam-
ple = open circles).
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AGE ESTIMATES (years)
249
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MYRICK ET AL.: REPRODUCTIVE BIOLOGY OF SPOTTED DOLPHINS
constant, a semilog plot of the frequency distribu-
tion of corpora counts would be linear. The slope of
this line would be negative, and its value would be
determined by mortality and ovulation rates. The
observed shape of the log-frequency distribution of
corpora counts for spotted dolphins (Fig. 3) suggests
that ovulation and/or mortality rates are not con-
stant. After about eight ovulations, log-frequencies
decrease monotonically and nearly linearly. For up
to the first eight ovulations, the rate is apparently
much higher (presuming, again, that mortality rates
do not change with the number of ovulations and
that all CAs persist for life [Perrin and Reilly 1984]).
This supports the findings of Perrin et al. (1976) that
ovulation rates decrease with reproductive age in
spotted dolphins.
mates using a variation of the method described by
DeMaster (1978). Age-specific maturation rates were
used to calculate mean ASM as
ASM = J. (x - 0.5) Px
where x is age class, Px is the probability of first
ovulating in age class x, and w is the maximum age
in the sample. The term (x - 0.5) was substituted
for DeMaster's (x) so that the mean age in an age-
class interval would be represented by the midpoint
of that interval. The terms Px were estimated as
Px =f(x + 1) -f{x),
Sexual Maturity
The age at which a female first ovulates is con-
sidered the age at attainment of sexual maturity
(DeMaster 1978, 1984). Using the aged samples, we
estimated average age at sexual maturity (ASM)
using two methods. For these estimates, ages were
grouped by 1-yr intervals: age-class 1 included
specimens 0-1.0 yr, age-class 2 from 1.1 to 2.0 yr, etc
The mean age of sexually mature females was 18.7
yr.
Method-One
ASM was estimated from both readers' age esti-
where/(:r) is the probability of being mature at age
x. The function f(x) was estimated as the best least-
squares fit of a curve (York 1983) to the observed
values of percent mature by age class. A 3-parameter
sigmoid curve based on a modification of the logistic
equation was found to give an adequate fit of the
data (Fig. 4).
ASMs were calculated separately for the aged
samples, 1973-74, 1975-78, and 1981. There were no
significant differences among these samples (P >
0.05). The ASM for all samples combined was 10.7
(var. = 0.03) to 12.2 (var. = 0.05) yr for the two
readers. The average of these two ASM estimates
was 11.4 yr. The precision between readers in age
estimates of the 1981 specimens was greater than
(O
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Figure 3.— Semilog plot of the frequency distribution
of corpora counts for female spotted dolphins.
J L
8 10 12 14
NUMBER OF CORPORA
16
18
20
251
FISHERY BULLETIN: VOL. 84, NO. 2
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ESTIMATED AGE (years)
Figure 4.— Fraction of sexually mature female spotted
dolphins versus age based on estimates of two readers.
Logistic curves are fitted to the data. Bars predict ages at
which 50% are sexually mature
for the 1973-78 specimens (Reilley et al. 1983); the
mean ASM range for the 1981 sample was 11.6-11.7
yr-
Method Two
The second method we used for estimating ASM
was to interpolate, from a maturation curve, the age
at which 50% of the specimens were mature Again,
sigmoid curve fits of the percent of mature speci-
mens as a function of age were used for the matura-
tion curves. For all aged samples combined, the
method predicts an ASM of 10.6-12.0 yr (for the two
readers), with an average of 11.3 yr.
Our overall estimates of ASM (11.3 or 11.4 yr) dif-
fer markedly from the ASM estimated for ETP
spotted dolphins by Perrin et al. (1976) which was
9 tooth layers, "5.1 to 8.3 yr, depending on [which]
layering hypothesis is used" (p. 250). Our estimates
also differ from the ASM estimate for spotted
dolphins off the Japanese coast by Kasuya (1976)
which was 9 yr.
Biases in ASM
All of the above estimates of ASM are dependent
on two important assumptions. First, we assume that
counts of dentinal and cemental GLGs give precise
and unbiased estimates of age Second, we assume
that our samples are unbiased with respect to the
maturity of the specimens collected. Potential biases
would result if the assumptions were invalid. Because
age estimates of the two readers differ significant-
ly (Reilly et al. 1983), the difference in ASM esti-
mates for the readers (1.5 yr) should be taken as a
minimum range in the ASM estimates.
Color Pattern and Maturity
Perrin (1969b) described the ontogenetic develop-
ment of color pattern in spotted dolphins in the ETP:
he divided the development into five sequential
phases (neonatal, two-tone, speckled, mottled, and
fused) based on patterns of ventral and dorsal spots.
Kasuya et al. (1974) described color-phase changes
in western Pacific spotted dolphins using somewhat
different definitions than those of Perrin (1969b),
although the description indicated that the onto-
genetic changes were similar to those observed by
Perrin. Perrin (1969b) found a close correlation be-
tween size and color pattern and (for a smaller sam-
ple) between sexual maturity and color pattern.
Kasuya et al. (1974) found that the development of
the adult color pattern in spotted dolphins from the
western Pacific coincides with the attainment of sex-
ual maturity.
In our sample of spotted dolphins, there was con-
siderable overlap in age and length between animals
with different color patterns, but a correlation be-
tween color pattern and state of maturity was evi-
dent. In females from the aged sample, speckled
animals ranged from 3 to 18 yr, mottled from 6 to
32 yr, and fused from 10 to 38 yr. A similar overlap
occurred in body-length distribution from the overall
sample of females, 135-200 cm (n = 166), 140-210
cm (n = 179), and 155-220 cm (n = 188) for speckled,
mottled, and fused specimens, respectively. However,
96% of fused animals (n = 2,764), 50% of mottled
animals (n = 857), and only 4% of speckled animals
(n = 559) were sexually mature
In addition, for a given length or age class, females
with a fused color pattern appeared to have been
mature for a longer time than animals with a mottled
pattern. For females of similar lengths, mature
specimens with a fused color pattern had more cor-
pora than those with a mottled color pattern (Fig.
5). Similarly for the aged sample, the fused speci-
mens within a given length group tended to have
more total corpora than mottled specimens, and
when specimens in the same body length categories
were of similar ages, fused animals had more total
corpora.
252
MYRICK ET AL.: REPRODUCTIVE BIOLOGY OF SPOTTED DOLPHINS
12
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LENGTH (cm)
200
210
220
Figure 5— Average number of corpora for mottled (M) and fused (F) color-phase specimens within each 5
cm length grouping for the overall sample of female spotted dolphins. Bars represent one standard error
from the mean. Sample sizes are shown.
These results suggest that color phase may in-
dicate sexual maturity more accurately than either
age or length. Perrin (1969b) found 0% speckled (n
= 5), 60% mottled (n = 16), and 100% fused (n =
33) females to be sexually mature Using color phases
that roughly correspond to the late mottled and
fused stages of Perrin (1969b), Kasuya et al. (1974)
found that 93% (n = 30) of the spotted dolphins in
the third stage and 100% in the last (fourth) stage
of dorsal spotting were sexually mature A similar
relationship between maturity and color pattern
exists in male spotted dolphins in the ETP (Hohn
et al. 1985). Assuming that the proportion of mature
specimens in a given color phase does not change
within a population, it would be possible to estimate
the percentage of sexually mature specimens in a
sample without having to examine the ovaries for
corpora.
Pregnancy Rate
The annual pregnancy rate (APR) of a population
is the fraction of mature females that would be ex-
pected to give birth in any given year. APR can be
estimated as the average fraction of mature females
that are pregnant divided by the gestation time in
years. The variance of this estimate is approximated
by
var(APR) = (-P/7V)2 var (TG)
+ (1/ZV) P(l - P)/np
where P is the proportion pregnant, TG is the
gestation time, and np is the sample size used to
estimate P (Perrin and Reilly 1984). We use 0.958
yr (11.5 mo) as the gestation period for spotted
253
FISHERY BULLETIN: VOL. 84, NO. 2
dolphins (Perrin et al. 1976). The variance in gesta-
tion time has not been calculated. We can, however,
reasonably estimate that 95% confidence limits
would span 0.1 yr. From this we estimate the var
(TG) to be 0.000625.
For the aged sample, 31.1% of the sexually mature
specimens (n = 542) were pregnant. For the overall
sample during the same years, 31.6% of the sexually
mature specimens (n = 2,458) were pregnant and
for all aged and imaged mature specimens from 1973
through 1981 inclusive (n = 2,979), 31.3% were preg-
nant (Table 1). By dividing the fraction of pregnant
females by the gestation period (0.958), annual
pregnancy rates of 0.325 and 0.330 were obtained
for the aged and overall samples, respectively. The
var (APR) for the overall sample is 0.0005.
To determine whether pregnancy rates changed
with age, we estimated percent pregnant for four
age-class intervals using the 1973-78 and 1981
samples combined. Sample size was small for esti-
mating age-specific rates with much precision.
Nevertheless, we detected neither a sustained in-
crease nor a sustained decrease in the percent of
pregnant females with age (Fig. 6); the variability
in the percent of pregnant females with age can be
accounted for by random sampling (x| = 4.6, P >
0.50). This result differs from that of Perrin et al.
(1976) which indicated a significant reduction in
pregnancy rate with age.
Calving Interval
Calving interval is an estimate of the mean period
between births for mature females. Typically, it is
estimated as the inverse of the annual pregnancy
rate (Perrin and Reilly 1984). The principal require-
ments for calculating the calving interval are un-
biased estimates of gestation time and of the frac-
tion of mature females that are pregnant. The
standard error in an estimate of calving interval (CI)
by these methods is approximated by
SE (CI) = (APR-4) var (APR)
(Perrin and Reilly 1984).
Given our calculated APR estimate of 0.330 for
the overall sample, the calving interval is 3.03 yr. The
standard error of this estimate is about 0.205. Al-
though it is difficult to prove that our estimates of
the percent of pregnant females are unbiased, sup-
port for such a position is given by Barlow's finding
that the percent of pregnant females varies little
with sampling conditions (including sampling season,
geographic area, dolphin school size, and dolphin kill-
per-set) (Barlow 1985). However, if annual variability
in the percent of pregnant females is important,
binomial sampling theory is likely to underestimate
our certainty in estimating the percent of pregnant
females, APR, and calving interval. Because no
significant trends were detected in the percentage
0.70 r
0.60
0.50
2 0.40
o
§ 0.30
E
O.
0.20
0.10 -
Lactating
Pregnant
<15 16-19 20-23 ^24
ESTIMATED AGE (years)
Figure 6— Proportion lactating and proportion pregnant as a function
of age for sexually mature female spotted dolphins, in 1973-78 and 1981.
Bars represent one standard error from the mean (n = 542).
254
MYRICK ET AL.: REPRODUCTIVE BIOLOGY OF SPOTTED DOLPHINS
of pregnant females from 1974 to 1983 (Barlow
1985) and because no significant changes were found
in pregnancy rates with age, estimates of calving in-
terval were not calculated for any of these possible
stratifications.
Previous estimates of calving interval for S. at-
tenuata include 2.5 yr for the southern offshore ETP
stock, 2.7-3.4 yr for the northern offshore ETP stock,
and 3.5-3.9 yr for a western North Pacific popula-
tion (all values taken from Perrin and Reilly 1984,
table 6). Our estimate, 3.06 yr, is thus close to
previous estimates for the ETP northern stock and
falls between the estimates for two other popula-
tions.
Lactation Period
The calving cycle in mammals can be thought of
as a gestation period, a lactation period, and (in some
cases) a resting period. Since gestation and lac-
tation can overlap, the calving interval can be less
than the sum of the gestation and lactation peri-
ods.
In this study, the duration of the lactation period
was estimated as the fraction of mature females that
are lactating multiplied by the calving interval in
years. Again, the assumption is that all reproduc-
tive stages of mature females are sampled without
bias. The estimated lactation period for the overall
sample is 1.66 yr.
Unlike the percent pregnant, the percentage of lac-
tating females has apparently increased over the
years between 1973-74 and 1981 (Table 1). Collabor-
ative evidence is provided by Barlow (1985). Barlow's
weighted regression of the percent of lactating
females regressed against year predicts values of
46% lactating for 1971 and 69% for 1983. These cor-
respond to a change in mean lactation period from
1.4 to 2.1 yr.
There were no significant differences in propor-
tion of lactating females in different age-classes for
all aged samples combined (x| = 2.58, P > 0.25)
(Fig. 6).
Evidence exists for considerable individual vari-
ability in calving interval and lactation period. The
sum of the estimated gestation time (0.958 yr)
plus the mean lactation period (1.66 yr) is about
2.6 yr; the mean calving interval, estimated as
the inverse of APR, is roughly 3 yr. We might pre-
dict from this that individuals would never be
simultaneously pregnant and lactating. In fact,
16% of the sampled pregnant females were lactat-
ing. This is implicit evidence of individual variabil-
ity.
Postreproductive Females
Several criteria have been used to identify post-
reproductive female odontocetes. Perrin et al. (1976)
described postreproductive spotted dolphins and Per-
rin et al. (1977) described postreproductive spinner
dolphins, S. longirostris. Both studies were based on
the presence of atrophic ("regressed" or "withered")
ovaries. In both cases, the incidence of postreproduc-
tive females was 1% or less of the sample In pilot
whales, Globicephala macrorhynchus, Marsh and
Kasuya (1984) found changes in the histology of the
ovary, such as a decrease in the volume of the cor-
tex and sclerosis of the arterial walls that are age
related and associated with senescence Senescent
females were characterized on the basis of follicle
abundance and the incidence of follicular atresia.
Postreproductive females also occurred in our sam-
ple Nine of the mature females collected from 1973
to 1982 had atrophic ovaries and thus are considered
to have been reproductively senescent. Their mean
ovary weights and maximum follicle diameters were
significantly different from the means of the other
mature females collected during these years (£-test,
P < 0.005) (Table 3, Fig. 7). None was lactating.
Evidence of decreased fertility was found in some
females without atrophic ovaries. Two groups were
extracted from the aged sample: 1) those specimens
that had 20 or more corpora (all but one was 20 yr
old or older), and 2) those specimens that were 20
yr old or older and had only four or fewer total cor-
pora (including atretica). Of the first group (n = 12),
the mean maximum follicle diameter was larger than
that of the atrophic-ovary sample (i-test, P < 0.005),
but the mean weights for both ovaries combined were
not significantly different (Table 4). Atretic corpora
constituted 24% of the total corpora, less than the
frequency of atresia found in the atrophic ovaries
(39%). The two specimens in this sample with the
highest proportion of corpora atretica also had
ovaries with maximum follicle diameter and ovary
weights within the range of the atrophic ovaries; in
addition, they had no CLs (corpora lutea) or Type
1 corpora. We consider these two females to have
been postreproductive Of the second group (n = 14),
the mean maximum follicle diameter and ovary
weight were not different from those in the sample
with more total corpora, but were markedly different
from those of the atrophic ovaries (£-test, P < 0.025).
None of these ovaries contained corpora atretica.
Comparison of females in the two groups provides
evidence that when the complement of follicles has
nearly been expended (through ovulation or atresia),
fertility diminishes. Of the first group, 5 of the 12
255
Table 3. — Combined ovary weights, maximum follicle diameter, and
corpora counts in "non-atrophic" (normal) ovaries with no corpus
lutem (n = 3,455) and atrophic ovaries (n = 9) of sexually mature
female spotted dolphins collected in 1973-82.
Non-atrophic
Atrophic
ovaries
ovaries
Variable
Mean
SE
Mean
SE
Combined ovary weight
4.9
0.05
3.0
0.30
Maximum follicle diameter
2.8
0.06
0.4
0.07
Total corpora excluding
atretica
6.8
0.09
12.4
1.36
Total corpora including
atretica
7.5
0.11
20.9
1.13
Corpora atretica
0.7
0.04
8.4
1.67
Percent of corpora
atretic
6.4
0.30
40.0
7.6
FISHERY BULLETIN: VOL. 84, NO. 2
lacked macroscopic follicles. Such specimens have
in common: 1) the absence of CLs and Type 1 cor-
pora, 2) a large number of total corpora, 3) a high
frequency of atresia (a relatively large proportion of
the total corpora), and 4) a maximum follicle
diameter of 0.5 mm or less. The incidence of obvious
senescence in the sample of spotted dolphins (0.4%)
is much less than that in pilot whale samples studied
(5% in Globicephala melaena from the northern
Atlantic Ocean [Sergeant 1962] and 25% in G.
macrorhynchus from the western Pacific [Marsh and
Kasuya 1984]). This may be indicative of inherent dif-
ferences in the social structure or longevity between
pilot whales and spotted dolphins.
Table 4.— Mean age, maximum follicle diameter, ovary weight, corpora counts, and reproductive states
for female spotted dolphins. Type 1 and Type 2 corpora defined by Perrin et al. (1976).
Maximum
Combined
follicle
ovary
Pregnant/
Age
diameter
weights
Total
Corpora
Percent
Type 1
Type 2
lactating
years
(mm)
(g)
corpora1
atretica
atretic
corpora
corpora
(0/0)
A. Females with 20 or more corpora (n = 12)
Mean
20.2
2.7
4.2
21.3
4.7
21.9
0.5
1.4
40
SE
1.0
0.5
0.5
0.3
0.8
3.6
0.2
0.4
B. Females 20
yr or older with four or
fewer corpora (n =
14)
Mean
22.6
2.5
5.1
2.7
0
0
0.9
0.9
100
SE
0.5
0.3
0.6
0.3
0
0
0.2
0.2
includes atretica.
specimens were pregnant or lactating. All 14 of the
second group were pregnant or lactating. Thus, the
first group shows reduced fertility when compared
with the second group. Marsh and Kasuya (1984)
described an age-related decline in follicle abundance
in pilot whales, stating that when follicles are
"depleted" the animals become senescent. The reduc-
tion in fertility indicated in our sample of spotted
dolphins is not strictly age-related; it is more depen-
dent on the number of corpora (including corpora
atretica) already present in the ovaries. This has been
shown to be true in western Pacific spotted dolphins
(Kasuya et al. 1974) and in sperm whales (Best 1967).
In addition to the postreproductive females with
atrophic ovaries, four mature females with normal-
appearing ovaries had no macroscopic follicles (one
of the atrophic ovaries contained no macroscopic
follicles). This is similar to the condition described
by Marsh and Kasuya (1984). The ovaries of these
specimens weighed from 2.2 to 5.9 g, had no CLs
or Type 1 or Type 2 corpora, and contained 8-22 total
corpora, 12% of which were atretic None were lac-
tating. They are considered to have been postrepro-
ductive also.
Spotted dolphin specimens were judged to have
been senescent when they had atrophic ovaries or
CONCLUSIONS
Several of our analyses have yielded results similar
to those reported previously for spotted dolphins by
others, notably Perrin et al. (1976) and Kasuya et
al. (1974). We found ovulation rates to have high in-
dividual variability with a markedly higher rate of
corpus formation in the earlier reproductive years
that decreases after a fixed number of ovulations has
occurred.
The conclusions reached by Perrin (1969b) and par-
ticularly by Kasuya et al. (1974) with regard to the
close correlation between color pattern and sexual
maturity in spotted dolphins are also supported by
our study. Ninety-six percent of the fused, 50% of
the mottled, and only 4% of the speckled specimens
were sexually mature Fused specimens had more
corpora and appeared to have been sexually mature
longer than mottled specimens of the same age or
length.
Our estimated length of the calving interval (3.03
yr) is within the range of earlier estimates calculated
for this stock by Perrin and Reilly (1984). It is also
within the range of estimates for two other spotted
dolphin stocks.
Some of our analyses, however, produced results
256
MYRICK ET AL.: REPRODUCTIVE BIOLOGY OF SPOTTED DOLPHINS
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FISHERY BULLETIN: VOL. 84, NO. 2
that contradict earlier findings. Based on the more
reliable method of estimating age in spotted dol-
phins, we believe that our findings present a clearer
picture of the reproductive information than has
been reported previously. Our aged samples showed
that the youngest sexually mature female was 10 yr
old— the same age as the youngest pregnant and the
youngest lactating specimens. This suggests that
some females must become sexually mature before
the age of 10, even though mature specimens
younger than 10 were not found in our sample The
average age of a pregnant female in our sample was
about 18 yr, and some females of about 35 yr old
were pregnant or nursing. These values are substan-
tially higher than estimated previously for this stock
(Perrin et al. 1976), but they are similar to, though
still somewhat higher than, estimates for the western
Pacific stock (Kasuya 1976).
The ASM estimate in this study (about 11.4 yr) is
higher than that estimated by Perrin et al. (1976).
Our calculations showed no significant difference
between the ASM calculated for the 1973-74 sam-
ple (taken during years of heavy fishing mortality)
and the ASM for the 1981 sample (taken after at
least 5 yr of reduced fishing mortality).
An ASM of 11.4 yr means that the youngest
average age of first parturition would be 12.3 yr (11
mo later). Since not all females would conceive at
first ovulation, the actual average age would be
greater than this. The implication of this protracted
period before reproduction and a long (3.03 yr)
calving interval is that spotted dolphin survival rates
must be very high in order to maintain a stable
population level.
There is a significant depression in the age struc-
ture of the 1973-78 and 1981 aged sample in the 6-12
yr age classes (Hohn and Myrick in prep.2). Similar
age-structure patterns, interpreted as reflecting
some sort of schooling segregation, have been en-
countered in studies of other delphinids (see review
by Perrin and Reilly 1984). If animals at or near the
age of sexual maturity have been regularly under-
sampled because their schools were not targets of
purse seines (Hohn and Scott 1983), the ASMs
calculated for the aged samples could be upwardly
biased. However, there is no evidence that the
depression in the age structure represents missing
animals that were sexually mature
The annual pregnancy rate averaged 0.33 from
1973 through 1981. There were no sustained upward
or downward changes in age-specific pregnancy rates
with increased age A similar result was shown by
Kasuya (1976) for the western stock, although his
values were somewhat lower than the rates we have
estimated for the northern offshore stock. Our esti-
mates are different from those of Perrin et al. (1976)
who reported high pregnancy rates among younger
specimens and a decreasing rate with increased age
The implications of an apparent progressive in-
crease in the lactation period are enigmatic It is
probable that the increase in lactation period reflects
the decrease in per capita mortality of calves due
to the more efficient releasing procedures employed
by the purse seine fleet from the mid-1970's onwards.
Decreased mortality of nursing calves would be
reflected by an apparent increase in the number of
lactating females because fewer nursing periods
were ended prematurely.
Our study of postreproductive specimens suggests
that fertility diminishes as the complement of
follicles for a female becomes expended through
ovulation or atresia. Female spotted dolphins with
atrophic ovaries or with no macroscopic follicles are
reproductively senescent. Although the expenditure
of follicles progresses with age, reduction in fertility
is not strictly age related. The occurrence of repro-
ductive senescence in spotted dolphins in this study
was negligible and the number of specimens in this
state probably is of limited importance to estimates
of reproductive parameters.
ACKNOWLEDGMENTS
We thank D. DeMaster, W. F. Perrin, and S. Reilly
for their helpful comments and recommendations on
early drafts of the manuscript. We are grateful to
J. Bengtson, D. Chapman, F Hester, J. Mead, A.
York, and R. Wells for their very thorough reviews.
J. Walker and S. Chivers assisted in organizing and
accessing the life history data and S. Chivers helped
with the analyses. D. Stanley and M. Kimura
prepared the tooth sections for the aged subsamples.
Special thanks go to H. Orr who prepared the figures
and to H. Becker and S. Richardson and the SWFC
Technical Support Staff who typed parts of the
manuscript. D. DeMaster, N. Lo, and S. Reilly
assisted in statistical testing of some of the samples.
J. Michalski edited the final draft.
2Hohn, A. A., and A. C. Myrick, Jr. The age structure of north-
ern offshore dolphins, Stenella attenuata, from the eastern tropical
Pacific Manuscr. in prep. Southwest Fisheries Center La Jolla
Laboratory, National Marine Fisheries Service, NOAA, P.O. Box
271, La Jolla, CA 92038.
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1985. Variability, trends, and biases in reproductive rates of
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MYRICK ET AL.: REPRODUCTIVE BIOLOGY OF SPOTTED DOLPHINS
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669.
Best, P. B.
1967. The sperm whale (Physeter catodon) off the west coast
of South Africa. 1. Ovarian changes and their significance
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Brodie, P. F
1971. A reconsideration of aspects of growth, reproduction,
and behavior of the white whale (Delphinapterus leucas) with
reference to the Cumberland Sound, Baffin Island, popula-
tion. J. Fish. Res. Board Can. 28:1309-1318.
DeMaster, D. P.
1978. Calculation of the average age of sexual maturity in
marine mammals. J. Fish. Res. Board Can. 35:912-
915.
1984. Review of techniques used to estimate the average age
at attainment of sexual maturity in marine mammals. In
W. F. Perrin, R. L. Brownell, Jr., and D. P. DeMaster (editors),
Reproduction in whales, dolphins and porpoises, p. 175-179.
Rep. Int. Whaling Comm. (Spec Issue No. 6).
Hammond, P. S., and K. T. Tsai.
1983. Dolphin mortality incidental to purse-seining for tunas
in the eastern Pacific Ocean, 1979-1981. Rep. Int. Whaling
Comm. 33:589-597.
Henderson, J. R., W. F Perrin, and R. B. Miller.
1980. Rate of gross annual production in dolphin populations
(Stenella spp. and Delphinus delphis) in the eastern tropical
Pacific 1973-78. SWFC, NMFS, NOAA, Admin. Rep.
LJ-80-02, 51 p.
Hohn, A. A., J. Barlow, and S. J. Chivers.
1985. Reproductive maturity and seasonality in male spotted
dolphins, Stenella attenuata, in the eastern tropical
Pacific Mar. Mammal Sci. l(4):273-293.
Hohn, A. A., and M. D. Scott.
1983. Segregation by age in schools of spotted dolphin in the
eastern tropical Pacific [Abstr.] Fifth Bienn. Biol. Mar.
Mammals, p. 47.
Kasuya, T.
1976. Reconsideration of life history parameters of the spotted
and striped dolphins based on cemental layers. Sci. Rep.
Whales Res. Inst. (Tokyo) 28:73-106.
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. (Tokyo)
26:157-226.
Marsh, H., and T. Kasuya.
1984. Changes in the ovaries of the short-finned pilot whale,
Globicephala macrorhynchus, with age and reproductive ac-
tivity. In W F. Perrin, R. L. Brownell, Jr., and D. P.
DeMaster (editors), Reproduction in whales, dolphins and
porpoises, p. 311-335. Rep. Int. Whaling Comm. (Spec Issue
No. 6).
Myrick, A. C, Jr., A. A. Hohn, P. A. Sloan, M. Kimura, and D.
Stanley.
1983. Estimating age of spotted and spinner dolphins (Sten-
ella attenuata and Stenella longirostris) from teeth. U.S.
Dep. Commer., NOAA Tech. Memo. NMFS SWFC-30, 17 p.
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.
Perrin, W F.
1969. Using porpoise to catch tuna. World Fishing 18(6):
42-45.
1970a. Color pattern of the eastern Pacific spotted porpoise
Stenella graffmani; Lonnberg (Cetacea, Delphinidae). Zool-
ogica (NY) 54:135-149.
1970b. The problem of porpoise mortality in the U.S. tropical
tuna fishery In Proceeding of the 6th Annual Conference
on Biological Sonar and Diving Mammals, p. 45-48. Stan-
ford Res. Inst., Menlo Park, CA.
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, 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 siren-
ians. Rep. Int. Whaling Comm. (Spec Issue No. 3), 229 p.
Perrin, W F, and S. B. Reilly.
1984. Reproductive parameters of dolphins and small whales
of the family delphinidae In W F. Perrin, R. L. Brownell,
Jr., and D. P. DeMaster (editors), Reproduction in whales,
dolphins and porpoises, p. 97-133. Rep. Int. Whaling Comm.
(Spec Issue No. 6).
Reilly, S. B, A. A. Hohn, and A. C. Myrick, Jr.
1983. Precision of age determination of northern offshore
spotted dolphins. U.S. Dep. Commer., NOAA Tech. Memo.
NMFS SWFC-35, 27 p.
Sergeant, D. E.
1962. The biology of the pilot or pothead whale Globicephala
melaena (Traill) in Newfoundland waters. Fish. Res. Board
Can. Bull. 132:1-84.
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.
York, A. E.
1983. Average age at first reproduction of the northern fur
seal (Callorhinus ursinus). Can. J. Fish. Aquat. Sci. 40:
121-127.
259
CHINOOK SALMON, ONCORHYNCHUS TSHAWYTSCHA,
SPAWNING ESCAPEMENT BASED ON MULTIPLE MARK-RECAPTURE
OF CARCASSES
Stephen D. Sykes and Louis W. Botsford1
ABSTRACT
Mark-recapture data from a population of chinook salmon, Oncorhynchus tshawytscha, carcasses were
collected for escapement estimates in a northern California stream. Escapement was taken to be im-
migration into the population of carcasses. Results from three methods of estimating total immigration
into this population— Jolly-Seber, Manly and Parr, and Jolly-Seber with a modified data set— were com-
pared to a weir count. Sources of violations of modeling assumptions, age-dependent catchability, and
survival were identified, but the estimates appeared to be relatively insensitive to these. The effect of
lower sampling intensity, which exacerbates effects of age-dependent catchability, was evaluated through
simulation. The third method appears to be the best of the three because 1) it requires the least sampling
effort, 2) it is the most robust with respect to violations of the assumption of equal catchability, and
3) it enables reanalysis of previously collected data. Standard errors and 95% confidence intervals of
estimates obtained by the third method were computed by simulation. Since the distribution of estimates
is asymmetrical, these confidence limits are preferred over standard expressions.
Pacific salmon fisheries are currently managed by
attempting to allow a specified number of fish to
escape the fishery, migrate upstream and spawn.
Proper management therefore requires accurate
estimates of this escapement. Since Pacific salmon
die immediately after spawning, escapement can be
estimated from the number of carcasses that accu-
mulate during a spawning season. The California
Department of Fish and Game (CDF&G) estimates
escapement of chinook salmon, Oncorhynchus
tshawytscha, each year using the methods of Schaef-
fer (Schaeffer 1951; Darroch 1961) and Peterson
(Seber 1982) to analyze mark-recapture data from
surveys of accumulated carcasses. Since the fish
enter the stream to spawn during the sampling
periods, the assumption of a closed population re-
quired by the Peterson estimate does not hold. The
Schaeffer method is designed to estimate numbers
from a stratified two sample experiment in which
fish are tagged at different locations (or different
times at one location as fish migrate upstream) and
are sampled at the same locations (or an upstream
point) at a later time. CDF&G carcass surveys, on
the other hand, involve sampling the same unstrati-
fied stretch of spawning stream several times. The
results described here are part of an attempt to
develop an accurate, efficient, and robust procedure
for estimating escapement from carcass data. A
department of Wildlife and Fisheries Biology, University of
California, Davis, CA 95616.
Manuscript accepted July 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
technique that allows not just estimates for current
and future years, but also could be used to analyze
mark-recapture data taken by CDF&G in past years
was desired.
Parker (1968) and Stauffer (1970) used standard
Jolly-Seber methods to estimate spawning run sizes
from mark-recapture data obtained from carcass
counts. However, they did not examine departures
from modeling assumptions by collecting appropri-
ate data in the field or statistically testing assump-
tions. Also, an independent count of the population
size was unavailable, hence actual errors in their
estimates could not be computed. In addition, car-
casses were carefully replaced where they had been
found after sampling and tagging, hence captured
carcasses would have a high probability of being
recaptured. Thus, their results were probably biased
because of heterogeneous capture probabilities.
To develop the estimation technique a mark-recap-
ture experiment was performed in the Bogus Creek
spawning area of the Upper Klamath River drainage
during the 1981 chinook salmon spawning run. As
a check on the estimates, a counting weir was placed
at the mouth of Bogus Creek. Salmon were counted
while they were in the weir trap, and were sub-
sequently released upstream. This mark-recapture
study differed from the usual mark-recapture
studies of fish and wildlife populations in that the
population was composed of carcasses (i.e., in-
dividuals enter the population by dying and leave
by predation and decay). Thus, the age of a carcass,
261
FISHERY BULLETIN: VOL. 84, NO. 2
as used here, refers to time since death rather than
time since recruitment.
The procedures followed here differed from
previous CDF&G surveys in that more data were
taken than were actually needed for the estimate
so that departures from model assumptions could
be examined. The additional data enabled simula-
tion of the sampling procedure to estimate bias and
variances, and allowed us to determine the sources
of failure of assumptions. We were also able to
develop estimates from which some sources of bias
had been removed.
METHODS
The study was conducted on a chinook salmon
spawning area of a small northern California
stream, Bogus Creek (Fig. 1). The stream was
sampled over a 6.5-mi reach from a counting weir
upstream to Bogus School road. Sampling was
begun on 15 September 1981, at the very beginning
of the spawning run, and discontinued on 12 Novem-
ber 1981, by which time very little spawning activ-
ity was apparent. The stream was sampled weekly
during that period; sampling took 2 d during the
peak of the run, with one half of the stream being
sampled per day. The stream was sampled by two
people walking upstream and capturing with a gaff
any carcasses seen. Data on each capture were
described as follows:
Place of capture: Edge top, edge bottom, middle
top, middle bottom, snagged, dry or buried.
Size: Small (<65 cm), medium minus (65-69 cm),
Klamath River
Figure 1— Study area in north-
ern California.
262
SYKES and BOTSFORD: CHINOOK SALMON SPAWNING ESCAPEMENT
medium (70-80 cm), medium plus (81-85 cm), or
large (>85 cm).
Sex: Male or female.
Condition: Alive, fresh (eyes clear), decayed
minus (eyes cloudy, flesh firm), decayed (flesh
soft), decayed plus (flesh very soft), or skeleton
(flesh falling off).
Carcasses were individually tagged with fingerling
fish tags which were attached around the maxillary
bone. Data on place of release for each released car-
cass were recorded as follows:
Pool, pool/riffle, or riffle.
The presence or absence of obstructions which
would trap and remove a carcass.
The speed of water flow.
Thus movements of individual carcasses and their
condition, both of which might affect catchability
and survival, could be examined on an individual
basis. During the sampling process about one-third
of the unmarked, captured carcasses was random-
ly removed from the population by cutting the fish
in two. This was done because of limited time
available for recording data. These individuals were
considered "trap mortalities" (i.e., they are counted
in the sample size but not in the total releases for
that time period). Because the mark-recapture
methods used allow for capture loss, removal of
these fish has no effect on errors other than lower-
ing sample sizes.
Two existing methods, those of Jolly and Seber
(Seber 1982) and Manly and Parr (1968), and a third,
a modified Jolly-Seber method, were used to es-
timate population sizes, recruitment, survival, and
their standard errors (when expressions were
available). The corrected estimates of Seber (1982)
were used for the Jolly-Seber method. When sur-
vival was estimated as greater than unity, or immi-
gration as <0.0, those values were replaced with 1.0
and 0.0 respectively in subsequent calculations. In
the third method, standard Jolly-Seber estimates
were calculated after modifying the mark-recapture
data so that all decayed (decayed minus or worse)
carcasses (marked and unmarked) were assumed to
have been destroyed upon capture. This method
simulates the way CDF&G has traditionally col-
lected data.
After these estimates had been calculated, the
estimated escapement, E, was calculated as the
number present at the first sample period, plus the
number of individuals immigrating during each
subsequent period.
E = nx + 02 - R, * *,)/(*!) b)
+ D2 + D3 + D4 (1)
where nx = the number sampled at the first sam-
ple time,
Rx = the number tagged and released at
the first sample time,
N2 = the estimated population size at sam-
ple time two,
A = Mn5,
<t>i = the survival rate from i to i + 1, and
B{ = the estimated number of carcasses
still present at the sample time i +
1 which immigrated between i and i
+ 1.
In this expression the initial number present at time
period 1 is conservatively taken to be the sample
size at time period 1 {n{). The number immigrating
during the subsequent period is taken to be the
estimated population at time period 2, minus the
number of tagged fish which had been accounted for
in the first sample. Immigration during the next two
periods are standard estimates. Each immigration
rate is divided by the square root of the survival rate
(the survival rate for half the sample period), to ac-
count for fish that enter the population and leave
it between sampling periods, and thus are never
sampled (Stauffer 1970).
Estimates of immigration during the last time
period are not computed in standard multiple mark-
recapture experiments; however, this immigration
(.B4 here) can be estimated from the standard Jolly-
Seber expression (Seber 1982), if the final numbers
(Nb) and survival rate (<t>4) can be estimated. If sur-
vival varies little from sample to sample, <t>4 can be
estimated by assuming that mortality is equal to the
value estimated over an earlier period in this study.
Since survival varied little between sampling periods
and the x2 test of Seber (1982) failed to reject the
null hypothesis of constant survival (x2 = 0.4648,
df = 2), we estimated survival from period 3 to
period 4 as the average of 4>1; 4>2> ana" ^3- To esti-
mate iV5, we estimated the capture probability at
sample period 5 (P5) as the ratio of the number of
carcasses released at sample 4 and recaptured at
sample 5 (r4) to the number released at sample 4
(R4) times survival to sample 5 (4>4),
P5 = rJ(R, * 4>4).
(2)
We then estimated the population size at sample 5
263
FISHERY BULLETIN: VOL. 84, NO. 2
(N5) as the sample size (n5) divided by the capture
probability (P5).
Standard errors and 95% confidence limits for the
third method were obtained by simulation. The sam-
pling process was simulated by generating a popula-
tion of carcasses based on population size estimates
from the third method. We then sampled the popula-
tion by comparing a uniformly distributed random
number with the appropriate probability of capture
[see Sykes (1982) for a more detailed description of
the simulation process, and a Fortran program].
From each simulation we calculated Jolly-Seber
estimates of survival, immigration, population sizes,
and their standard errors. An estimate of E was
then calculated as above. This simulation process
was repeated 1,000 times. In addition to calculating
the average and standard error of each of these
estimates, 95% confidence limits were calculated by
Buckland's (1980) method 1. To obtain 95% con-
fidence limits by this method, one adds the dif-
ference between the average of the 25th and 26th
lowest estimates (out of 1,000) and the average value
to the field estimate to obtain the upper bound and
subtracts the difference between the average of the
25th and 26th highest estimates and the average
value to obtain the lower bound.
All three methods assume that all individuals are
equally catchable. The methods based on the Jolly-
Seber model also assume that all individuals have
equal probabilities of survival. Since violation of
these assumptions could result in biased estimates,
we determined whether catchability and survival
varied and the effects of these on the estimates.
Several statistical tests can be used to check for
differential catchability and mortality, but only
among animals that are already marked. Two x2
tests, which compare expected frequencies of cap-
ture histories with actual frequencies (Seber 1982;
Jolly 1982) were calculated from the unmodified field
data. The test of Leslie and Carothers (Carothers
1971) was not performed because of the small
number of sampling periods. Since both tests yielded
expected values less than unity, pooled x2 values
were also calculated, using a conservative df value
of df = (number of pools - 1). For Seber's test, all
values less than unity were pooled; for Jolly's, each
value less than unity was pooled with the next
highest value.
Following Leslie et al. (1953, cited by Seber 1982)
we tested for homogeneity of catchability and sur-
vival by comparing estimates of population param-
eters obtained by different methods. These methods
differ in sensitivity to survival and capture heter-
ogeneity, hence the presence of heterogeneity
should cause differences in estimates of the same
parameter by the different methods. We tested the
unmodified field data by calculating the following
parameter estimates as per Leslie et al. (1953):
v{: the estimated number of new marks re-
leased at time i
4> . {: the estimated survival for the subpopulation
of marked carcasses, and
N.z: the number of marked carcasses.
and compared them with, respectively,
v{: the actual number of new marks released
at time i
fy: the Jolly-Seber estimate of survival, and
M^ the Jolly-Seber estimate of the number of
marked carcasses.
If differential catchability or survival, when present,
results in significant bias, these estimates will be
different.
Since only marked (and thus decayed) carcasses
are considered in the statistical tests discussed thus
far, these tests do not address the potential for age-
dependent catchability. To evaluate possible effects
of age-dependent catchabilities we "corrected" the
sample size n{ by reducing it to account for the fact
that fewer fresh (shiny, silver colored) carcasses
would have been captured if they had not been more
visible than decayed (dull brown colored) carcasses.
We then recalculated the escapement estimates
using the corrected sample size. We used two ratios
of average fresh to decayed catchability: 2.0 and 1.4.
Since visibility only differed among carcasses on the
stream bed, and only 30% of the captures were on
the stream bed, these values represented actual
ratios for carcasses on the stream bed of approx-
imately 6.7 and 4.7, respectively.
To evaluate the potential advantage of increasing
the efficiency of the third method by lowering the
sampling effort we examined the effect of lowered
sampling intensity on behavior of the three
estimators. Lower effort would most likely result
in less searching on the bottom of the stream for
carcasses. We therefore simulated lowered sampling
by generating new capture histories for each in-
dividual according to the following set of rules: 1)
If an individual was buried at a capture event, that
and all subsequent captures were ignored, 2) cap-
tures of decayed carcasses on the stream bed and
surface were ignored according to comparison of a
uniform random number with the appropriate
decrease in capture probability, and 3) the next cap-
264
SYKES and BOTSFORD: CHINOOK SALMON SPAWNING ESCAPEMENT
ture of an individual whose previous bottom capture
was ignored was considered to be a bottom capture,
as movement was probably the result of the previous
capture event.
RESULTS
Total escapement estimates for the three methods
and the weir count of fish moving into the spawn-
ing area are presented in Table 1. All three methods
result in escapement estimates that are close to the
weir count. The third method is the most efficient
Table 1.— Estimates of total escapement and the estimates used
to compute them for each of the three methods.
Jolly-Seber
Manly and Parr
Method 3
N2
999
1,076
1,063
SE A/2
95
128
139
N3
2,302
2,312
1,886
SEA/3
166
184
161
W4 .
1,845
1,853
1,452
SEA/4
67
72
93
B2
1,801
1,740
1,459
SES2
174
(1)
183
S3
150
136
371
SE03
128
(1)
179
02
0.7617
0.7789
0.7297
SE 4>2
0.353
(1)
0.439
*>3
0.7878
0.7940
0.8578
SE*3
0.0305
(1)
0.0548
"1
87
87
87
[A/2 - flt <t>
,]/<*>Ub
1,042
1,139
1,142
D2
2,062
1,970
1,708
03
169
151
401
D4
84
91
170
E
3,445
3,438
3,508
Weir count:
3,642
'Estimate of these standard errors are not available.
in the sense that it requires the least sampling effort.
For the third method, Jolly-Seber estimates and
associated estimated standard errors, computed
from the survey data along with the average value,
standard errors, and 95% confidence limits obtained
from simulation, are presented in Table 2. Esti-
mated standard errors and simulated standard
errors are in close agreement, except that the distri-
bution of estimates around the mean value is clear-
ly asymmetrical. Since they are based on simulation
of the actual process rather than approximate
analytical expressions, confidence limits obtained
from simulation are presumably more realistic than
those estimated by the methods of Jolly and Seber.
The sum of the estimated escapement by time
i + 2 is plotted with the sum of the weir count at
time i in Figure 2. Since the numbers of fish which
migrated through the weir correlates well with the
estimated number of fish that died 2 wk later, most
salmon probably spawned and died within 2 wk of
having entered the stream. Since the estimate of
immigration during the last sampling interval seems
to fit the known number of fish immigrating, the
assumption of constant survival seems to be a good
one. It is clear that our criteria for stopping sam-
pling when most spawning activity had ceased
resulted in an estimate of the complete run. Sam-
pling for another week would have removed the
need to make any assumptions in estimating B4,
but since this value will always be small in relation
to the total escapement, the increase in accuracy
does not seem worth the additional effort.
Data regarding the condition of carcasses at the
time of capture reflect a declining trend in catch-
Table 2.— Estimates of escapement (E), population size (W), immigration (S), survival
(O), and associated standard errors obtained from a Jolly-Seber analysis of data for
method three. Also shown are the computed mean, standard error, and 95% con-
fidence intervals obtained by simulation.
Simulation value
Upper
Lower
Field estimate
Mean
SE
95% C.I.
95% C.I.
A?2
1,063
1,041
145
+ 222
-344
SE N2
139
138
43
+ 66
-100
N3 .
1,886
1,889
166
+ 289
-360
SEA/3
161
165
28
+ 46
-62
N4
1,452
1,458
94
+ 167
-199
SEA/4
93
94
19
+ 33
-43
*2
0.7297
0.7327
0.0459
+ 0.0892
-0.0929
SE<D2
0.0439
0.0447
0.0021
+ 0.0039
-0.0046
•b
0.8578
0.8559
0.0551
+ 0.1003
-0.1127
SE*3
0.0548
0.0554
0.0090
+ 0.0145
- 0.0205
*2
1,459
1,446
193
+ 360
-415
SES2
183
189
29
+ 46
-68
S3
371
377
143
+ 307
-252
SE63
179
143
22
+ 36
-53
E
3,508
3,503
100
+ 186
+ 192
265
FISHERY BULLETIN: VOL. 84, NO. 2
4000 r
3500
3000 -
2500
2000 -
1600 -
1000 -
600 -
Figure 2.— Total numbers offish immigrating
as of week i by the weir count and total num-
bers of fish estimated by method three to have
died as of week i + 2.
ability and/or survival with conditon among
"marked" (and thus decayed) animals (Fig. 3). For
each week, smaller and more decayed carcasses ap-
pear to have lower recapture rates. (Note that since
this figure represents catchability at and after the
earliest time of recapture, these data do not reflect
catchabilities of fresh fish. Also, recapture rates for
week 3 are higher than those for week 4 because
there is one more opportunity for recapture.) These
low recapture rates can be the result of either lower
survival or lower catchability of smaller and more
decayed carcasses. The effects of these differences
in catchability on absolute numbers of recaptures
would be small because of the small number of car-
casses in the lower capture probability categories.
Note also in Figure 3 that recapture rates of fresh
carcasses vary less with size than decayed carcasses.
The expected and actual values for the tests for
differential catchability and mortality, the contribu-
tion of each difference to the x2 value, and the nor-
mal and pooled x2 values are presented in Tables 3
(Seber 1982) and 4 (Jolly 1982), respectively. Al-
though the fit between expected and observed
values appears to be quite good, the total differences
are statistically significant, hence catchability is not
strictly homogeneous.
The comparison of estimated and actual param-
eters as suggested by Leslie et al. (1953, cited by
08
0 6 _
I
u
0)
tr
0 2 -
00
Small
Medium -
Medium
Medium*
Large
fresh decayed
(AL.F.D-I (D)
very decayed
ID'.SK)
fresh decayed
(AL.F.D-) (D)
very decayed
(D*.SK)
Week 3
Week 4
Figure 3.— Fraction of marked fish recaptured by size, condition,
and week of release. Circled data points have sample sizes of
numbers of fish recaptured <10. Where <5 fish were released, that
point was not plotted. Note that all fish are decayed upon recap-
ture. The "fresh" category here includes alive, fresh and decayed
minus; the "decayed" category includes decayed and the "very
decayed" category includes decayed plus and skeleton.
Seber 1982) is presented in Table 5. The close agree-
ment between both sets of estimates indicates any
266
SYKES and BOTSFORD: CHINOOK SALMON SPAWNING ESCAPEMENT
Table 3.— Expected [E(bJ] and actual (bw) numbers of individuals with the specific
capture history w and the contribution of the difference between these values to the
X2 test of Seber (1982). The listed capture histories indicate the fish was caught only
at those times.
w
E(K)
K
[E(bw) - bw]2IE{bw)
2
120.22
116
0.1480
3
247.59
248
0.0007
4
589.01
588
0.0017
1,2
17.78
22
1 .0000
1,3
2.37
2
0.0585
1,4
4.56
7
1.3121
1,5
0.30
2
9.4810
2,3
34.88
36
0.0362
2,4
66.97
68
0.0160
2,5
4.46
8
2.8045
3,4
359.38
355
0.0535
3,5
23.95
19
1 .0225
4,5
150.07
153
0.0572
1,2,3
5.16
4
0.2603
1,2,4
9.91
9
0.0827
1,2,5
0.66
0
0.6601
1,3,4
3.44
2
0.6052
1,3,5
0.20
0
0.2295
1,4,5
1.16
0
1.1606
2,3,4
50.62
58
1 .0749
2,3,5
3.37
5
0.7843
2,4,5
17.06
10
2.9266
3,4,5
91.56
102
1.1894
1,2,3,4
7.49
5
0.8267
1,2,3,5
0.50
0
0.4490
1,2,4,5
2.52
4
0.8636
1,3,4,5
0.88
0
0.8774
2,3,4,5
12.90
10
0.6511
1,2,3,4,5
1.91
2
0.0045
X2 = 28.68 df = 14
a = 0.025
Pooled
X2 = 17.06 df = 10
a = 0.10
Table 4.— Expected and actual numbers of individuals caught at
sample /' and / (m.«), regardless of their capture history before / and
after/, and the contribution of the difference between these values
to the x2 test for equal catchability and survival of Jolly (1982).
',/
E(m
m
[Efrn.g) - m.HflE(m.$
1,3
6.95
4
1.2510
2,3
117.05
120
0.0743
1,4
5.74
7
0.2752
2,4
96.74
91
0.3410
3,4
529.51
534
0.0380
1,5
0.31
2
9.2562
2,5
5.20
8
1 .5064
3,5
28.49
24
0.7066
X2 = 13.44
df = 3
a = 0.005
Pooled
X2 = 6.34
df = 2
a = 0.05
differential catchability or survival that does exist
(as indicated by x2 tests and differential recapture
rates) does not significantly bias resultant estimates.
Values of E computed from data "corrected" for
age-dependent catchability are presented in Table
6. Again, it appears that if age-dependent catch-
ability is present, it has little effect on the estimates.
Also, that our estimates correlate well with the weir
count estimates, whereas "corrected" estimates are
Table 5.— Estimates of the number of marks released (v,), survival
($;), and the marked population size {n) for the standard Jolly-
Seber method and the same estimates (v/t O.,, N.t, respectively)
for the test for equal catchability and survival of Leslie et al. (1 953,
cited by Seber 1982).
Sample
SE V;
*,
<t>
M;
N
1
84
—
—
0.7995
—
67
—
2
311
—
—
0.7617
—
288
319
3
724
680
44
0.7878
0.7969
797
796
4
741
756
214
—
—
1,201
1,234
5
—
—
—
—
—
—
—
far too low, indicates that this bias was probably not
present in our sampling process. Thus biases en-
countered here are insignificant, both in relation to
possible imprecision in estimating the percent run
and area covererd, and the estimated standard
errors.
Estimates computed to evaluate the effects of
lowering sampling intensity are shown in Table 7.
Simulations are listed according to the percent of
top and the percent of bottom captures ignored for
that simulation. The estimates obtained by the third
267
FISHERY BULLETIN: VOL. 84, NO. 2
Table 6.— Escapement estimates obtained by correcting for differential
catchability of fresh and decayed carcasses for three methods of estimating
escapement. For each correction, the ratio of the average fresh to decayed
catchabilities that was assumed to obtain the corrected estimate is given.
Assumed fresh/decayed
Catchabilities
Corrected escapement
Jolly-Seber Manly and Parr Method 3
Original estimate
3,445
3,438
3,508
1.4/1.0
3,446
3,471
3,274
2.0/1.0
3,321
3,319
3,262
Table 7.— Escapement estimates obtained by simulation of reduced sampling effort
for three methods of estimating escapement. For each simulation the fraction of
decayed top carcass captures and the fraction of decayed bottom carcass captures
ignored is given.
Fraction of decayed
Carcass captures ignored
Escapement estimate
Top Bottom
Jolly-Seber
Manly and Parr
Method 3
Original estimate
3,445
3,438
3,508
0.0 0.4
3,740
3,765
3,676
0.0 1.0
3,944
4,058
3,777
0.2 0.4
3,890
3,917
3,977
0.4 0.6
4,844
4,934
4,364
method are less biased than those obtained by the
other two methods.
DISCUSSION
The estimates of total immigration are all remark-
ably close to the weir count. This accuracy is even
more remarkable in light of the fact that CDF&G
has traditionally used a correction factor of 0.95 to
account for an estimated 5% of the spawning
grounds that is not sampled on Bogus Creek. Inclu-
sion of this factor brings all of the estimates to
within 1.4% of the weir count. Since the third
method provides a high degree of precision (Table
2) at much less sampling cost, it is preferable over
the other two methods. We can compare the preci-
sion of the third method with the Jolly-Seber and
Manly and Parr methods by comparing the standard
error estimates that are available for those two
methods (Table 1). The Jolly-Seber method is more
precise in estimates of AT, B, and <t>. This is expected,
since both the Manly and Parr method and the third
method use fewer individuals in estimates than the
Jolly-Seber method does. However, the precision of
the third method is more than adequate: 95% con-
fidence intervals are +5.3% and -5.5% of the
escapement estimate.
The detected violations of assumptions, age-
dependent catchability and heterogeneity of capture
probabilities and survival, are those that would be
expected on the basis of physical considerations.
Survival of carcasses is a function of two processes:
fresh carcasses being removed by carnivores, and
old carcasses decaying and becoming buried in the
stream bed. Rates of disappearance could thus be
affected by condition, and therefore age and size,
of carcasses. Older carcasses and smaller carcasses,
which decay more quickly and are buried more easily
than larger carcasses, would be expected to have
lower survival rates.
Catchability is a function of both visibility and loca-
tion, both of which would be expected to vary with
condition and size of carcasses. This causes two dif-
ferent types of problems: age-dependent catchability
and size-dependent catchability. Shiny, fresh car-
casses were much more visible on the bottom of the
stream than the brown, decayed carcasses. Car-
casses on the stream surface were in general visi-
ble regardless of their condition. Since carcasses lost
their high visibility in about a week, no marked car-
casses will be in this high visibility category, and un-
marked carcasses will on the average be more catch-
able than marked carcasses. This can be thought of
as age-dependent catchability. Size-dependent catch-
ability stems from the fact that decayed individuals
that were large were more visible than those that
were small. This can be viewed as capture heter-
ogeneity. Since fresh fish were high visible regard-
less of their size, this heterogeneity existed only
among decayed individuals. Based on these con-
siderations we would expect catchability to vary
with age and size according to Figure 4.
268
SYKES and BOTSFORD: CHINOOK SALMON SPAWNING ESCAPEMENT
While both Jolly's (1982) and Seber's (1982) tests
indicate differential catchability and/or mortality are
present, the issue of real importance is the amount
of any resulting bias. Manly (1970) concluded that
if age-specific mortality is present in a sampled
population, Manly and Parr (1968) estimates should
fare better than those of Jolly and Seber (Seber
1982). Both methods, however, are biased for the
case in which mortality increases with age; in fact,
Manly's (1970) estimates of bias for additions (B) are
greater for Manly and Parr estimates than for Jolly-
Seber estimates for those simulations with param-
eters closest to our population. Survival, population
size, and catchability estimates were negatively bi-
ased by only 1 or 2%. Seber (1982) pointed out that
Jolly-Seber estimates should be relatively unbiased
even with differential mortality if mark status and
mortality were not correlated. Both estimators,
then, should have relatively unbiased estimates of
survival and catchability for "marked" animals. A
positive bias in estimates of immigration, B, (and
consequently in E) would arise primarily from apply-
ing mortality of marked animals to the entire
population, when marked animals are in general
older, and thus have lower survival than unmarked
animals.
The age-dependent catchability detected in this
study would be expected to result in a positive bias
in the estimate of total escapement, E. Because each
capture sample includes fresh, recently immigrated
individuals, and recapture samples include older,
decayed individuals, we expect N to be overesti-
mated (i.e., nIN > m/M in Jolly-Seber and pN < n
in Manly and Parr), which results in estimates of
B and E being positively biased also. Since bias from
age-dependent catchability in N decreases as M ap-
frash
decayed
Age
Figure 4.— Expected changes in capture prob-
abilities with age at different sizes.
proaches N, and removing carcasses after capture
in the third method decreases the ratio of marked
to total carcasses, we would expect the third esti-
mator to be more biased by age-dependent catch-
ability problems than the first two methods.
However, the simulations of lower sampling in-
tensity, which would exacerbate the effects of age-
dependent catchability, show that the estimate
obtained by the third method is more robust with
regard to lowered sampling intensity. This unex-
pected result is probably due to compensating
effects which decrease bias in E. The two most im-
portant components of E are the second ((N2 - Ri
Oi)/$i'5) and third (D2). In the standard estimates
these values both increase with increases in the
number of captures ignored. In the third method,
however, the second component increases, but the
third decreases. This is because as catchability
declines, fewer marks are captured and "removed",
hence more carcasses are available for later capture.
This is not the case in the first two methods because
marked carcasses are not removed at capture. Since
in the third method the composition of M and N is
relatively unchanged at the second sample period,
but at the third sample period, M increases relative
to N (because of the increase in the number of
decayed marks present), the estimate of population
size at the third sample period will be less biased
than the estimate for the second sample period. This
results in a negative bias in the estimated immigra-
tion from time period two to three. This compensa-
tion makes the third method more robust with
respect to age-dependent catchability problems than
the other two methods. Bias in the estimates is not
severe until large numbers of capture events are ig-
nored (Table 7). While all three methods produce
accurate estimates, even when lowered sampling
exacerbates differential catchability problems, the
magnitude of the bias relative to standard errors can
be substantial. For this reason, samples must be
carefully taken if estimates from different streams
or different years (which will have different biases
because of different conditions) are to be compared
statistically.
Heterogeneity of capture probabilities affects
Jolly-Seber and Manly and Parr estimates in the
same manner. Since in the Jolly-Seber method the
individuals marked and released at sample i, Rit
are on the average younger than the individuals
marked and released prior to sample i, M{ is a low
estimate (i.e., rlR > zl(M - m), or M > (Rzlr) + m).
This decreases the positive bias in N which is caused
by age-dependent catchability. Since bias in M in-
creases as more individuals are marked, we expect
269
estimates of M from the third method to be less bi-
ased than those from the first two.
Usually, capture heterogeneity leads to the more
catchable animals joining the marked population,
and we expect marked animals to be more catchable
than unmarked animals. Capture heterogeneity,
however, is only prevalent among decayed in-
dividuals who are all less catchable than fresh, un-
marked individuals. Thus, capture heterogeneity, by
placing the more catchable decayed individuals in
the marked population, results in the capture prob-
ability of marked animals being closer to the cap-
ture probability of unmarked animals. This reduces
the negative bias in population size (N), immigra-
tion (B), and escapement (E) estimates, which was
caused by age-dependent catchability. Again, the
third method, by removing decayed individuals and
decreasing the fraction of the population which is
decayed, will not be affected by capture heteroge-
neity as strongly as the other two methods.
Manly and Parr estimators will have the same
ameliorating affects because of capture heteroge-
neity as their Jolly- Seber counterparts. Since the
estimate of catchability, p, should be accurate for
the more catchable animals, estimated survival
should be accurate for that group. Bias would result
from correlations between catchability and survival.
Also, since p is estimated for marked (and thus
decayed) individuals, using the more catchable
decayed individuals to estimate p brings the
estimated catchability closer to the actual catch-
ability of the unmarked individuals. Again, this
reduces the bias in N, B, and E which is caused by
age-dependent catchability.
There are other approaches to estimating param-
eters from populations with age-dependent survival
and capture rates. By placing carcasses in two readi-
ly identifiable age classes, fresh (and thus <1 wk old)
or decayed (and thus older than 1 wk), Pollock's
(1981) modified Jolly-Seber analysis of the data could
have been made. Since this method requires recap-
tures of decayed individuals, it could not be used to
analyze data from previous surveys, and it would
require more sampling effort in future surveys than
the method 3 estimate. If different age classes have
sufficiently different capture or survival rates, then
this method will provide more accurate estimates.
If not, then it will yield the same estimate as the
third method, but would have higher variances, as
more parameters are estimated.
FISHERY BULLETIN: VOL. 84, NO. 2
ACKNOWLEDGMENTS
We would like to thank L. B. Boydston of the
California Department of Fish and Game for making
us aware of this problem, for many helpful discus-
sions, and for assisting in data collection. S. Sykes
was supported by the California Department of Fish
and Game during the sampling. We are grateful for
the comments by K. Pollock, T. Schoener, and N.
Matloff on an earlier version of this manuscript. We
would also like to thank Ivan Paulsen for assistance
in data collection.
LITERATURE CITED
BUCKLAND, S. T.
1980. A modified analysis of the Jolly-Seber capture-recapture
model. Biometrics 36:419-435.
Carothers, A. D.
1971. An examination and extension of Leslie's test of equal
catchability. Biometrics 27:615-630.
Darroch, J. N.
196 1 . The two-sample capture-recapture census when tagging
and sampling are stratified. Biometrika 48:241-260.
Jolly, G. M.
1982. Mark-recapture models with parameters constant in
time Biometrics 38:301-321.
Manly, B. F. J.
1970. A simulation study of animal population estimation
using the capture-recapture method. J. Appl. Ecol. 7:13-39.
Manly, B. F. J., and M. J. Parr.
1968. A new method of estimating population size, survivor-
ship, and birth rate from capture-recapture data Trans. Soc
Br. Entomol. 18:81-89.
Parker, R. R.
1968. Marine mortality schedules of pink salmon of the Bella
Coola River, central British Columbia. Can. J. Fish. Res.
Board 25:757-794.
Pollock, K. H.
1981. Capture-recapture models allowing for age-dependent
survival and capture rates. Biometrics 37:521-529.
Schaefer, M. B.
1951. Estimation of the size of animal populations by mark-
ing experiments. U.S. Fish Wildl. Serv., Fish. Bull. 52:
191-203.
Seber, G. A. F.
1982. The estimation of animal abundance and related param-
eters. MacMillan Publishing Co., Inc, N.Y. 654 p.
Stauffer, G.
1970. Estimates of population parameters of the 1965 and
1966 adult Chinook salmon runs in the Green-Duwamish
River. M.S. Thesis, Univ. Washington, Seattle, 155 p.
Sykes, S. D.
1982. Multiple mark-recapture estimators of salmon spawn-
ing runs sizes. M.S. Thesis, Univ. California, Davis, 64 p.
270
THE DISTRIBUTION OF THE HUMPBACK WHALE,
MEGAPTERA NOVAEANGLIAE, ON GEORGES BANK AND IN
THE GULF OF MAINE IN RELATION TO DENSITIES OF
THE SAND EEL, AMMODYTES AMERICANUS
P. Michael Payne,1 John R. Nicolas,2 Loretta O'Brien,2
and Kevin D. Powers1
ABSTRACT
The distribution of the humpback whale, Megaptera novaeangliae, (based on shipboard sighting data) is
significantly correlated (r = 0.81, df = 13) with the number of sand eel, Ammodytes americanus, per
standardized tow (based on NMFS/NEFC groundfish surveys) by strata within the Gulf of Maine A
demonstrated increase in the number of humpback whale sightings in the southwest Gulf of Maine since
1978 concurrent with an increase in the number of sand eel in the same area supports the hypothesis
that within the Gulf of Maine the present distribution of humpback whales is due to the distribution of
their apparent principal prey, the sand eel. A similar correlation between humpback whale sightings and
sand eel abundance on Georges Bank was not significant (r = 0.24, df = 18) despite dense patches of
sand eel in that region. Therefore, within the combined Gulf of Maine-Georges Bank regions, factors other
than simply prey availability must influence the feeding distribution of the humpback whale We argue
that the bottom topography of the Gulf of Maine and the foraging behavior of the whales are critical
factors influencing their present feeding distribution.
In the northwest Atlantic, the major summer con-
centrations of humpback whales, Megaptera novae-
angliae, occur off the coasts of Newfoundland-
Labrador and off the coast of New England in the
Gulf of Maine which includes Georges Bank (Katona
et al. 1980; Whitehead et al. 1982). During this
period feeding is their principal activity. The major
winter concentrations in the western North Atlan-
tic occur along the Antillean Chain in the West
Indies, principally on Silver and Navidad Banks
which lie north of the Dominican Republic (Winn et
al. 1975; Balcomb and Nichols 1978; Whitehead and
Moore 1982). During this season conception and
calving are their primary activities; food does not
seem to be an important determinant of the hump-
backs in these areas (Whitehead and Moore 1982).
Humpbacks have been generally considered
coastal animals (Mackintosh 1965). However, their
migratory routes between regions of winter breed-
ing and summer feeding in the northwest Atlantic
(based on sighting data) occur in deeper, slope
waters off the continental shelf (Hain et al. 1981;
Kenney et al. 1981; Payne et al. 1984). Several possi-
ble offshore routes between winter and summer
grounds suggest reasonably distinct stocks (Katona
^anomet Bird Observatory, Marine Mammal and Seabird
Studies, Box 936, Manomet, MA 02345.
2Northeast Fisheries Center Woods Hole Laboratory, National
Marine Fisheries Service, NOAA, Woods Hole, MA 02543.
et al. 1980). Kenney et al. (1981) suggested that for
the Gulf of Maine stock, the Great South Channel
(Fig. 1) is the major exit-entry between the Gulf of
Maine feeding area and the deeper, offshore migra-
tion route.
Humpback whales have been described as general-
ists in their feeding habits (Mitchell 1974). The
reported prey of humpbacks in the Gulf of Maine
are Atlantic herring, Clupea harengus; Atlantic
mackerel, Scomber scombrus; pollock, Pollachius
virens; and the American sand eel, Ammodytes
americanus (Gaskin 1976; Katona et al. 1977;
Watkins and Schevill 1979; Kraus and Prescott
1981). In recent years, observations of feeding
humpbacks indicate that sand eels have become an
increasingly important prey item in the Gulf of
Maine (Overholtz and Nicolas 1979; Hain et al. 1982;
Mayo 1982).
Kenney et al. (1981) hypothesized that the ob-
served distribution of the Gulf of Maine humpback
stock was due to the distribution of sand eel, their
apparent principal prey species. However, the pres-
ent distribution of the humpback whale in the Gulf
of Maine and throughout the remaining shelf waters
of the northeastern United States is not so clearly
related to the distribution of sand eel as was sug-
gested. Although we recognize an important
predator-prey interaction between humpbacks and
sand eel, we hypothesize that behavior and bottom
Manuscript accepted July 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
271
FISHERY BULLETIN: VOL. 84, NO. 2
GOM = Gulf of Maine
GB=Georges Bank
Figure 1— The geographical areas and NMFS/NEFC bottom-trawl survey strata in the study area (upper) and
the combined strata into regions (lower) referred to throughout the text.
272
PAYNE ET AL.: DISTRIBUTION OF HUMPBACK WHALE
topography are also critical factors in the foraging
strategy of humpbacks, hence the present distribu-
tion of these whales. We base this hypothesis on
observed sightings of humpbacks throughout the
shelf waters of the northeastern United States in
relation to sand eel abundance, and on an apparent
shift in the center of feeding areas used by hump-
backs in the Gulf of Maine since the mid-1970's.
METHODS
The collection of fisheries data used in these
analyses was carried out by National Marine Fish-
eries Service/Northeast Fisheries Center (NMFS/
NEFC) scientists and technicians on domestic
research vessels during standardized spring bottom-
trawl surveys. These surveys measure trends in fin-
fish population abundance and have been used to
monitor changes in the size and composition of fin-
fish biomass (Clark and Brown 1977; Grosslein et
al. 1980).
Meyer et al. (1979) found that spring (March-May)
bottom-trawl surveys accurately reflect trends in
sand eel abundance. Therefore, the fisheries data
we examined were from these surveys, 1978-82. The
stratified mean catch per tow of sand eel was
calculated for each region and considered propor-
tional to the population size within each region. We
transformed the mean catch into logarithmic values;
then, using a two-way analysis of variance (F-
statistic), we compared sand eel population size by
region and year.
The survey area includes shelf waters from Cape
Hatteras north to Nova Scotia and has been spatially
stratified by the NMFS/NEFC, based principally on
depth and latitude (Grosslein 1969). Sampling sta-
tions are randomly assigned within a stratum and
the number of stations allocated to strata approx-
imately in proportion to the area of each stratum
(Grosslein 1969). In this study, individual stratum
have been combined into regions (Fig. 1), in a man-
ner consistent with NMFS/NEFC management
units. The two important regions emphasized are
the Gulf of Maine and Georges Bank.
Sightings of humpback whales were recorded by
observers from the Manomet Bird Observatory
(MBO) on NMFS/NEFC research vessels conducting
standardized surveys. Observations were recorded
continuously along the predetermined cruise path
between the sampling stations (following Payne et
al. (1984)) in 15-min periods where each period
represents a transect. Thus, the duration of each
observation period was constant, but the linear km
surveyed within each 15-min period depended upon
vessel speed. The location (latitude-longitude) of
each 15-min observation and the location and num-
ber of humpback whales observed were recorded
and assigned to appropriate regions to facilitate
direct comparisons between the observed number
of humpbacks per linear km (humpbacks/effort) and
potential prey densities.
Humpback whales are generally present in the
study area from spring through fall (March-Novem-
ber) and absent during the winter (CETAP 1982).
Therefore, sighting data and effort for winter
months were excluded from the analyses. We also
examined sighting data collected only during op-
timum sea conditions less than Beaufort (Kenney
et al. 1981) (<16 nmi/h). Difference between the
number of humpbacks/effort sighted by region and
year were also compared by a two-way analysis of
variance (F-statistic).
A coefficient of correlation (r) from the linear
regression between the stratified mean catch of sand
eel (log) and the number of humpbacks/effort was
used to determine whether concentrations of hump-
back whales co-occurred with patches of sand eel
within regions of the Gulf of Maine and Georges
Bank.
A P < 0.05 was considered statistically significant.
RESULTS
Distribution of Sand Eel
The stratified mean number of sand eel varied sig-
nificantly between regions on Georges Bank (F =
14.14, df = 3, 12) and in the Gulf of Maine (F =
16.90, df = 2, 8). On Georges Bank, sand eel were
very abundant on the shoals with catches ranging
from 1.117 sand eel/tow (log value) in 1978 to 2.846
(log value) in 1982 (Table 1). Sand eel were absent
from most tows along the northern and shelf edges.
Sand eel were also abundant in the southwest Gulf
of Maine ranging from 0.670 sand eel/tow (log value)
in 1978 to 2.422 in 1981 (Table 1). Sand eel were not
abundant in the deeper, central Gulf of Maine This
patchy distribution reflects a known preference of
the sand eel for sand-bottom substrates (Bigelow and
Schroeder 1953) characteristic of submarine banks
and shoals. No significant differences were found
between the stratified mean catch per tow (log value)
by year.
Distribution of Humpback Whales
Since 1978, the observed number of humpbacks/
effort in the Gulf of Maine has steadily increased
273
FISHERY BULLETIN: VOL. 84, NO. 2
Table 1.— Stratified mean number of sand eel per tow + SE (in
parentheses) and the number of sampling tows (lower number) by
region and year.
Region
1978 1979
1980
1981
1982
Georges Bank
shoals
northern edge
shelf edge
central bank
Gulf of Maine
central gulf
southern
southwest
1.117
(0.233)
15
0.000
9
0.100
(0.707)
15
0.941
(0.182)
21
0.000
64
0.000
9
0.670
(0.371)
20
1.200
(0.305)
30
0.256
(0.211)
16
0.000
2.752
(0.590)
15
0.000
8
0.000
1.850
(0.499)
15
0.747
(0.464)
8
0.000
2.846
(0.691)
15
0.000
8
0.000
14 14
0.410 0.236
(0.202) (0.132)
38 18
10 14
0.654 0034
(0.396) (0.341)
19 19
0.012
(0.012)
61
0.141
(0.101)
47
0.055
(0.545)
45
0.625 0.116
(0.422) (0.115)
12 6
1.286 1.240
(0.289) (0.384)
34 16
0.000
47
1.077 0.116
(0.617) (0.115)
6 6
2.422 0.860
(0.756) (0.318)
18 21
(Table 2). Over 90% of the humpbacks/effort ob-
served each year in the combined Georges Bank-Gulf
of Maine waters were seen in the Gulf of Maine. The
increased number of humpbacks/effort observed was
significantly different between regions in the Gulf
of Maine (F = 7.098, df = 2, 8). The greatest con-
centrations of humpbacks in the Gulf of Maine are
located in the southwest region (Table 2). Between
1978 and 1982, 82% of the total humpbacks/effort
in the Gulf of Maine were observed in the southwest
region. The importance of this region for feeding
humpbacks has been previously reported (Kenney
et al. 1981; Hain et al. 1982).
Although there were no significant differences
between the number of humpbacks/effort seen by
year (F = 0.824, df = 4, 12) or region (F = 0.609,
df = 3, 12) on Georges Bank, the number of hump-
backs/effort observed on the bank has steadily de-
clined since 1978. Sixty percent of the humpbacks/
effort observed on Georges Bank between 1978 and
1982 occurred during 1978 (Table 2).
We examined the apparent increase in the south-
west Gulf of Maine more thoroughly by dividing it
into two smaller components (Table 3), a southern
which extends from the Great South Channel north
along the outside of Cape Cod (NMFS/NEFC strata
23, 25, from Figure 1) and a northern which centers
on Stellwagen Bank (NMFS/NEFC strata 26, 27,
from Figure 1). The number of humpbacks/effort
observed within the southwest Gulf of Maine-north-
ern segment steadily increased by an order of mag-
nitude from 1.86 x 10 ~2 whales/effort in 1978 to
29.01 x 10"2 whales/effort in 1982. Therefore, the
observed increase in the number of humpbacks/
effort in the southwest Gulf of Maine since 1978 has
occurred primarily in the northern half of this region
(NMFS/NEFC strata 26, 27).
Table 2.— The number of humpback whales per linear km x 10 "2
(humpbacks/effort) seen during shipboard observations and the
total number of linear km surveyed (in parentheses) by region and
year.
Region
1978
1979
1980 1981
1982
Georges Bank
shoals
northern edge
shelf edge
central bank
Gulf of Maine
central gulf
southern
southwest
— 0.189 — — —
(480.9) (529.0) (190.0) (342.6) (744.5)
1 .500 — —
(200.0) (176.8) (66.5)
(230.0) (213.6) (115.6)
0.168 0.285 0.299
(593.6) (701.9) (334.4)
0.750
(933.1)
2.449
(489.8)
1.174
(681 .2)
0.119
(841.7)
0.828
(482.8)
2.817
(745.4)
(966.0)
(267.6)
7.679
(547.0)
(89.8)
(207.0)
(895.9)
0.855
(467.6)
0.393
(254.2)
11.172
(454.9)
(222.7)
0.225
(198.6)
0.116
(863.5)
(1,172.8)
1.662
(223.5)
6.814
(692.5)
-2
Table 3.— The number of humpback whales per linear km x 10
(humpbacks/effort) seen during shipboard observations and the
total number of linear km surveyed (in parentheses) within the par-
titioned southwest Gulf of Maine.
Region
1978
1979
1980
1981
1982
Northern 1.864 2.655 10.794 22.469 29.014
(strata 26, 27) (34.9) (263.6) (333.5) (252.6) (299.6)
Southern 0.556 3.113 2.811 1.987 3.308
(strata 23, 25) (359.3) (481.8) (213.5) (202.3) (392.9)
Correlation Between
Humpback Whale Distribution
and Sand Eel Abundance
A significant correlation (r = 0.81, df = 13) ex-
ists between the observed number of humpbacks/
effort and the log-mean number of sand eel/tow by
region within the Gulf of Maine (Fig. 2). This in-
dicates that within the Gulf of Maine the distribu-
tion of humpback whales do co-occur with dense
patches of sand eel in that region. The greatest den-
sities of sand eel in the Gulf of Maine and the
greatest observed numbers of humpbacks/effort
have both occurred in the southwest Gulf of Maine
since 1978. This supports the hypothesis by Kenney
et al. (1981) that within the Gulf of Maine, the
274
PAYNE ET AL.: DISTRIBUTION OF HUMPBACK WHALE
10.0
8.0-
6.0
O
Ul
m 4.0
HI
_l
<
I
o
<
en
Q.
D
I
2.0-
Georges Bank
y=0.20-0.08x
n=20
r---0.24
—i-
1.0 2.0
STRATIFIED MEAN SAND EEL PER TOW (LOG)
3.0
Figure 2— The regression and correlation coefficient (r) between
the stratified mean number of sand eel/tow (log value) and the
number of humpback whales/effort x 10 ~2 by region and year on
Georges Bank (closed circles) and in the Gulf of Maine (open cir-
cles).
observed distribution of the humpback whale was
due to the distribution of sand eel.
However, the correlation between the observed
number of humpbacks/effort and the log mean num-
ber of sand eel/tow by region on Georges Bank (Fig.
2) was not significant (r = 0.24, df = 18). The mean
number of sand eel/tow (log value) on Georges Bank
was greatest on the shallow shoals. Only one hump-
back whale was observed on the shoals between
1978 and 1982. Our data does not support any
co-occurrance between humpback whale distribution
and sand eel abundance on Georges Bank despite
dense patches of sand eel in that region.
DISCUSSION
Our data suggest that the distribution of hump-
back whales in the Gulf of Maine-Georges Bank
region is presently centered in the southwest Gulf
of Maine. This distribution is correlated with dense
concentrations of sand eel, a principal prey item,
which has dramatically increased throughout shelf
waters of the eastern United States including the
southwest Gulf of Maine since the mid-1970's (Meyer
et al. 1979; Sherman et al. 1981). This increase in
sand eel followed a decline of Atlantic herring stocks
from the mid-1960's to the mid-1970's (Anthony and
Waring 1980; Grosslein et al. 1980), and possible
replacement by sand eel of depleted fish stocks in
the northwest Atlantic (Sherman et al. 1981). The
correlations between the humpback distribution in
the Gulf of Maine and sand eel abundance supports
the theory by Kenney et al. (1981) that the present
distribution of the whales in that region is due to
the distribution of sand eel. A demonstrated shift
in the humpback distribution since the mid-1970's
from the upper Gulf of Maine-lower Bay of Fundy
southward into the southwest Gulf of Maine also
supports this theory.
A 10-yr summary of observations from Mt. Desert-
Rock, ME (MDR, Fig. 1) in the northern Gulf of
Maine shows a dramatic decrease in the number of
humpback sightings/observer hour since 1977 (Mul-
lane and Rivers 1982). The maximum number of
humpbacks observed in that summary occurred in
1975 (98 whale sightings, 0.123 humpbacks/observer
hour). Only 10 humpbacks were seen from 1978 to
1982, and the maximum number of humpbacks/ef-
fort since 1975 has been 0.005/observer hour in
1982. This decline in the number of humpbacks at
MDR coincides with the increased numbers of hump-
backs observed in the southwest Gulf of Maine.
Twelve of the 17 humpbacks photo-identified from
1975 to 1977 at MDR have subsequently been seen
in the southwest Gulf of Maine, principally on Stell-
wagen Bank. At least three of these whales have
been observed during three different years on Stell-
wagen Bank since they were first identified at MDR
(Mullane and Rivers 1982). In comparison, only one
whale identified at MDR has consistently returned
to the coastal waters of eastern Maine and New
Brunswick. Katona et al. (1977) also listed the Grand
Manan Banks, Briers Island-St. Mary's Bay, Nova
Scotia, and the lower Bay of Fundy as areas of
humpback congregations. However, humpbacks
were not common in the Bay of Fundy during 1981
and 1982 (Kraus and Prescott 1981, 1982).
Shifts in the distribution of humpbacks caused by
changes in the distribution and density of prey
species have been shown elsewhere (Lien and Merd-
soy 1979; Whitehead et al. 1980). We believe that
the correlations between humpbacks/effort and
mean sand eel catches in the southwest Gulf of
Maine, and the demonstrated decline of humpbacks
throughout the upper Gulf of Maine-lower Bay of
Fundy concurrent with an increase in the numbers
275
FISHERY BULLETIN: VOL. 84, NO. 2
of humpbacks in the southwest Gulf of Maine
reasonably explains the present distribution of
humpbacks within the Gulf of Maine. However, it
does not adequately explain the paucity of hump-
backs on Georges Bank (Table 2) and throughout the
remaining shelf waters of the northeastern United
States (Hain et al. 1981; Kenney et al. 1981; Payne
et al. 1984), areas where sand eel have also increased
since 1975. The nonsignificant correlation between
humpbacks/effort and the log-mean catches of sand
eel/tow on Georges Bank suggests that factors other
than simply food concentrations, perhaps behavioral
or environmental, may influence the humpback's
feeding strategy and location.
Sutcliffe and Brodie (1977) reported that hump-
backs are led into ecological or oceanographic bound-
aries (i.e., isopleths or shelf-edges) and feed in
patchy areas of dense prey aggregations along these
boundaries. A change in depth on the shelf is often
accompanied by a concentration of near-surface zoo-
plankton; in general, the more abrupt the change,
the greater the concentration (Sutcliffe and Brodie
1977). Concentrations are especially noticeable
along the edge of banks where the availability of
prey is most affected (Jaansgard 1974). Reay (1970)
found that sand eel concentrations are greatest on
the edges of sandy banks where currents and prey
(zooplankton) are optimum; thus the whales, in seek-
ing the highest concentrations of prey, feed most
frequently along the edges of the banks (Sutcliffe
and Brodie 1977; Brodie et al. 1978). Observations
of feeding humpbacks in the Gulf of Maine have oc-
curred primarily along the edge of submarine banks
or canyons (Hain et al. 1982; CETAP 1982).
If bottom topography influences feeding behavior
of humpbacks (by concentrating prey), then the
paucity of humpbacks on Georges Banks and
throughout the mid-Atlantic Bight regions becomes
more understandable. The floor of the broad mid-
Atlantic Bight is gently sloping continental shelf
with no relief until it steepens sharply at the shelf
break, at about 200 m depth, to form the continen-
tal slope. Since the feeding behaviors for humpbacks
described by Hain et al. (1982) occur principally over
a shelf-floor with rugged relief, the strategies used
by humpbacks seem most efficient in these waters.
This also explains the present lack of sightings in
the mid-Atlantic shelf waters and the offshore
migration route between calving and feeding areas.
It seems energetically advantageous for the hump-
back, a relatively slow-moving whale, to migrate
over deep water with little apparent feeding, then
feed on the densely concentrated prey along the bot-
tom profiles of the Gulf of Maine.
We maintain that humpbacks are merely utilizing
the first concentrations of prey available to them
in spring, after they reach shelf-waters from their
offshore migration route between winter-calving
and summer-feeding grounds. The humpbacks seem
to use the Great South Channel as an entry-exit in-
to the Gulf of Maine (as hypothesized by Kenney et
al. (1981)), and follow the bottom profile northward,
using this profile to their feeding advantage until
they reach the dense concentrations of sand eel
available within the southwest Gulf of Maine. The
quantities of sand eel available to humpbacks at this
location have allowed the whales to remain through-
out the feeding season; therefore, the recent paucity
of sightings in the northern Gulf of Maine.
ACKNOWLEDGMENTS
The authors wish to thank T. R. Azarovitz, S. K.
Katona, P. Major, M. P. Pennington, M. P. Sissen-
wine, G. Waring, H. Whitehead, and anonymous
reviewers for criticizing previous drafts of this
manuscript. The study was funded by the National
Marine Fisheries Service, Northeast Fisheries
Center, Woods Hole, MA.
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277
SEABIRDS NEAR AN OREGON ESTUARINE SALMON HATCHERY IN
1982 AND DURING THE 1983 EL NINO
Range D. Bayer1
ABSTRACT
In the summer of 1982, 14.4 million salmon, Oncorhynchus sp., smolts were released at the Yaquina
Estuary, OR; and in the summer of 1983, 12.8 million salmon smolts were released. Within hours after
release, fish-eating seabirds aggregated at the estuary mouth. In 1982, the number of no seabirds was
significantly correlated with the number of days since a release. In 1983, however, numbers of common
murres, Uria aalge; gulls, Larus sp.; and brown pelicans, Pelecanus occidentalis, were significantly in-
versely correlated with the date of a release, and the number of cormorants, Phalacrocorax sp., was
significantly more abundant the second day after a release. In contrast, numbers of Caspian terns, Sterna
caspia, and pigeon guillemots, Cepphus columba, showed no relationship with releases in 1983.
There were significantly more cormorants and marbled murrelets, Brachyramphus marmoratus,
in 1983 than in 1982. There were also significantly more murres in 1983 than in 1982 before 1 August,
but fewer afterwards. Gull and brown pelican numbers were about the same between years, but significant-
ly fewer pigeon guillemots were present in 1983 than in 1982.
Seabirds have been estimated to consume 29% of
the pelagic fish production within 45 km of a British
seabird colony (Furness 1984b), and several simula-
tion models for various geographical areas indicate
that 20-30% of the annual pelagic fish production
may be preyed upon by seabirds (Furness 1984a).
Since the mortality of salmon, Oncorhynchus sp.,
smolts as a result of predation and environmental
factors is greater shortly after they first enter the
ocean than after they move offshore (Parker 1962,
1968), the impact of seabird predation on salmon
smolts just released along a coast could also be
significant.
El Nino is the intrusion of anomalously warm
water off the coast of Peru and Ecuador (Barber and
Chavez 1983); an El Nino of varying intensity oc-
curs on the average of every 3-5 yr (Quinn et al.
1978; Duffy 1983a). Along the Oregon coast, warm-
water conditions concurrent with an El Nino appear
much more rarely, and in the last century have oc-
curred only in 1983, 1957-1958, and perhaps in 1941
(Huyer 1983; Reed 1983). The impact of seabirds on
hatchery-released salmon smolts would be expected
to be greater in years of anomalously warm water
associated with El Nino, when natural prey for sea-
birds become rare and seabirds starve or have low
nesting success (Boersma 1978; Duffy 1983a, b;
Ainley 1983; Schreiber and Schreiber 1984).
'Oregon Aqua-Foods, Inc., 2000 Marine Science Drive, New-
port, OR 97365; present address: P.O. Box 1467, Newport, OR
97365.
Here, I correlate bird numbers with salmon smolt
releases at Yaquina Estuary, OR, and examine
variation in bird numbers between the summer of
1982 and the summer of 1983, when warm water
associated with an El Nino was present.
STUDY AREA AND METHODS
Yaquina Estuary (Fig. 1) is located on the mid-
Oregon coast and is a drowned river valley. It has
an intertidal and submerged area of 15.8 km2
(Oregon State Land Board 1973). During this study,
all releases were from the site designated as OAF
in Figure 1.
The most abundant seabird nesting nearby was
the common murre, Uria aalge, but western gulls,
Larus occidentalis; Brandt's cormorants, Phalacro-
corax penicillatus; pelagic cormorants, P. pelagicus;
and pigeon guillemots, Cepphus columba, also nested
there (Table 1; Pitman et al. in press). Within Ya-
Table 1.— Distance of nesting birds from the mouth of Yaquina
Estuary in 1979 (calculated from Pitman et al. in press).
Cumulative number of nesting birds
<7 km <20 km <25 km <45 km <50 km
common murres1 22,800 26,800 26,800
western gulls 398 528 536
cormorants 418 653 1,581
pigeon guillemots 45 191 201
26,800 322,000
541 1,231
1,727 3,041
206 220
'Includes all breeding and nonbreeding adults at colony.
^Estimated for 1983 (USFWS, aerial survey; pers. obs.).
includes 1983 as well as 1979 estimates.
Manuscript accepted July 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
279
aS'T-f- 2-*^
FISHERY BULLETIN: VOL. 84, NO. 2
x =JETTY
OBSERVAT ION
POINT
REGIONS
0A SC
SB (D D
o
33 KM
TO HEAD
OF TIDE
I 2 4"^ 0 2
Figure 1.— Yaquina Estuary study regions. OAF indicates site of
smolt releases.
quina Estuary, <30 pairs of western gulls (Bayer
1983) and an undetermined number of pigeon
guillemots also nested in association with manmade
structures. The typical nesting phenology of these
birds at Yaquina Head (which is about 6.5 km north
of Yaquina Estuary) has been examined by Scott
(1973) and Bayer (1983) with murres beginning to
fledge young in early July, gulls and pelagic cor-
morants in late July, and Brandt's cormorants and
pigeon guillemots in early to mid- August. However,
it would be invalid to assume that nesting in 1983
followed the chronologies of typical years because
nesting success for cormorants and murres was ab-
normally low in 1983 with eggs and young being
abandoned (Bayer2). Although the nesting success
of gulls was not unusually low in 1983 (Bayer fn.
2), the chronology of their nesting might have been
different than in 1982. Thus, comparing 1982 and
1983 bird numbers at Yaquina Estuary for the same
stage of the nesting cycle would be tenuous. Brown
pelicans, Pelecanus occidentalis, and Caspian terns,
Sterna caspia, do not nest in this area.
I divided the estuary and the area around its
mouth into four censusing regions (Fig. 1) with
region A having an area of about 1.8 km2; region
B, 0.5 km2; region C, 3.0 km2; and region D, 3.2
2Bayer, R. D. In prep. Breeding success of seabirds along the
mid-Oregon coast concurrent with the 1983 El Nino. Unpubl.
manuscr. P.O. Box 1467, Newport, OR 97365.
km2. I censused birds from observation points
where I could overlook the estuary or estuary mouth
with a 20 x telescope when glare, heat waves, and
water conditions did not obscure birds. I censused
the areas around the mouth of the jetties from an
observation point about halfway out on the south
jetty (Fig. 1). The boundaries of region A were
estimated -by using the distance to the first naviga-
tion buoys to the west of the jetties as a radius that
was about 1.5 km from the observation point and
1.0 km from the end of the jetties to estimate the
outer boundary. All taxa except pigeon guillemots
were censused during a single continuous sweep of
nonoverlapping portions of a region; pigeon guille-
mots were enumerated during two sweeps per por-
tion with the maximum number of the two sweeps
recorded.
I censused "active" (see below) gulls and cor-
morants, nonflying common murres and pigeon
guillemots (including guillemots standing on station-
ary objects), roosting Caspian terns, all brown
pelicans, and all marbled murrelets, Brachyramphus
marmoratus. "Active" gulls were those that flew
over or sat in the water (gulls sitting on stationary
roosts were not included). Gull species included
western, glaucous-winged, L. glaucescens, and
western x glaucous-winged gull hybrids (Hoffman
et al. 1978). Cormorants present were usually either
Brandt's or pelagic cormorants, but some double-
crested cormorants, P. auritus, were also included.
"Active" cormorants were those on the water sur-
face or those making short flights in association with
a feeding flock; cormorants on transit flights
through a region or roosting on stationary objects
were not counted. Only nonflying murres and guille-
mots were included because others flew through
regions A and B without landing (and feeding). Al-
though roosting Caspian terns were obviously not
feeding, they were recorded because their numbers
were an index of the total numbers present and
because it was not possible to count foraging (i.e.,
flying) Caspian terns accurately. There were 166
censuses during 37 d from 1 June to 16 September
1982 at regions A-D during variable tidal conditions,
and 39 censuses within 2 h of low tides before 1500
Pacific Daylight Time (PDT) during 39 d from 1 June
to 30 August 1983 at regions A-C. Each census took
45-75 min, depending upon the number of birds
present.
Comparisons of bird numbers between 1982 and
1983 were only made for censuses within 2 h of low
tides before 1500 PDT. Comparisons were made
during the 1 June to 30 August period for brown
pelicans, "active" cormorants, "active" gulls, and
280
BAYER: SEABIRDS NEAR OREGON ESTUARINE SALMON HATCHERY
pigeon guillemots because the numbers of these
birds during this period did not show any signs of
seasonal variation. But for common murres, the
periods of comparison were 1 June-31 July and 1-30
August, and the periods for Caspian terns were 1
June-10 July, 11 July-5 August, and 6-30 August.
The periods for common murres and Caspian terns
were chosen because in one or both years there were
marked seasonal changes in bird numbers between
or among these periods.
The number of days postrelease refers to the num-
ber of daylight periods after a smolt release (Myers
1980). For example, if smolts were released on Mon-
day night or early Tuesday morning, then Tuesday
after dawn would be considered as 1-d postrelease
(i.e., the first day, or first daylight period, after a
release).
If variances were not significantly different, then
the student's £-test for two means or the analysis
of variance (ANOVA) for three or more means were
calculated to determine statistical differences be-
tween or among means. If variances were signifi-
cantly different, the Mann-Whitney U test or nor-
malized Mann-Whitney z test (Zar 1974, p. 109-113)
for two samples or the Kruskal-Wallis rank H or Hc
(if ranks were tied) test (Zar 1974, p. 139-142) for
three or more samples was used. All tests were
two-tailed.
RESULTS AND DISCUSSION
Smolt Releases
Oregon Aqua-Foods, Inc. (OAF) has released 2
million or more salmon smolts (almost all coho
salmon, Oncorhynchus kisutch) each year since 1977
into Yaquina Estuary between June and August. In
1982 and 1983, the proportion that were coho
salmon was 98% and 94%, respectively; the re-
mainder were chinook salmon, 0. tshawytscha. Un-
til 1983, these releases were under variable tidal con-
ditions in the evening just after dark to minimize
bird predation of smolts as they were released. In
1983, salmon smolts were released either in the
evening or early morning on the ebbing tide while
it was still dark.
Salmon smolts do not immediately swim to the
ocean after they are released. Myers (1980) found
that the number of OAF smolts in the Yaquina
Estuary declined exponentially after a release. Dur-
ing June- August releases in 1978, half the smolts
left the estuary within an average of 3.9 d (SE =
0.7 d, range 1.7-9.0 d, N = 9 releases) with a few
smolts remaining in the estuary several months
(calculated from Myers 1980). There are no data to
determine if the smolt residency time in the estuary
differed between 1982 and 1983.
In 1982 and 1983 from June through August, the
interval between releases averaged <2.5 d, and an
average of 0.2-0.3 million fish were released each
time (Table 2). Although the average release inter-
val was longer and the number of fish per release
usually greater in 1983, these differences were not
significant (Table 2). But the biomass of fish per
release was significantly greater in 1983 than in
1982 in the June- July and June- August periods
(Table 2). Overall, 1.6 million fewer fish were re-
leased in 1983 than 1982, but the total biomass
released was almost 38 metric tons (t) greater (Table
2); this resulted from smolts weighing more on the
average in 1983 (32.9 g/smolt) than in 1982 (26.7
g/smolt) (calculated from Table 2).
Bird Predation of Salmon Smolts
Although all birds in this study except marbled
murrelets were observed with salmon smolts in their
bills, the importance of smolts in these birds' diets
was not documented in this study. However, Mat-
thews (1983) found that coho salmon smolts com-
Table 2.— Releases of salmon smolts in 1982 and 1983 at Yaquina Estuary. Total
= total number or biomass of fish released during a period. Differences between years
tested with student's f, Mann-Whitney U, or normalized Mann-Whitney z test. NS =
not significant.
Re-
Release
interval
(d)
No. fish/release
(millions)
Fish biomass/release
(t)
Period
Year
N
X
SD
P
x SD
P
Total
x SD P
Total
June-July
1982
30
2.0
1.2
0.3 0.1
9.6
7.5 2.4
225.3
1983
25
2.4
1.7
NS
0.4 0.1
NS
9.0
11.3 4.6 <0.01
268.4
August
1982
20
1.6
0.7
0.2 0.1
4.7
7.9 3.4
158.6
1983
12
2.4
1.6
NS
0.3 0.2
NS
3.7
12.8 9.0 NS
153.0
June-
1982
50
1.8
1.0
0.3 0.1
14.4
7.7 2.8
383.9
August
1983
37
2.4
1.6
NS
0.3 0.2
NS
12.8
11.8 6.3 <0.01
421.4
281
FISHERY BULLETIN: VOL. 84, NO. 2
posed 13% of 287 prey items of common murres col-
lected within 2 km of the Yaquina's jetties during
the summer of 1982.
Salmon smolts appeared to be most vulnerable to
predation soon after a release. When they first
entered the estuary after exiting a pond through a
large tube, smolts seemed disoriented and milled
around the surface where they could easily be caught
by birds. Night releases allowed smolts several hours
to become adjusted before becoming vulnerable to
predators at daylight. (The only somewhat signifi-
cant nocturnal bird predator were heerman's gulls,
L. heermanni, but they usually numbered <50 birds,
were not present for every release, and were pres-
ent mainly in late July and August.)
Within about 4 h after daylight after a release,
some smolts were observed jumping at the mouth
of the jetties in regions A and B, where birds also
concentrated. For censuses of regions A-D within
2 h of low tides and within 2 d of a release in 1982,
an average of 97.9% (SD - 6.3, N - 17 d) of the
common murres, 91.5% (SD = 16.2, N = 17 d) of
the "active" gulls, and 90.5% (SD = 26.8, N = S
d) of the "active" cormorants censused were at
regions A and B. But regions A and B accounted
for only about 27% of the area of regions A-D.
Evidently, the turbulent action of the estuarine
water entering the ocean and/or the funneling ef-
fect of the jetties (Fig. 1) caused the smolts to be
particularly vulnerable to predators there.
During the first 12 h of daylight after a release,
some smolts within 0.5 km of the release site were
still vulnerable to bird predation as many smolts
were near the water surface. Many jumped out of
the water, and some rolled on their sides exposing
their silver undersides, which were highly conspic-
uous against the dark water background. Gulls often
sat on the water and grasped a fish as it jumped into
the air. Schools of smolts also milled near the sur-
face where they were clearly visible to humans (and
presumably birds).
Within-Day Variation in Bird Numbers
Bird abundance was clearly not constant within
a day, and taxa did not reach maxima synchronously
(Fig. 2). Censuses within 2 h of early low tides (i.e.,
low tides before 1500 PDT) averaged closer to the
maximum number censused daily for all taxa, and
censuses near high tide were usually closer to the
daily maximum than counts within 2 h of evening
low tides (i.e., after 1800 PDT) for all taxa except
brown pelicans (Table 3). But differences in censuses
among tidal conditions within a day were only sig-
IOO
COMMON MURRES
( MAX=442 I)
LO A 0.8
0600 0800 1000 1200 1400 1600 1800 2000
PACIFIC DAY L IGHT TIME
Figure 2.— Percentage of daily maximum number of common
murres, "active" gulls, "active" cormorants, and pigeon guillemots
(PCs) observed on 5 August 1982 (which was two days postrelease)
at regions A-D. Times and heights of measured low (LO) and high
(HI) tides are indicated by open and closed triangles, respective-
ly. MAX - maximum number of birds seen on 5 August.
nificant for common murres and "active" gulls
(Table 3).
A single census at any time of day is unlikely to
estimate accurately the maximum number of birds
of any taxon present that day (Table 3). The average
census only ranged from 10.8% to 63.7% of the daily
maximum (Table 3). The best censuses to use for
estimates would be those within 2 h of a morning
or afternoon low tide because their averages
(44-64% of daily maxima) were greater than for
high and evening low tides, and their CV's (41-82%)
were generally lower than for other tides (Table
3).
Daily Variation in Bird Numbers
On a day to day basis, bird numbers could often
be seen to increase in the first day postrelease and
then to decline (Fig. 3). However, the degree of in-
crease was variable. Overall, murres, "active" gulls
in 1983, and brown pelicans exhibited the same pat-
282
BAYER: SEABIRDS NEAR OREGON ESTUARINE SALMON HATCHERY
Table 3.— Percentage of daily maximum number of birds observed within 2 h of ac-
tual high tides, early low tides (i.e., time of low tide before 1500 PDT), and late low
tides (i.e., time of low tide after 1800 PDT). Censuses between 6 July and 17 September
1982 at regions A-D with 9-11 censuses/d (i.e., 13-14 h period). N = total censuses;
CV = coefficient of variation.
Days
Percent of daily maximum birds within 2 h of
High tide
Early low tide
CV
N x (%)
Late low tide
N
X
CV
(0/0)
CV
N x (%)
common murres
"active" gulls
brown pelicans
"active" cormorants
pigeon guillemots
9
10
6
4
3
31
35
21
14
10
130.8
237.9
339.1
"32.6
552.9
92.5
81.5
79.0
112.6
58.8
24 163.7 55.3
28 249.5 71.9
14 344.0 81.8
7 "61.3 65.3
8 558.O 41.0
11 120.3 100.0
11 218.1 100.0
8 349.1 58.9
6 "10.8 142.6
3 533.9 93.8
'Heterogeneity, Kruskal-Wallis Hc = 16.36, P< 0.01.
heterogeneity, Kruskal-Wallis Hc = 7.62, P< 0.10.
heterogeneity, Kruskal-Wallis Hc = 0.80, P > 0.10.
"Heterogeneity, Kruskal-Wallis Hc = 5.62, P > 0.10.
5Heterogeneity, Kruskal-Wallis Hc = 1.87, P > 0.10.
tern of more birds present the first day after a
release than later; this pattern, however, was sig-
nificant only in 1983 (Tables 4, 5). In contrast, only
"active" cormorants were more numerous the
second day after a release than on the first day;
however, the differences in cormorant numbers
among days were only significant in 1983 (Table
5).
Numbers of pigeon guillemots and Caspian terns
did not show any indication of dependence on the
number of days postrelease. The differences in
pigeon guillemot numbers in the 1 June-30 August
period among 1,2, and 3-6 d postrelease was insig-
nificant (1982: F = 0.23, df = 2, 34; P > 0.10; 1983:
Kruskal-Wallis Hc = 0.61, P > 0.10). Sample sizes
were too small to test differences for Caspian terns
in 1982, but in 1983 variation with 1, 2, and 3-6 d
postrelease was insignificant in either the 1 June- 14
July period (when there were few Caspian terns
(Kruskal-Wallis Hc = 2.74, P > 0.10)) or the 15
July-30 August period (when they were abundant
(Kruskal-Wallis Hc = 2.74, P > 0.10)).
T FIRST
DAY POSTRELEASE
80
0
\
in
0
O CORMORANTS
0
*40
CD
\\
\\
0 — 1
, x / 0N /
l/\ W \ /
% \ ° 9/
/
0
T
1 1
. t r t , ?
T
4000
cr
3 2000
- 800
o
c
400 1
J I I
T , T , ■ T
- 0
13 14 15 16 17 18 19 20 21 22
JULY 1983
Figure 3.— Number of brown pelicans, "active" cormorants,
"active" gulls, and common murres with relation to dates of salmon
smolt releases during 14-22 July 1983 censuses that were within
2 h of low tides before 1500 PDT.
Table 4.— Numbers of common murres at regions A-C in 1982 and 1983 during the 1 June-31 July period when
murres were abundant and the 1-30 August period when murres were infrequent in 1983. N = number of cen-
suses (1 census/d within 2 h of low tides before 1500 PDT); MAX = maximum number of birds counted.
1 June-31 July
1-30 August
1-d postrelease
2-d postrelease
3-6 d postrelease
N x SD MAX
1-3 d postrelease
Year
N x SD MAX
N
x SD MAX
N x SD MAX
1982
1983
8 i23,053 967 4,310
13 2.63J10 2,746 9,638
6
8
131,823 2,114 5,988
362,462 2,063 6,206
2 1 "1,276 824 1,858
6 46561 711 1,972
4 51,860 2,091 4,419
10 S106 280 901
1 Heterogeneity among days: Kruskal-Wallis H = 4.88, P > 0.10.
21982 vs. 1983: Mann-Whitney U = 52, P > 0.10.
31982 vs. 1983: student's f = 2.12, df = 12, P< 0.10.
"1982 vs. 1983: not tested because of small sample sizes in 1982.
M982 vs. 1983: Mann-Whitney U = 38, P < 0.02.
6Heterogeneity among days: Kruskal-Wallis H = 8.91, P < 0.05.
283
FISHERY BULLETIN: VOL. 84, NO. 2
Table 5.— Comparison of bird numbers at regions A-C during 1
June-30 August period in 1982 with 1983. Day(s) = days post-
release of salmon smolts, N = number of censuses (1 census/d
within 2 h of low tides before 1500 PDT), and MAX = maximum
number of birds counted.
"active"
brown
"active"
gulls
pelicans
1 2 3-6
cor
1
morants
Days(s):
1 2 3-6
2 3-6
1982 N
10 7 2
10
7
3
9
7 3
Birds (x)
1391 13811445
231
211
27
318
328 347
SD
272 294 36
36
10
10
13
41 38
MAX
919 729 470
106
30
19
38
110 88
1983 N
20 9 9
20
9
9
20
9 9
Birds (x)
MOO 1332 !26
225
217
27
346
381 321
SD
349 450 25
19
22
8
33
90 15
MAX
1,311 1,200 77
84
69
20
128
286 52
11 d vs. 2 d vs. 3
Kruskal-Wallis Hc =
0.07, df = 28, P >
21 d vs. 2 d vs. 3
Kruskal-Wallis Hc =
= 107,P>0.10;2d,
U = 14, P> 0.10.
31 d vs. 2 d vs. 3-
Kruskal-Wallis Hc =
= 142.5, P< 0.02; 2
U = 20, P>0.10.
6 d: 1982, Kruskal-Wallis Hc = 0.44, P > 0.10; 1983,
14.62, P < 0.01. 1982 vs. 1983; 1 d, student's f =
0.10; 2 d, student's f = 0.25, df = 14, P > 0.10.
6 d: 1982, Kruskal-Wallis Hc = 2.44, P > 0.10; 1983,
8.71, P< 0.02. 1982 vs. 1983: 1 d, Mann-Whitney U
Mann-WhitneyU = 32.5, P>0.10; 3-6 d, Mann-Whitney
6 d: 1982, Kruskal-Wallis Hc = 1.84, P > 0.10; 1983,
6.14, P < 0.05. 1982 vs. 1983: 1 d, Mann-Whitney U
d, Mann-Whitney U = 49, P< 0.10; 3-6 d, Mann-Whitney
Yearly Variation in Bird Numbers
Cormorants were significantly more abundant for
1 and 2 d postrelease in 1983 than in 1982 but not
for 3-6 d postrelease (Table 5). Brown pelicans were
about as numerous in 1983 as in 1982 in the 1
June-30 August period (Table 5).
Gulls were not significantly more abundant in
1983 than in 1982 in the 1 June-30 August period
(Table 5), and their nesting success was also not
lower in 1983 than in other years (Bayer fn. 2). But
Caspian terns were significantly more abundant dur-
ing the 11 July-5 August period (when many
emigrated) in 1983 than in 1982 (Bayer 1984).
There were an average of about 650 more com-
mon murres per census in 1983 than in 1982 dur-
ing the 1 June-31 July period for either 1 or 2 d post-
release, but the differences were only significant for
2 d postrelease (Table 4). In contrast, there were
more murres in 1982 than in 1983 during this period
for 3-6 d postrelease, but there were only two
samples in 1982 (Table 4).
In the 1-30 August period, there were significantly
fewer murres in 1983 than in 1982 (Table 4). The
low numbers in 1983 resulted from the mass exodus
of murres after 31 July, whereas in 1982 murre num-
bers did not decline as dramatically until after 12
August. In fact, there were still more murres pres-
ent within 2 h of low tides on 3 and 16 September
1982 (186 and 318 murres, respectively) than in 10
censuses on different days between 1 and 18 August
1983 (i.e., <56 murres). The early exodus of murres
in 1983 probably resulted from them migrating
north early because they were unusually numerous
in inland marine waters of Washington during the
summer of 1983 (Mattocks et al. 1983).
During the June through August period at regions
A-C, pigeon guillemot numbers were about 29%
greater during 1982 (x = 23.9, SD = 11.0, N = 13
d) than in 1983 (x = 17.1, SD = 7.8, N = 35 d), a
significant difference (t = 2.39, df = 46, P < 0.05).
This decrease could have resulted from the large
number of mortalities in the spring of 1983
(Hodder3).
Marbled murrelets were not observed in any of
120 censuses of regions A-D in the June through 20
August period of 1982. In 1983 at regions A-C, they
were observed in only 1 of 21 censuses in June and
August, but an average of 3.9 murrelets/census (SD
= 8.7, range 0-32, N = 17 censuses) were counted
in July. The difference in the number of murrelets
per census in July was significantly greater in 1983
than in 1982 (normalized Mann-Whitney z = 2.18,
P < 0.05). They were only observed at region A.
CONCLUSIONS
It is not possible to relate the number of birds
nesting near the Yaquina Estuary with the number
feeding there for several reasons. First, the num-
ber of nesting and nonbreeding birds is unknown,
so it is not possible to determine what proportion
of the birds censused were nonbreeders. Second,
censuses of feeding birds represent the number of
birds feeding at only one point in time, but nesting
birds probably fed serially at the Yaquina Estuary
(i.e., birds came and went as individuals or small
flocks not as massive synchronous flocks). With
serial use, the number of nesting birds using the Ya-
quina Estuary could be much larger than indicated
by censuses. Unfortunately, birds would have to be
individually recognizable to determine the degree
of serial use, and this was beyond the scope of this
study.
It also was not possible to tell from how far nest-
ing birds came to feed at the Yaquina Estuary in
either year because birds were not individually
marked. Murres, however, may have come from
long distances. In both years, the average number
of murres one day after a salmon release (Table 4)
was greater than the number of murres at a colony
<7 km away (Table 1), and the maximum number
3J. Hodder, Institute of Marine Biology, Charleston, OR 97420,
pers. commun., 1984.
284
BAYER: SEABIRDS NEAR OREGON ESTUARINE SALMON HATCHERY
of murres simultaneously seen at the Yaquina (Table
4) was greater than the number of murres at
colonies within 45 km of the Yaquina (Table 1).
It was somewhat surprising that more cormorants
and common murres were not at the Yaquina
Estuary in 1983, because they then had a poor
nesting season, probably as a result of a food short-
age (Bayer fn. 2). There are several possible reasons
why there were not more cormorants and murres
counted in 1983. First, the number of salmon smolts
available at the Yaquina Estuary might have been
insufficient or the distance between the Yaquina and
their nesting site too great for these birds to be
dependent solely on salmon smolt releases. If the
salmon smolt releases had been oftener and nearer
to bird nesting colonies, the numbers of birds pres-
ent could have been much greater. Second, there
may have actually been many more birds in 1983
than in 1982, but a single census per day regime was
inadequate to measure this (Table 3). Censuses
throughout the day in 1983 or measurements of the
serial use of the Yaquina Estuary in 1982 and 1983
might have indicated that there were dramatically
more birds using the Yaquina in 1983 than in 1982.
Finally, the lack of there not being a greater influx
of birds in 1983 might be because many of the
murres and cormorants that normally remained
near the Yaquina dispersed to avoid the generally
poor feeding conditions between releases. Many
Oregon pelagic and Brandt's cormorants had aban-
doned nesting by mid-July 1983 (see Bayer fn. 2;
Hodder fn. 3), and many murres may have left the
Oregon coast before it became apparent at the Ya-
quina Estuary at the end of July. Early dispersal
or migration is known for southern seabirds during
an El Nino (Duffy 1983a; Schreiber and Schreiber
1984).
ACKNOWLEDGMENTS
I am grateful to Bill McNeil, Vern Jackson, Rob
Lawrence, Mike Bauman, and Andy Rivinus of
Oregon Aqua-Foods for facilitating the logistics and
funding of this project; to Dan Varoujean for advice
about censusing murres prior to the 1982 field
season; and to Jan Hodder, Dan Matthews, Daniel
W. Anderson, Peter Stettenheim, and two anony-
mous reviewers for constructive comments on an
earlier draft of this manuscript.
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1983. Nesting success of western gulls at Yaquina Head and
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1984. Oversummering of whimbrels, Bonaparte's gulls, and
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Boersma, P. D.
1979. Breeding patterns of Galapagos penguins as an in-
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Can. Minist. Supply Cat. No. CW66-65/1984.
1984b. Seabird-fisheries relationships in the northeast Atlan-
tic and North Sea. In D. N. Nettleship, G. A. Sanger, and
P. F. Springer (editors), Marine birds: their feeding ecology
and commercial fisheries relationships, p. 162-169. Proc.
Pacific Seabird Group, 6-8 January 1982, Can. Wildl. Serv.,
Can. Minist. Supply Cat. No. CW66-65/1984.
Hoffman, W., J. A. Wiens, and J. M. Scott.
1978. Hybridization between gulls (Larus glaucescens and L.
occidentalis) in the Pacific Northwest. Auk 95:441-458.
Huyer, A.
1983. Anomalously warm water off Newport, Oregon, April
1983. Trop. Ocean-Atmos. Newsl. 21:24-25.
Mattocks, P., Jr., B. Harrington-Tweit, and E. Hunn.
1983. Northern Pacific Coast region. Am. Birds 37:1019-
1022.
Matthews, D. R.
1983. Feeding ecology of the common murre, Uria aalge, off
the Oregon coast. M.S. Thesis, Univ. Oregon, Eugene, 108
P-
Myers, K. W.
1980. An investigation of the utilization of four study areas
in Yaquina Bay, Oregon, by hatchery and wild juvenile sal-
monids. M.S. Thesis, Oregon State Univ., Corvallis, 234 p.
Oregon State Land Board.
1973. Oregon estuaries. State of Oregon, Div. State Lands.
Parker, R. R.
1962. Estimations of ocean mortality rates for Pacific salmon
(Onc&rhynchus). J. Fish. Res. Board Can. 19:561-589.
1968. Marine mortality schedules of pink salmon of the Bella
Coola River, central British Columbia. J. Fish. Res. Board
Can. 25:757-794.
Pitman, R. L., M. R. Graybill, J. Hodder, and D. H.
Varoujean.
In press. The catalog of Oregon seabird colonies. U.S. Dep.
Fish Wildlife, USFWS FWS/OBS.
Quinn, W. H., D. O. Zopf, K. S. Short, and R. T. W. Kuo Yang.
1978. Historical trends and statistics of the Southern Oscilla-
tion, El Nino, and Indonesian droughts. Fish. Bull., U.S.
76:663-678.
285
FISHERY BULLETIN: VOL. 84, NO. 2
Reed, R. K. Scott, J. M.
1983. Oceanic warming off the U.S. West Coast following the 1973. Resource allocation in four syntopic species of marine
1982 El Nino. Trop. Ocean-Atmos. Newsl. 22:10-12. diving birds. Ph.D. Thesis, Oregon State Univ., Corvallis,
SCHREIBER, R. W., AND E. A. SCHREIBER. 107 p.
1984. Central Pacific seabirds and the El Nino Southern Zar, J. H.
Oscillation: 1982 to 1983 perspectives. Science 225:713- 1974. Biostatistical analysis. Prentice-Hall, Englewood
716. Cliffs, N.J., 620 p.
286
DEVELOPMENT AND EVALUATION OF METHODOLOGIES FOR
ASSESSING AND MONITORING THE ABUNDANCE OF
WIDOW ROCKFISH, SEBASTES ENTOMELAS
Mark E. Wilkins1
ABSTRACT
Rapid expansion of a new fishery for widow rockfish, Sebastes entomelas, stocks off the Pacific coast of
the United States began in 1979. Within 3 years, landings rose from <1,000 t to almost 30,000 t of a
species for which little information on abundance or life history was available. It was known that widow
rockfish occurred in irregularly distributed, dense, midwater, and semidemersal schools primarily during
the night, which posed problems in directly assessing this resource Therefore, a project was designed
to further investigate the habits and distribution of the species and develop an adequate assessment
methodology.
Line transect survey methods, using sector scanning sonar to estimate the number of schools per
unit area and standard hydroacoustic echo integration techniques to estimate school biomass, were used
in study areas off Washington and Oregon. The applicability of this methodology will depend on our abil-
ity to resolve technical problems and minimize the effects of distributional variability by refining survey
design. The need for more sophisticated sonar equipment to improve data collection and processing, the
extreme temporal and spatial variability of widow rockfish school size and location, and the difficulty
of identifying the species composition of observed schools are matters of special concern.
The rockfish (genus Sebastes) of the Pacific Ocean
are comprised of over 65 species exhibiting a wide
array of colors, sizes, body forms, behavior, and life
history characteristics. Members of this family are
generally demersal or semidemersal and school over
hard substrate on the continental shelf and slope.
The widow rockfish, Sebastes entomelas, is atypical.
As an adult it aggregates in dense midwater schools
during the night.2 These schools tend to disappear
from established fishing grounds at dawn or shortly
thereafter, becoming less vulnerable to the fishery.
The role of this species in the Pacific coast ground-
fish fishery changed from an undesirable incidental
catch in 1978 to a major target species by 1980. Ad-
vances in fishing technology and product handling
and marketing, as well as new vessels seeking alter-
native fisheries, promoted an increase in landings
from 1,107 t in 1978 to 28,419 t in 1981 (Table 1).
By 1981, schools were becoming more difficult to
locate and there was concern that the resource was
being overharvested. The fishery began expanding
into new areas to maintain profitable catch rates.
During late 1981 and early 1982, most of the widow
Northwest and Alaska Fisheries Center Seattle Laboratory, Na-
tional Marine Fisheries Service, NOAA, 7600 Sand Point Way N.E.,
Building 4, BIN C15700, Seattle, WA 98115.
2Groundfish Management Team. 1981. Status of the widow
rockfish fishery. Unpubl. manuscr., 41 p. Pacific Fishery Manage-
ment Council, 526 S.W Mill Street, Portland, OR 97201.
rockfish were being taken from the vicinities of
Bodega Bay and Monterey, CA, though fishing was
taking place as far north as Cape Flattery, WA.
The rapid growth of this new fishery resulted in
large catches from a resource about which little was
known. Research on this species prior to 1979 was
limited to general descriptions of distribution,
habitat, and biological characteristics (Hitz 1962;
Phillips 1964; Pereyra et al. 1969). Scientists began
gathering data in 1978 to determine the impact of
the fishery on the condition of the stock, to define
the distribution and size of the stock, and to establish
a baseline of biological characteristics of the species.
Commercial landings have been sampled by State
Table 1.— Landings of widow rockfish by state for
years 1973-83 in metric tons.
Year
Washington
Oregon
California
Total
1973
81
15
29
125
1974
18
7
47
72
1975
13
11
57
81
1976
51
55
147
253
1977
277
34
267
578
1978
428
472
207
1,107
1979
1,697
1,960
636
4,293
1980
6,632
8,718
4,808
120,677
1981
7,211
14,689
6,519
28,419
1982
6,030
9,262
10,270
25,562
1983
3,293
3,151
3,455
9,899
This also included 519 1 of joint venture and foreign catch.
Manuscript accepted July 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
287
FISHERY BULLETIN: VOL. 84, NO. 2
and Federal agencies in Washington, Oregon, and
California for information on size and age composi-
tion, sex ratio, maturity, feeding habits, morpho-
metries, meristics, and fecundity.
Widow rockfish abundance was estimated by the
Groundfish Management Team (fn. 2, 19823) of the
Pacific Fisheries Management Council, using cohort
and stock reduction analyses (SRA) (Kimura and
Tagart 1982). These stocks were found to have been
fished down from their virgin level and were thought
to be approaching a biomass level which would,
under prudent management, produce a maximum
sustainable yield of about 12,000 t in the INPFC (In-
ternational North Pacific Fisheries Commission) Col-
umbia and Eureka areas.
Research surveys were needed to complement
these analyses by providing independent estimates
of abundance, describing the distribution, and col-
lecting biological information not available from
fishery data (for example, data on prerecruits and
fish in areas which will not support a profitable
fishery). Widow rockfish present special problems
to those seeking to estimate their abundance
through research surveys. The species is not usual-
ly available to bottom trawls, precluding traditional
"area-swept" trawl surveys, and its tightly clustered
distribution and inconsistent schooling behavior
reduce the effectiveness of traditional hydroacous-
tic surveys.
In 1980, the Northwest and Alaska Fisheries
Center (NWAFC) began developing a practicable
method to survey widow rockfish stocks. Scientists
needed to understand the distribution and behavior
of widow rockfish to determine which survey
methods might be most appropriate to measure the
size of the resource The first objective of the project,
therefore, was to study aspects of the behavior,
distribution, and biology of the species. The distri-
bution of its characteristic nighttime aggregations
relative to features of submarine topography was of
particular interest. The distribution of this species
is highly variable both on a diel basis and over longer
periods, and the reasons for this variability were also
of interest. Another question concerned what pro-
portion of the total resource is present in detectable
schools and how that proportion changes in space
and time Clark and Mangel (1979) described a
theoretical situation in yellowfin tuna stock dynamics
wherein detectable, fishable schools are constantly
being replenished from an undetectable portion of
3Groundfish Management Team. 1982. Status of the widow
rockfish fishery. Unpubl. manuscr., 22 p. Pacific Fishery Manage-
ment Council, 526 S.W. Mill Street, Portland, OR 97201.
the population. They discussed the implications of
this behavior in a fishery. If such a phenomenon
could be confirmed in widow rockfish, determining
the detectable proportion of the population might
enable us to estimate the absolute size of the
resource
The second objective of the project was to inves-
tigate methodologies with potential for estimating
widow rockfish stock size, considering the species'
behavior and distribution patterns. The final objec-
tive was to evaluate the effectiveness of the chosen
technique when actually implemented.
The project was conducted in three phases: 1) an
examination of the biology and behavior of widow
rockfish on commercial fishing grounds, 2) the
development of a practical survey method for assess-
ing distribution and abundance, and 3) an evaluation
of the feasibility and effectiveness of applying such
assessment methodology to widow rockfish on a
routine coastwide monitoring basis. Field studies
were initiated in March 1980 and concluded in April
1982. Behavior studies were conducted during
August 1980 and April 1981. Field work focusing
on methodology development took place during late
March 1980 and mid-March 1981, and the trial
assessment survey took place during mid-March to
early April 1982. All field work was conducted off
Oregon and southern Washington (Fig. 1).
The purpose of this report is to document the work
done to date on the development of widow rockfish
assessment methodologies, to evaluate the utility of
those methods for routine assessment and monitor-
ing of widow rockfish stocks and other species ex-
hibiting a similar behavior, and to recommend means
of enhancing future assessment efforts.
BEHAVIOR STUDIES (1980-81)
The nature of the fishery made it apparent that
the behavior of widow rockfish differed from that
of other commercially important species of the genus
Sebastes. Extremely large widow rockfish catches
were taken by midwater trawlers operating almost
exclusively at night and fishing on very dense mid-
water schools in only a few small areas along the
coast.
The first phase of the project studied the behavior
and habits of widow rockfish to determine their
distribution patterns, using demersal and midwater
trawls and hydroacoustic observations. This included
determining where the fish go when the dense, mid-
water schools disperse; whether there are compo-
nents of the stock other than the typical midwater
aggregations; and at what period in their daily cycle
288
WILKINS: ABUNDANCE OF WIDOW ROCKFISH
Nelson
Islanc
Halibut Hill
The Fingers-
Heceta
Bank
Cape Blanco
- 45° 00'
47° 00' N
46° 00'
44° 00'
- 43° 00'
126° 00'W
125° 00'
124° 00'
123° 00'
Figure 1.— Widow rockfish survey areas off the coasts of Washington and Oregon occupied during field work
conducted between 1980 and 1982.
289
FISHERY BULLETIN: VOL. 84, NO. 2
their availability is most stable. Other objectives were
to investigate the possible causes of their diel
aggregation habits and to develop an ability to
distinguish widow rockfish schools from those of
other species on the basis of echosign4 characteris-
tics and test fishing.
Methods
The behavior study was initiated 11-13 August
1980 aboard the chartered trawlers Pat San Marie
and Mary Lou. Concurrently, scientists aboard the
NOAA RV Miller Freeman conducted a conventional
echo integration survey in the study area and made
four midwater tows to identify the species composi-
tion of the schools sighted. The survey was repeated
during 10-26 April 1981 aboard the NOAA RV Chap-
man and included 7 d of hydroacoustic and sonar
observations.6 Descriptions of the vessels, trawls, and
hydroacoustic equipment employed appear in Tables
2, 3, and 4, respectively.
Demersal trawl stations were located around a
seabed rise known as Nelson Island off Newport, OR,
to determine if significant quantities of widow rock-
fish occurred on or near the bottom in an area where
they were known to form dense midwater aggrega-
tions. A 4 x 4 station grid with interstation
distances of 4.6 km (Fig. 2) was established between
the depths of 110 and 360 m with the rise at the
center. Two trawl hauls were attempted at each sta-
tion: one during daylight and one during darkness.
When significant midwater fish schools were ob-
served, they were sampled with midwater trawl gear
for species composition.
The contents of each trawl haul were sorted by
species, weighed, counted, and recorded. Otoliths
were removed from samples selected for age deter-
mination and stage of maturity was recorded for
some individuals. Stomach sample collections,
stratified by fish length, were also taken and pre-
served for feeding studies.6 No meaningful descrip-
tion of age and length composition was possible
because of the small catches.
Consultations with fishermen, observation trips
aboard commercial trawlers, and observations dur-
ing research operations provided further informa-
tion about school characteristics and diel behavior
patterns of widow rockfish and other species on and
around widow rockfish fishing grounds.
Results
Twenty-seven demersal tows were completed dur-
ing the August 1980 widow rockfish behavior study,
including 12 at night and 15 during the day. The
trawl was damaged during two night hauls. The wi-
dow rockfish catch was small, with 1 or 2 specimens
in six hauls and 20 specimens in one of the night
hauls during which the trawl was damaged (Fig. 3,
1980). Therefore, no conclusions about diel move-
ment patterns were possible from the 1980 study.
The Miller Freeman transected the Nelson Island
area during the same study period and found one
4"Echosign" can be defined as the echo return output (paper echo-
grams, video chromoscope displays, etc) of an echo sounder aimed
at targets in the water column.
6Thomas, G. L., C. Rose, and D. R. Gunderson. 1981. Rockfish
investigations off the Oregon coast, annual report. Unpubl.
manuscr., 20 p. Univ. Wash., Fish. Res. Inst, FRI-UW-8119.
6Adams, P. B. 1984. The diet of widow rockfish (Sebastes en-
tomelas) in northern California. Unpubl. manuscr. Southwest
Fisheries Center Tiburon Laboratory, National Marine Fisheries
Service, NOAA, 3150 Paradise Drive, Tiburon, CA 94920.
Table 2.-
-Vessels used during the widow rockfish assessment project.
Main
Length
engine
Survey
Vessel
(m)
(hp)
type
Agency1
Dates
Muir Milach
26
800
Hydroacoustic
sonar
FRI
19 Mar.-2 Apr. 1980
Pat San Marie
31
765
Behavior
NWAFC
11-13 Aug. 1980
Mary Lou
26
700
Behavior
NWAFC
11-13 Aug. 1980
Miller Freeman
66
2,200
Behavior and
hydroacoustic
NWAFC
11-13 Aug. 1980
Alaska
30
600
Hydroacoustic
sonar
FRI
12-23 Mar. 1981
Chapman
39
1,165
Behavior and
hydroacoustic
sonar
NWAFC
7-26 Apr. 1981
Ocean Leader
36.5
1,125
Hydroacoustic
sonar
NWAFC
14 Mar.-7 Apr. 1982
1FRI = Fishery Research Institute; NWAFC = Northwest and Alaska Fisheries Center.
290
WILKINS: ABUNDANCE OF WIDOW ROCKFISH
Table 3.— Fishing gear used during the widow rockfish assessment project.
Trawl type
Vessels
Doors and accessory gear
Approximate
fishing dimensions
Bottom trawl
Nor'eastern
Midwater trawl
Alaska Diamond
Norsenet
No. 7 Gourock
rope wing
No. 8 Gourock
rope wing
Pat San Marie 1.5 x 2.1 m steel V-doors, 55 m triple
and Mary Lou dandylines, 32 mm mesh cod end
liner, roller gear
Muir Milach Same as above but with 1.8 x 2.7 m
and Chapman steel V-doors 2,500 lb
Alaska Same as above but with 1.6 x 2.9 m
aluminum V-doors
Chapman 1.8 x 2.7 m steel V-doors, 55 m dou-
ble dandylines with 4 sets of 5.5 m
bridles, 125 kg weights attached to the
bottom of each wingtip, 32 mm mesh cod
end liner
Alaska Same as above but with 1.6 x 2.9 m
aluminum V-doors
Miller Freeman 6 m2 Waco doors, 75 m double dandy-
lines, 46 mm mesh cod end covered with
a double braided 144 mm mesh bag
Muir Milach 4.6 m2 Suberkrub doors, 73.2 m dou-
ble dandylines, 114 mm mesh cod end
(no liner)
Ocean Leader 4.5 m2 Suberkrub doors, 100 m dandy-
lines 200 kg weights attached to the
bottom of each wing, 32 mm mesh cod
end liner
9.1 m headrope height, 13.4
m wingspread
6.10 m headrope height, 16.7
m wingspread (Wathne1)
(not measured)
11.0-14.6 m vertical opening
15.2 m wingspread
Same as above
18-20 m vertical opening
18.3 m vertical opening,
wingspread not measured
21.3 m vertical opening,
wingspread not measured
'Wathne, R, Northwest and Alaska Fisheries Center, 2725 Montlake Blvd. E., Seattle, WA 98115, pers. commun. June 1981.
Table 4.— Hydroacoustic equipment used during widow rockfish behavior and assessment surveys, 1980-82.
Institute; NWAFC = Northwest and Alaska Fisheries Center.
FRI = Fisheries Research
Vessel:
Muir Milach
Miller Freeman
Alaska
Chapman
Ocean Leader
(FRI)
(NWAFC)
(FRI)
(NWAFC)
(NWAFC)
Dates used
19 March-
2 April 1980
11-13 August 1980
12-23 March 1981
21-26 April 1981
14 March-
7 April 1982
Echo sounder and
Simrad1 EK-38
Simrad EK-38
Simrad EK-38
Simrad EK-38
Biosonics 101
transducer
11° beam at -3dB
12° beam at -3dB
11° beam at -3dB
11° beam at -3dB
7° beam at -3dB
Towed V-fin
2-ft Braincon
2-ft Braincon
2-ft Braincon
2-ft Braincon
2-ft Braincon
transducer housing
Tape recorder
TEAC 3440A
cassette
TEAC 3440A
TEAC 3440A
cassette
reel-to-reel
reel-to-reel
reel-to-reel
Chart recorder
Simrad wet paper
Simrad dry paper
Simrad wet paper
Simrad wet paper
EPC 1600 dry
paper
Portable echo
Biosonics 120
NWAFC acoustic
Biosonics 120
Biosonics 120
Biosonics 120
integrator
research container
system
Computer
Not used
NWAFC acoustic
research container
system
Not used
Not used
Radio Shack
TRS-80
Sonar system
C-Tech LSS-68
Not used
C-Tech LSS-68
Simrad SQ
Furuno FSS-75
68 kHz sector
68 kHz sector
searchlight beam
75 kHz sector
scanning
scanning
scanning
Video camera and
RCA C004 camera
Not used
RCA C004 camera
RCA C004 camera
RCA C004 camera
recorder
Panasonic recorder
Panasonic recorder
Panasonic recorder
Panasonic recorder
'Reference to trade names does not imply endorsement by the National Marine Fisheries Service, NOAA.
291
FISHERY BULLETIN: VOL. 84, NO. 2
44° 50' N
- 44° 40'
44° 30'
124° 50' W
124° 40'
Figure 2.— The demersal trawl station grid occupied during 1980 and 1981 widow
rockfish behavior studies on the Nelson Island ground off Newport, OR. The 16 trawl
stations are marked with a (+).
school of widow rockfish, which was sampled with
midwater trawl gear (Fig. 4). It was not possible to
stay in contact with the school long enough to
observe diel changes in behavior.
When the study was repeated in April 1981, only
4 of 20 demersal tows contained widow rockfish. Two
of these tows contained only a single specimen each,
while the others contained 20 and 28 specimens.
Results again indicated that widow rockfish were
relatively unavailable to demersal trawl gear and that
their distribution was somewhat more closely
associated with Nelson Island during the night than
during the day (Fig. 3, 1981).
It is important to be able to distinguish widow
rockfish from other species on the basis of echosign
in order to draw conclusions about their behavior,
distribution, and abundance Commercial fishermen
targeting on this species have shown that this can
be done. We characterized the echosign produced by
widow rockfish and other species occurring on widow
rockfish grounds using echograms obtained aboard
research and commercial vessels and through discus-
sions with commercial fishermen on echograms and
corresponding catches. Widow rockfish schools most
frequently appeared on echograms as tall, slender
columns suspended over an irregular bottom (Fig.
5). These were often accompanied by less dense
layers probably composed of salps and other zoo-
plankton. Widow rockfish were sometimes present
during evening and morning in smaller schools high
in the water column (Fig. 6). Shortbelly rockfish,
Sebastes jordani, and redstripe rockfish, S. proriger,
have similar echosign characteristics and are most
likely to be confused with widow rockfish off the
Oregon coast (Figs. 7, 8). Other midwater targets
in the area were identified as layered schools of
292
WILKINS: ABUNDANCE OF WIDOW ROCKFISH
I
44° 50' N
Figure 3.— Locations of demersal tows which
contained widow rockfish during day (D) and
night (N) sampling during the 1980 and 1981
behavior studies.
44[> 50' N
44° 40'
44° 30'
124° 50' W
124° 40'
293
FISHERY BULLETIN: VOL. 84, NO. 2
44° 50' N
- 44° 40'
44° 30'
124° 50' W
124° 40'
Figure 4.— Hydroacoustic transects (dashed lines) and midwater trawl hauls (solid ar-
rows) conducted by the RV Miller Freeman during the 1980 behavior study. Only haul
43 contained widow rockfish (1,247 kg).
Pacific whiting, Merluccius productus, (Fig. 8) or less
dense layers of zooplankton.
The formation and dispersal of widow rockfish ag-
gregations was observed during the research cruises.
During a typical night, small schools would appear
in late evening (from 2000 to 2400) either near bot-
tom or high in the water column. As the night pro-
gressed, these schools tended to grow and those high
in the water would settle toward the bottom. Peak
school size and density usually occurred between
0200 and dawn. Shortly after daybreak, most schools
would separate into smaller schools and rise off the
bottom. The schools would sometimes move over
deeper water while maintaining their nighttime
configuration.
Departures from the typical behavior patterns
have been reported. For example, while observing
widow rockfish schools over the continental shelf (not
aggregating around a seamount), Gunderson et al.7
noted a progressive offshore shift in the location of
the schools during one night. By sunrise most of the
schools were located near the edge of the shelf. Most
of these schools dispersed after dawn, but some re-
mained on the bottom in the area (in one case as late
as 1037 when observations were terminated). This
apparent shift may have been related to diurnal ver-
tical migration behavior (Pereyra et al. 1969).
METHODOLOGY DEVELOPMENT
(1980-81)
The methodology development was conducted by
7Gunderson, D. R., G. L. Thomas, P. Cullenberg, and R. E.
Thome 1981. Rockfish investigations off the coast of Washing-
ton and Oregon. Final report. Unpubl. manuscr., 45 p. Univ.
Wash., Fish. Res. Inst, FRI-UW-8125.
294
WILKINS: ABUNDANCE OF WIDOW ROCKFISH
. > ■ •*'■ ,
14
Figure 5— Echogram showing the typical configuration of widow rockfish schools at night (arrows).
Figure 6 -Echogram showing the configuration of "evening and morning" widow rockfish schools (arrows).
295
FISHERY BULLETIN: VOL. 84, NO. 2
Figure 7— Echogram showing the typical configuration of shortbelly rockfish schools (arrows).
Figure 8— Echogram showing configuration of Pacific whiting (W), redstripe rockfjsh (R), and shortbelly rockfish (S) schools.
296
WILKINS: ABUNDANCE OF WIDOW ROCKFISH
the University of Washington's Fishery Research In-
stitute (FRI) under contract with the NWAFC
(Gunderson et al. fn. 7, 8). The objectives of the work
were to evaluate the applicability of several resource
assessment techniques and refine the most prom-
ising approaches. In particular, it involved a compar-
ison of three methods of quantifying widow rockfish
abundance in small areas off southern Washington
and northern Oregon: conventional echo integration,
line transect survey theory (Burnham et al. 1980;
Seber 1980), and line intercept survey theory (Seber
1973, 1980).
Methods
This study involved three research cruises off
southern Washington and northern Oregon. Tables
2-4 present the dates of these cruises and specifica-
8Gunderson, D. R., G. L. Thomas, P. Cullenberg, D. M. Eggers,
and R. E. Thorna 1980. Rockfish investigations off the coast of
Washington. Annual report. Unpubl. manuscr., 68 p. Univ. Wash.,
Fish. Res. Inst., FRI-UW-8021.
tions of the vessels, fishing gear, and hydroacoustic
equipment employed. The field work entailed system-
atically transecting the survey areas, simultaneously
recording data from quantitative echo integration
equipment and sector scanning sonar. Data were col-
lected on the number of fish schools, their perpen-
dicular distance from the transect, their depth below
sea surface, the size and density of selected schools,
and the distribution of schools in relation to various
features of submarine topography. The echo integra-
tion system was used in a conventional manner to
obtain a measure of the density of fish within a
relatively narrow acoustic beam of 10°-11° directly
below the vessel (Fig. 9). Sector scanning sonar can-
not measure fish density, but by employing an ar-
ray of transducers radiating an acoustic signal over
a 200° x 9° semicircular wedge perpendicular to the
path of the vessel (Fig. 9), it can be used to count
schools within about 100-200 m to each side of the
vessel, measure their dimensions, and determine
their perpendicular distance from the transect. The
sonar's transducer array was aimed straight down-
ward for these studies. The entire wedge was
ECHOSOUNDER
SONAR
s
.
1
.
-
Editing of data
to include only
schools likely to be
widow rockfish.
Jl"""'\—>-ll
*
Within-school fish
density
Schools that were
also detected on
echo integration
system
Mean school
biomass estimate
(metric tons/school)
»
School height
*
School width
*
School length
'
'
Biomass
estimate
(t)
Area of survey
area (km2 )
i
Number of schools
sighted with sonar
School density
estimate
(schools/km2 )
Distance between school
center and transect
plane
Figure 9— Schematic diagram depicting the analysis of echo sounder and sonar data collected during hydroacoustic line transect surveys.
297
FISHERY BULLETIN: VOL. 84, NO. 2
displayed simultaneously on a 10-in diameter cathode
ray tube (CRT) screen which provided information
on the location and size of fish schools within its
200-400 m wide path (Fig. 10).
Data was collected electronically during the echo
integration and sonar surveys. Echo sounder return
signals were processed by an echo integrator capable
of measuring voltages in variable-sized depth inter-
vals. The echo integrator produced periodic printouts
of summed integrated voltage values which corre-
sponded to relative fish densities along the transect
in various depth intervals. Analog data (receiver out-
put voltages) were recorded onto magnetic tape as
a back-up procedure and for further processing. The
sonar CRT display screen was video-taped for play-
back and data reduction in the NWAFC laboratory.
Survey design of the 1980 and 1981 FRI studies
off southern Washington was generally similar,
though some aspects differed. In 1980, preselected
tracklines were run and were between lat. 46°20'N
and 46°48'N and between 55 and 183 m isobaths at
intervals of of 3.7 km. When a significant aggrega-
tion of fish was encountered, its bounds were deter-
mined by making several mapping runs perpen-
dicular to the main trackline. Trawling followed to
determine the species composition of the aggrega-
tion and to collect biological samples. Most of the
1980 work was done during daylight with the intent
of mapping and measuring yellowtail rockfish,
Sebastes flavidus, schools. After encountering
numerous widow rockfish schools at night, it became
apparent that this species' schooling behavior was
better suited for evaluating this methodology.
Thereafter, three nights were spent transecting a
smaller "widow rockfish subarea". Diel behavior and
distribution were examined by making several repeti-
tions of three selected tracklines. Near the end of
this cruise an area occupied by a dense aggregation
of widow rockfish schools was encountered. A short
nonrandom transect was run to obtain comparable
line intercept and line transect results.
In 1981, tracklines spaced every 3.7 km were
transected between the depths of 128 and 220 m off
northern Oregon between lat. 45°50'N and 46°18'N.
Figure 10.— Measurements and calculated dimensions of fish schools from videotaped sonar records.
298
WILKINS: ABUNDANCE OF WIDOW ROCKFISH
The same procedures were used as in 1980 except
that nearly all operations were conducted after dark
and no mapping runs were made to define the
bounds of school groups. A diel variability study was
conducted on 20 March 1981 between the hours of
0153 and 1037, consisting of 13 replicates of track-
line 21.
The conventional analysis of echo sounder data (in-
tegration) is based on the principle that the acoustic
intensity of a signal reflected from fish targets is pro-
portional to the density of fish in the region irradi-
ated by the echo sounder. Detailed descriptions of
the technique can be found in Moose and Ehrenberg
(1971), Forbes and Naaken (1972), and Thorne
(1977). During the 1980 and 1981 surveys, density
estimates from this method were obtained by aver-
aging returning acoustic signals over a series of
transmissions (25 transmissions over 12.5 s during
the Muir Milach cruise and 40 transmissions over
50 s during the Alaska and Chapman cruises). These
averages were then converted from relative to ab-
solute densities (kg/m2) for various depth intervals
using calibration data and a scaling factor based on
an average target strength of -35 dB/kg.9 Absolute
abundance (biomass) was estimated by extrapolating
absolute density estimates to the survey area.
Each survey area was systematically transected
using the echo sounder and sonar to search for fish
schools and, thereby, to derive line intercept and line
transect estimates of school abundance (schools/
km2). Data on school dimensions and density were
collected from those schools sighted. With the line
intercept method, only the presence of a school (as
detected by the echo sounder) and its width were
used to estimate school abundance. This technique
is based on the theory that, for systematically
located transects, the probability of intersecting
school i equals wJW, where w^ is the width of
school i and W is the distance between adjacent
transects. The number of schools per unit area {D)
can then be estimated by
0-1
y-i wjL
(Seber 1980)
where n
Wi
number of schools measured on a
transect of length L
width of jth school.
9The target strength value used in these analyses (-35 db/kg)
was not derived during work on widow rockfish. Since accurate
target strength estimation was not necessary for evaluating the
utility of the methodology, we used a value which had been esti-
mated for Pacific whiting (Dark et al. 1980) which has a similar
scattering cross section.
The line intercept method was applied only to data
collected from the nonrandom run made on the night
of 27-28 March 1980. The data from this line were
subdivided into two artificial transects of unequal
length and the jackknife method (Seber 1980) was
used to estimate D and its variance. This technique
is described fully by Gunderson et al. (fn. 8).
Line transect theory is based on the premise that
the probability of sighting a given object (or school)
is a function of its perpendicular distance from the
transect. A "detection function" is derived from
school sighting data which relates the probability of
a school being sighted to its distance from the
transect. This function is used to expand the number
of schools actually sighted to obtain an estimate of
school abundance. The advantage of this method is
that not all schools within sighting range need to
be detected in order to estimate the number of
schools in the area.
Using line transect estimation, the school abun-
dance (schools per unit area) was estimated by
D =
nf(0)
2L
n
L
/(0)
where D = estimated number of schools per unit
area
number of schools sighted
length of transect
"detection function'— a parameter
estimated from probability function
for the perpendicular distances off
transect of schools sighted.
The assumptions necessary for the use of this
method are
1) Schools directly on the transect plane will always
be sighted.
2) Schools are sighted in the position they occupied
prior to the approach of the vessel, i.e. there is
no avoidance of or attraction to the vessel.
3) Perpendicular distances off transect are mea-
sured precisely, particularly near the transect
plane
4) The detection function remains constant.
The computer program TRANSECT (Laake et al.
1979) was used to estimate the probability density
function of the perpendicular distance of schools
from the transect. The estimator model used is based
on a nonparametric Fourier series expansion fit to
data sets of observed perpendicular distances of
299
FISHERY BULLETIN: VOL. 84, NO. 2
schools off the transect plane Quinn (1979) and
Burnham et al. (1980) showed that this model is
robust and flexible and provides the best fit to the
detection function in most applications. This esti-
mator, at zero distance, is
1(0)
= ^ + £
w
k=\
%
where w* = truncation width, or the effective limit
of the range of detection, beyond
which all observations are discarded
and
<*fc
nw
Z. COS
1=1
knX;
w
(Burnham et al. 1980)
where n = number of schools observed
x{ = perpendicular distance off transect
for the ith school
k = term number = 1,2,3,. . .m [The num-
ber of terms (m) is determined by a
stopping rule in the computer pro-
gram TRANSECT].
TRANSECT also computes the school abundance
estimate D and its variance which is estimated by
the equation:
var 0) = (Df
var (n) var [/"(0)]
nc
Lf(0)]2
Dimensions measured directly included depth of
school from the surface, distance off bottom, width,
thickness, radial distance from vessel, and bearing
to the right or left of a vertical line below the vessel
(Fig. 10). The perpendicular distance of the school
from the vertical plane of the vessel's path ("distance
off transect") was calculated from the radial distance
and bearing. All distances were measured or cal-
culated to the apparent geometric center of each
school (Burnham et al. 1980). The length of each
school was calculated from the product of vessel
speed and the duration that the school was being
detected by the sonar, and was corrected to account
for the variable sonar beam width parallel to the
vessel's path due to depth.
The biomass of individual schools was estimated
by the formula
h% = ti l{ w% di
where bt = estimated biomass of school i
t{ = average thickness of school i, top to
bottom (echo sounder data)
l{ = length of school i, parallel to transect
(sonar data)
w{ = average width of school i perpendicular
to transect plane (sonar data)
di = mean integration density for school i
(g/m3) assuming a target strength of
-35 dB/kg (see footnote 9) (echo
sounder data).
The mean school biomass (MSB) was estimated from
the individual school biomass estimates; its variance
was determined from
Mean school biomass estimates were derived from
density information (from echo sounder data), school
dimension information (from sonar data), and an
assumed target strength of -35 dB/kg. These esti-
mates were used in the line transect and line inter-
cept analyses. All information on schools detected
by the hydroacoustic systems was edited to discrim-
inate widow rockfish from other species using judg-
ments based on school form, density, location, and
test trawl records. Data on each school identified as
widow rockfish were then integrated to obtain mean
within-school density. The CRT display of the sec-
tor scanning sonar provided representations of the
size, shape, and position of fish schools within its
range of detection. The dimensions of all schools
identified as widow rockfish were measured on the
screen of a video monitor using the slow motion and
freezeframe features of the video recorder-player.
" (b, - MSB)2
var (MSB) = 2. —
v ; i-i N(N-1)
where N = number of schools averaged for MSB.
Total biomass estimates from the line transect and
line intercept methods were calculated for each
survey area using the formula
B = AD (MSB)
where B = estimated total biomass for the survey
area, and
A = total area (km2) of the survey area.
The variance of these estimates was determined
from
300
WILKINS: ABUNDANCE OF WIDOW ROCKFISH
var B = A2 [(D)2 var(MSB) + (MSB)2 var0)
- var (MSB) var 0)] (Goodman) 1960)
Results
Twenty one trawl hauls were made during the 1980
FRI survey aboard the Muir Milach; 6 with bottom
gear and 15 with midwater gear. Widow rockfish
were caught only in midwater hauls and comprised
99% of those catches. The most abundant species in
the bottom tows were spiny dogfish, Squalus acan-
thias, and black rockfish, Sebastes melanops. The
acoustic survey consisted of 22 systematic transects
covering about 550 km and employed sonar and echo
integration equipment. Twenty six schools were
sighted and measured to provide data for a line
transect estimate of school abundance. During the
nonrandom transect run on the night of 27-28 March
1980, 73 schools were sighted and measured for use
in developing line transect and line intercept esti-
mates of school abundance in a small subarea.
Only four trawl hauls were attempted during the
1981 FRI survey due to severe gear damage. Red-
stripe rockfish, Sebastes proriger, comprised 90% or
more of the two catches which contained fish (one
midwater haul and one bottom haul). The midwater
haul was made quite close to bottom near midnight
and contained small quantities of sharpchin rockfish,
Sebastes zacentrus; widow rockfish; and greenstriped
rockfish, S. elongatus, suggesting an association of
these species in nearbottom schools at night. Fifteen
systematic transects were covered during this survey
(about 400 km) during which 49 schools were sighted
and measured. One of the transects was replicated
13 times during one night to observe the behavior
of a group of schools over the continental shelf just
south of the Columbia River. These schools were not
gathered around a prominent bottom feature As the
night progressed they moved deeper and further off-
shore, reaching the shelf break about sunrise After
sunrise most of the schools dispersed, though some
remained on bottom at least until observations
ceased at 1037 (Gunderson et al. fn. 7).
During the 1981 NMFS cruise, quantitative hydro-
acoustic data were collected from 21 transects on
the Nelson Island, The Fingers, Heceta Bank, and
Cape Blanco grounds (Fig. 1, Table 5) using echo
integration (Thomas et al. fn. 5). The searchlight-
beam sonar available on the Chapman was inade-
quate to identify school types or provide estimates
of school density. This is because it employed only
a single transducer programmed to sweep back and
forth and did not provide continuous coverage of the
area within its range Therefore, all density and
biomass figures for this survey refer to total nekton
rather than widow rockfish.
Table 5.— The mean fish and nekton density (g/m2) and biomass (metric tons) by location, date, and
transect estimated by a conventional echo integration survey performed aboard the NOAA RV Chap-
man, 21-26 April 1981 .1
Transect
Mean
Trans-
length
density
Var
Area
Biomass
Var
Location
Date
sect
(km)
Density
D
D
(km2)
B
B
Crater
4/21
1
18.56
1.78
4/22
2
17.11
5.86
2.82
2.45
228.87
646
1.28 x
10s
4/22
3
15.02
0.66
Cape Blanco
4/23
4/23
4/23
4
5
6
4.19
4.35
4.67
16.17
26.22
4.50
4/23
7
5.32
1.12
6.47
11.31
200.81
1,301
4.56 x
10s
4/23
8
6.11
1.79
4/24
9
2.44
1.63
4/24
10
3.87
0.34
4/24
11
3.87
0.06
Heceta Bank
4/24
12
17.59
4.67
4/25
13
18.37
0.12
4.89
9.44
87.15
427
7.17 x
104
4/25
14
15.30
10.88
The Fingers
4/25
15
14.74
1.78
4/25
16
14.74
1.01
1.73
0.19
75.11
130
1.07 x
103
4/25
17
12.22
2.54
Crater
4/26
18
5.57
0.00
4/26
19
6.96
0.00
1.79
2.83
34.78
62
3.43 x
103
4/26
20
6.28
6.75
4/26
21
5.63
0.26
1Thomas, G. L, C. Rose, and D. R. Gunderson. 1981. Rockfish investigations off the Oregon coast, annual
report. Unpubl. manuscr, 20 p. Univ. Wash., Fish. Res. Inst. FRI-UW-8119.
301
FISHERY BULLETIN: VOL. 84, NO. 2
The results of echo integration, line intercept, and
line transect analyses were compared using data col-
lected during the 1980 and 1981 FRI cruises
(Gunderson et al. fn. 7, 8). Large differences were
seen between echo integration and line transect
estimates in a situation where schools were relatively
small and scarce (1980 transect data, Table 6). The
principal reason for this is that the threshold echo
voltage required to trigger the sonar CRT display
was higher than that needed to detect a school on
the echo integration system, so many of the sparser
schools detected by the echo sounder were not
detected with the sonar. In situations where schools
were larger and more plentiful (1980 nonrandom
runs and 1981 transects) all three methods produced
similar estimates. The precision of abundance
estimates generated by line transect and line inter-
cept methods is usually comparable to that of con-
ventional echo integration methods and can exceed
it in some cases (Gunderson et al. fn. 7). The major
factors which led us to concentrate our efforts on
line transect surveys were the ability to cover large
areas rapidly and the ability to expand the number
of schools sighted by a detection function, yielding
more accurate estimates of school abundance.
APPLICATION OF
ASSESSMENT METHODOLOGY
By 1982 the aforementioned studies had provided
a foundation of information on which to expand
developmental research. The behavioral observations
suggested that widow rockfish aggregations were
most stable and susceptible to assessment during the
night. Line transect estimation of school abundance
through the use of sonar and echo integration equip-
ment was found to be the most effective of the tech-
niques compared, especially when school abundance
was likely to be low. The next step in the project was
to evaluate the feasibility of applying the line
transect survey method in a comprehensive survey
to assess and monitor widow rockfish stocks.
Methods
The trawler Ocean Leader was chartered to survey
five areas off Oregon (Fig. 1) where widow rockfish
had been caught consistently between 1980 and
1982. Specifications of the vessel, fishing gear, and
hydroacoustic equipment used appear in Tables 2-4.
The proximity of alternative grounds was important
for the success of the survey, should widow rockfish
not be found in one or more of the areas. At each
of the grounds the survey procedure was as follows:
1) The ground was systematically surveyed with
hydroacoustic equipment during the night to
determine whether fish schools were in the area.
The locations of schools suspected to be composed
of widow rockfish, or species likely to be confused
with widow rockfish, were noted. The final bound-
aries of the study area were then delineated.
2) The study area was surveyed at night along
parallel tracklines about 1 km apart using the line
transect survey technique The tracklines were
replicated as many times as practical throughout
Table 6.— Summary of estimates of school abundance (D), mean school biomass (MSB),
and total biomass (6) for widow rockfish. Coefficients of variation (CV) are given for each
estimate.1
D
(schools/
MSB
No. Of
B
nm2)
CV
(t)
schools
CV
(t)
CV
1980
Transect data
26 schools, 2 transects
Line transect estimate
69.5
0.84
0.12
15
0.20
204
0.84
Echo integration estimate
778
0.16
Nonrandom run data
73 schools, 1 transect
Line transect estimate
242.2
0.19
0.85
16
0.50
5,003
0.53
Line intercept estimate
248.9
0.10
0.85
16
0.50
5,139
0.51
Echo integration estimate
6,453
—
1981
Transect data
29 schools, 3 transects
Line transect estimate
12.1
0.24
0.62
27
0.33
342
0.40
Echo integration estimate
342
0.77
'Gunderson, D. R., G. L. Thomas, P. Cullenberg, and R. E. Thorne. 1981. Rockfish investigations
off the coast of Washington and Oregon. Final report. Unpubl. manuscr, 45 p. Univ. Wash., Fish.
Res. Inst. FRI-UW-8125.
302
WILKINS: ABUNDANCE OF WIDOW ROCKFISH
the night to provide information on variability of
abundance and distribution within a given night.
Selected study areas were again surveyed after
an interlude of several days to study variability
over longer periods.
3) Fish aggregations noted during transecting were
sampled with midwater trawls for species iden-
tification. This was done on alternate nights so
as not to impede the progress of the acoustic
assessment portion of the survey. Biological data
(eg, size composition, maturity, stomach con-
tents) were collected from widow rockfish in the
catches.
Results
About 725 km of transects were covered in the five
study areas during the 12 nights of hydroacoustic
data collection. Ten midwater trawl hauls were made
to identify species present in various schools. Widow
rockfish schools were seen in all areas, but were
sparse on the Cape Blanco, Heceta Bank, and The
Fingers grounds. The Halibut Hill ground, only
recently exploited, contained the highest density of
widow rockfish schools and also the largest average
school size After editing videotaped sonar records,
127 schools were identified as widow rockfish; data
from 37 of these were integrated on the echo sounder
system and used to calculate school biomass esti-
mates. Ideally, a mean school biomass would have
been derived for each ground, but because few
schools were observed there, school biomass
estimates were pooled and averaged for the Nelson
Island, The Fingers, and Heceta Bank grounds. No
measurable widow rockfish schools were seen dur-
ing surveys of the Cape Blanco ground. School abun-
dance was estimated for each area by treating each
pass through the area as a replicate and pooling data
from all replicates within the area. School abundance
(excepting Cape Blanco) ranged from 0.6035 schools/
km2 on The Fingers ground to 1.4810 schools/km2
on the Halibut Hill ground. Area biomass estimates
are summarized in Table 7. The total estimated
biomass for the five survey areas was about 830 t;
50% at Halibut Hill ground, 30% at Heceta Bank,
11% at The Fingers, and 9% at Nelson Island.
Sampling was concentrated on the Halibut Hill
ground, where widow rockfish schools were largest
and most plentiful, in order to investigate the diel
and night-to-night variability in school abundance
The survey of this ground was repeated seven times;
three times each night on 26-27 March and 31
March-1 April and once on 30 March. Separate
sighting functions for each night were estimated by
pooling observations. Corresponding school abun-
dance and mean school biomass estimates were then
calculated for each night. School abundance ranged
from 0.39 schools/km2 on 26-27 March to 4.50
schools/km2 on 30 March. Mean school biomass
tended to decline as school abundance increased,
however, so biomass estimates for each of the sam-
pling periods changed less than either school abun-
dance or mean school biomass (Table 8). It was not
possible to analyze the Halibut Hill data on a
replicate-by-replicate basis because few schools were
sighted during any single replicate The number of
sightings per replicate ranged from 4 to 34. Burn-
ham et al. (1980) cautioned that such stratification
procedures for line transect surveys should be
"severely limited to those few surveys where the
number of objects seen on replicate lines is fairly
large (perhaps at least in the 20 to 30 range)".
Table 7— Summary of estimates of school abundance (D), mean school biomass (MSB), and
biomass (fl) in each of four study areas covered during the 1982 widow rockfish assessment
feasibility survey.
Study area
, D
schools
km2 j
Var0)
MSB
Area B
school / Var(M$8 (km2) (t) Var(£)
CV(6)
[Var(g)]1/2
6
Heceta Bank 0.9490 0.0305 1.968 0.656 68.60 245.76 6,758.37 0.335
(6 schools)
The Fingers 0.6035 0.0711 6.409 5.486 40.47 92.20 2,212.03 0.510
(4 schools)
Nelson Island 0.7587 0.3010 3.924 9.514 27.44 78.59 3,467.75 0.749
(2 schools)
3 above areas
pooled1 3.775 1.151
Halibut Hill 1.4810 0.2028 9.639 21.668 28.81411.27 51,758.47 0.553
(25 schools)
'School biomass data from Heceta, The Fingers, and Nelson Island were pooled to provide a mean school
biomass which was used to calculate total biomass in each area.
303
FISHERY BULLETIN: VOL. 84, NO. 2
Table 8.— Summary of estimates of school abundance (D), mean school biomass (MSB), and biomass (8) of widow
rockfish on the Halibut Hill ground during replicates on 26-27 March, 30 March, and 31 March-1 April 1982.
Sampling
period
No. of
repli-
cates
No. of
schools
sighted/
replicate
schools |
km2 /
Var(D)
MSB
t
Area
Var(MSB) (km2)
B
(t)
Var(8)
CV(B)
[Var(B)]1'2
school
B
26-27 March
3
9
14
13
0.394
0.1264
21.674 153.878 28.81
MSB based on 8. schools)
245.96
52,852.69
0.935
30 March
1
34
4.499
0.8908
0.729 0.160 28.81
MSB based on 7 schools)
94.49
2,962.75
0.576
31 March-
3
9
1.325
0.1687
0.935 0.088 28.81
35.69
238.52
0.433
1 April
11
11
MSB based on 9 schools)
Variations in the pattern of school abundance over
the course of a night were common. Echograms
recorded during the seven replicates of one transect
on the Halibut Hill ground (Fig. 11) illustrate one
case when abundance was high early in the night
and decreased toward dawn (26-27 March). The op-
posite trend of low abundance increasing toward
dawn is illustrated (31 March-1 April) in the same
figure.
DISCUSSION
The objectives of this 3-yr project were to study
the schooling behavior of widow rockfish to provide
the background needed to design effective abun-
dance estimating surveys; then to develop an appro-
priate survey methodology for the species; and,
finally, to test the feasibility of implementing such
a survey. Substantial progress was made toward
satisfying these objectives. The studies of widow
rockfish habits and distribution have provided a base
for designing surveys which cover its range and pro-
duce the best likelihood of encountering the ex-
ploitable population at a time when it will be most
available
Understanding the schooling and dispersal be-
havior of widow rockfish was important to develop
an appropriate survey approach for estimating abun-
dance The nighttime aggregations which are the
targets of the commercial fishery tend to disperse
about daybreak, perhaps scattering throughout the
water column or seeking shelter near the bottom.
If the latter had been the case, more conventional
survey methods (i.e, bottom trawl or conventional
echo integration surveys) might have been more
appropriate
Although daytime concentrations of widow rock-
fish were observed, bottom trawl catches during the
1980 and 1981 surveys showed that this species is
relatively unavailable to bottom trawls in an area
where widow rockfish are known to aggregate at
night.10 This is substantiated by low incidences of
widow rockfish in catches of other bottom trawl
surveys during periods when midwater trawlers were
making large landings. Consequently, when mid-
water schools disappear during the day, it is unlike-
ly that they disperse along the bottom. In recent
years, skippers of midwater trawlers have com-
mented that widow rockfish are becoming more
evasive and dive below their nets to avoid capture
Some skippers have taken advantage of this behavior
by purposely driving the schools toward bottom with
engine noise where they capture them with bottom
trawls equipped with roller gear. Although these are
classified as bottom trawl landings, the fishermen
are, in a sense, capturing midwater schools. Fisher-
men have also reported encountering daytime aggre-
gations of this species over the continental slope in
waters deeper than they are usually found at night
(>500 m) and some have been able to catch them on
or near the bottom during the day. Thus the distribu-
tion of widow rockfish relative to the sea bottom is
quite unpredictable during the daytime These
schools are also not as large as those that occur at
night. The appropriate time to survey this resource
thus appeared to be at night. The line transect survey
method, adapted for use with sector scanning sonar
and echo integration equipment, was chosen over
conventional echo integration and the line intercept
method because of its ability to survey areas more
quickly and thoroughly.
Application of the method exposed several
problems affecting the precision and accuracy of the
abundance estimates. The estimation of school abun-
dance was hampered primarily by limitations of the
sonar equipment and by small samples. We were not
'"Observations of midwater echosign and landing information
from commercial vessels fishing in the area confirmed that the
usual dense midwater widow rockfish aggregations were present
in the area at night during the 1981 bottom trawl survey.
304
WILKINS: ABUNDANCE OF WIDOW ROCKFISH
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305
FISHERY BULLETIN: VOL. 84, NO. 2
able to calibrate the sonar systems so that the sensi-
tivity of all transducers in the array were equal.
Hence, the probability of detecting a given school
in one sector of the sonar display was not necessarily
the same as detecting it at an equal distance in
another sector. The inability to calibrate the trans-
ducers may have compromised our ability to detect
all schools directly below the transect. This is the
most important assumption of line transect surveys;
school abundance estimates will be biased downward
if it is violated. Intercalibration of the transducers
would also help establish a more accurate detection
function which would apply throughout the sonar's
range
The limited lateral resolution of sector scanning
sonar hampers the accurate measurement of school
width, an important value for determining mean
school biomass. Each transducer in the fan-shaped
array acts as an independent echo sounder and if
any portion of a school enters the radiation pattern,
the entire width of the 9° -10° sector sampled by that
beam will be displayed as a reflective target (Fig. 12).
This results in an overestimation of school width and
a distortion of the school's size and location, yield-
ing overestimates of biomass and inaccurate
measures of distance from the transect plane The
detection function will be altered by these inac-
curacies and may modify estimates of school abun-
dance depending on the magnitude and the direc-
tion of the errors. The distortion may be aggravated
by interference of side lobes in the directivity pat-
tern of individual transducer beams (Fig. 13). Even
these lower power lobes can produce echo signals if
very dense targets are encountered and may inter-
fere with the acoustic signals from adjacent trans-
ducers.
Another weakness of sector scanning sonar in this
application is insufficient detection sensitivity. This
weakness became apparent during calculations of
the lengths of individual schools. Lengths were cal-
culated twice for each school, once based on echo
sounder data and again based on sonar data. The
theoretically correct method would employ the sonar
data because schools could be detected further to
each side of the vessel. The echo sounder could only
detect the portion of the school within the 10° -11°
beam directly below the vessel. Consequently, if a
large part of the school was outside the beam, its
length was underestimated. In practice however, the
length estimates based on sonar detections were
usually shorter than those based on echo sounder
data (Table 9) due to the lower sensitivity of the sonar
system. The sonar-based lengths were chosen, how-
ever, because they measured the dimensions of the
part of the school having densities above the thres-
hold required to trigger the sonar. This is probably
Segment covered by
one element in sonar
transducer array
True school center
Apparent school
center
Apparent location of school
as seen on the sonar display
True location of school
Figure 12— A facsimile of the sector scanning sonar output display exemplifying biases in apparent school loca-
tions resulting from the limited resolution of the instrument.
306
WILKINS: ABUNDANCE OF WIDOW ROCKFISH
•?0°
3dB ?°°
Half-power point
roc
YOo
Figure 13— The theoretical directivity pattern of one transducer element of the sector scanning sonar show-
ing side lobes which may interfere with the signals received by adjacent transducers.
a more proportional measurement of school length
than the echo sounder-based lengths. The accuracy
of school dimension measurements could be im-
proved by using more sensitive and specialized sonar
equipment.
These problems with the limitations of sector scan-
ning sonar should not be difficult to overcome More
sensitive quantitative sonar equipment is now avail-
able or relatively easy to develop. Lateral resolution
may remain a problem because of the difficulty and
expense of producing narrow-beam transducers, but
the errors it causes are relatively unimportant.
The accuracy of mean school biomass estimates
would be improved by target strength studies specific
to widow rockfish. Calculation of average fish den-
sity within each school was relatively straight-
forward but involved assuming a target strength of
-35 dB/kg. Ideally, the target strength should be
calculated specifically for widow rockfish but such
specialized work was beyond the scope of this
study.
The ability to distinguish widow rockfish schools
from those of other species using hydroacoustic
equipment is an important element of this tech-
nique Through these studies, our ability to correct-
ly identify widow rockfish echo sign has been im-
proved. The accuracy of species identification varies
depending on the nature of the species complex in
the survey area. Where shortbelly and redstripe
rockfish are present, the potential for misidentifica-
tion increases. Technological improvements in sonar
equipment may help to reduce this problem. The
density of a school is an important criterion for
distinguishing widow rockfish from other species and
newer sonar equipment includes density-graded color
video displays. Other techniques, such as underwater
photography or remote video camera vehicles, might
also improve our ability to identify species. I believe,
however, that test fishing will always be a necessary
component of hydroacoustic resource assessment
surveys.
Surveys of widow rockfish resources must be
designed with the behavior and distributional vari-
ability of the species in mind. The diel behavior of
the species indicates that the most effective sampling
period is at night, but even then unpredictable be-
havior places special demands on survey design.
Observations from hydroacoustic transects which
were replicated on several nights (Fig. 11) show that
long-term variability in abundance (eg, night-to-
night or week-to-week) is even more marked than
that over a shorter time These results are substan-
tiated by other surveys (see footnotes 5, 7, and 8)
and illustrate the difficulty of estimating widow
rockfish abundance Long-term variability is also a
factor in area-swept bottom trawl surveys. The
307
FISHERY BULLETIN: VOL. 84, NO. 2
Table 9.— Comparison of school length measurements
(m) derived from echo sounder versus sector-scanning
sonar data collected aboard the FV Ocean Leader, 14
March-7 April 1982.
Density
(kg/m2)
Length from
Length from
School
echo sounder
sonar
1
0.1292
48.5
45.0
2
0.0265
85.8
2.1
3
1 .4860
66.2
5.8
4
1.6996
51.8
19.2
5
0.6374
37.4
74.0
6
0.3559
37.4
79.6
7
1.2415
59.9
52.3
8
0.7513
93.2
66.5
9
0.2119
117.5
118.1
10
0.7567
81.9
236.2
11
0.0686
526.9
497.5
12
0.0453
45.0
31.9
13
0.0490
96.9
353.1
14
0.0068
138.0
18.7
15
1.1400
511.9
393.2
16
0.6089
189.7
64.2
17
0.3055
76.6
18.4
18
0.4564
84.6
70.6
19
0.2154
27.8
93.0
20
0.0080
62.5
116.6
21
0.0487
103.0
16.9
22
0.1057
130.3
49.3
23
0.0936
147.5
28.5
24
0.1730
27.4
9.9
25
0.0103
46.8
39.6
26
0.1262
53.6
40.9
27
0.0182
67.7
43.9
28
0.1013
30.1
124.9
29
0.0830
67.7
84.2
30
0.0430
67.7
189.4
31
0.0208
48.9
33.5
32
0.0117
23.8
41.4
33
0.0128
22.4
14.8
34
0.1808
106.4
50.2
35
0.1809
292.2
216.7
36
0.0424
81.0
66.4
37
3.3097
158.3
101.6
x 0.3990
105.8
94.8
s 0.6587
113.5
112.2
assumption is that the variability has a strong ran-
dom component and catch per unit effort values are
consequently unbiased. The same situation may well
be true here, in which case an important component
of the survey design would be multiple replication
to obtain good estimates of both long- and short-term
variance
Burnham et al. (1980) reported that good results
from line transect surveys require observation of a
minimum of about 40 objects per replicate Fitting
the observed perpendicular sighting distances to a
detection function becomes less reliable with a
smaller number of objects. Widow rockfish abun-
dance is now low on all major grounds and the
recommended minimum number of schools was not
observed during any single replicate in the 1982
survey, but by pooling replicates a sufficient data-
base was constructed. Sample sizes could be in-
creased through more intense sampling. A time-
stratified analysis of the data would be desirable
to define within-night variability, but this would
place even further demands on a sampling pro-
gram.
Surveys of the type used for widow rockfish must
cover the geographic range of the species of interest
more thoroughly than most other survey methods.
The dynamic behavior of widow rockfish suggests
that the survey method should cover large areas in
a relatively short time in order to survey a given
fishing ground at least once during the night. Be-
cause of day-to-day variability, surveys should include
sampling each area during several nights over a 1-
or 2-wk period. Most areas containing fishable widow
rockfish concentrations have probably been iden-
tified and there are a limited number of these
grounds (probably 12-20); nearly all are character-
ized by ridges or rises on the outer continental shelf
or upper slope and are relatively small in area. In-
tensive sampling of widow rockfish, therefore, is
more feasible than for most other groundfish species
inhabiting less well-defined areas.
Because widow rockfish schools are continually
forming and breaking up, there may be a significant
portion of the population which is not schooling at
any given time and is therefore not susceptible to
these survey techniques. This project did not answer
whether this is so, but nothing was found to suggest
that widow rockfish are significantly detectable by
trawl or hydroacoustic surveys in any form other
than midwater schools. Until more is learned about
the proportion of the stock occurring as schools,
surveys must be considered as yielding minimum
biomass estimates. Clark and Mangel (1979) pro-
posed a study of rates of school formation and disper-
sal to explain and evaluate a similar relationship be-
tween overall stock size and the proportion of a
yellowfin tuna stock occurring as schools. Such a
technique should receive further consideration in this
situation, but present low widow rockfish school
abundance (schools/km2) and lack of a consistent
pattern of school formation and dispersal would
probably make its application in widow rockfish
assessment difficult. This question is analogous to
that of defining catchability coefficients (i.a, what
proportion of those fish in the path of a net are ac-
tually captured) for quantitative trawl surveys.
Changes in relative abundance can be monitored by
such surveys without knowing the catchability if one
assumes that the available proportion of the popula-
tion is constant.
Results of other analyses of widow rockfish be-
308
WILKINS: ABUNDANCE OF WIDOW ROCKFISH
havior and stock size should be used to evaluate
survey methodology. The groundfish management
team of the Pacific Fisheries Management Council
(see footnotes 2 and 3) used stock reduction and
cohort analyses to estimate the abundance of this
species. In an area comparable to our 1982 survey
area, the widow rockfish biomass was estimated to
be 21,664 t at the begining of 1982. This estimate
is based in part on commercial landing information
and, consequently, the definition of the grounds to
which it applies is somewhat vague. The fishery-
based estimates are much higher than those derived
from the 1982 survey data (about 830 1). The relative-
ly low sensitivity of the sonar systems used would
result in underestimating biomass and is undoubted-
ly responsible for much of this difference The
discrepancy is also partly due to the fact that our
survey methods only estimate the portion of the
stock present as detectable schools and are therefore
a measure of relative, rather then absolute, abun-
dance. This is true to some extent for most types
of surveys.
Innovations are also needed to resolve the techni-
cal problems related to data collection, identification
of school species composition, and survey design.
Some suggestions include
1) a two-vessel survey to improve the efficiency of
data collection— such a technique would separate the
chore of delineating areas of widow rockfish ag-
gregations, estimating school abundance, and test
fishing from that of estimating mean school biomass
(Gunderson et al. fn. 7);
2) a means of recording a time base on both the
audio and video tape records of the echo sounder
and sonar to simplify finding the same school on
each system for school dimension measurements;
and
3) a method of estimating all school dimensions
and the density within the school from a single data
collection system— this would entail development of
a sophisticated, quantitative sonar-integration sys-
tem with the capability of recording the output onto
videotape (Ehrenberg 1979).
Such refinements could probably be implemented
with relative ease. The methodology should be re-
evaluated when these technological and sampling
improvements have been made. Widow rockfish
management could have been significantly improved
with the knowledge of stock size from an effective
resource assessment survey. There are also other
species which exhibit similar behavior and which,
although presently unexploited, need to be assessed
(eg, shortbelly, redstripe, and black rockfish). This
methodology could probably be easily adapted for
surveying these resources.
CONCLUSIONS
Based on the results of research conducted dur-
ing this project, the line transect survey method
using a sector scanning sonar and a quantitative
echo sounder appears to be the best means of assess-
ing widow rockfish abundance with research surveys.
A weakness of this method is that it only measures
the portion of the population existent as distinguish-
able schools and that portion may be quite variable
It also relies heavily on subjective experience for
identifying the species composition of schools. Its
strengths are that large areas can be covered quickly
and it is not necessary that all schools within sighting
range be detected in order to estimate school abun-
dance It appears that this could be a useful assess-
ment method for widow rockfish and for several
other Pacific coast groundfish species which are not
yet being seriously exploited. The effectiveness of
the technique could be enhanced by employing or
developing more sensitive and specialized quan-
titative sonars and by improving the methods of data
collection. The technological and survey design prob-
lems encountered should be relatively easy, though
somewhat costly, to resolve The method should then
be reevaluated to determine its utility. As the tech-
nique is used, scientists will gain a better under-
standing of the behavior and habits of the target
species.
ACKNOWLEDGMENTS
The work described in the developmental section
was ably conducted by Donald R. Gunderson and
Gary L. Thomas and their associates at the Fisheries
Research Institute, University of Washington Col-
lege of Fisheries, Seattle, WA, under contract to the
National Marine Fisheries Service (contract no. 79-
ABC-00203). Much of the information presented in
that section is extracted from their contract reports.
The hydroacoustic expertise during the 1982 survey
work was provided by the Pelagic Resources Assess-
ment Task of the Resource Assessment and Conser-
vation Engineering (RACE) Division, Northwest and
Alaska Fisheries Center, NMFS; in particular, Ed-
mund Nunnallee, Jimmie J. Traynor, and John Gar-
rison. I am expecially grateful to Nunnallee for
advice and guidance during the analysis of echo
sounder and sonar data. I also wish to thank Thomas
A. Dark, RACE Division, and Nunnallee and Traynor
309
for their thoughtful and constructive review of this
manuscript.
LITERATURE CITED
Burnham, K. P., D. R. Anderson, and J. L. Laake.
1980. Estimation of density from line transect sampling of
biological populations. Wildl. Monogr. 72, 202 p.
Clark, C. W., and M. Mangel.
1979. Aggregation and fishery dynamics: a theoretical study
of schooling and the purse seine tuna fisheries. Fish. Bull.,
U.S. 77:317-337.
Dark, T. A., M. 0. Nelson, J. J. Traynor, and E. P. Nunnallee.
1980. The distribution, abundance and biological character-
istics of Pacific whiting, Merluccius productus, in the Cali-
fornia-British Columbia region during July-September 1977.
Mar. Fish. Rev. 42(3-4): 17-33.
Ehrenberg, J. E.
1979. The potential of the sector-scanning sonar for in situ
measurements of fish target strengths. In Proceedings of
the 1979 Institute of Acoustics Meeting on sector scanning
sonars. Lowestoft, England.
Forbes, S. T., and 0. Nakken (editors).
1972. Manual of methods for fisheries resource survey and
appraisal. Part 2. The use of acoustic instruments for fish
detection and abundance estimation. FAO Man. Fish. Sci.
5, 138 p.
Goodman, L. A.
1960. On the exact variance of products. J. Am. Stat. Assoc
55:708-713.
Hitz, C. R.
1962. Seasons of birth of rockfish (Sebastes spp.) in Oregon
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coastal waters. Trans. Am. Fish. Soc. 91:231-233.
Kimura, D. K., and J. V. Tagart.
1982. Stock reduction analysis, another solution to the catch
equation. Can. J. Fish. Aquat. Sci. 39:1467-1472.
Laake, J. L., K. P. Burnham, and D. R. Anderson.
1979. User's manual for program TRANSECT. Utah State
Univ. Press, Logan, 26 p.
Moose, P. H., and J. E. Ehrenberg.
1971. An expression for the variance of abundance estimates
using a fish echo integrator. J. Fish. Res. Board Can. 28:
1293-1301.
Pereyra, W. T, W. G. Pearcy, and F. E. Carve y, Jr.
1969. Sabastodes Jlavidus, a shelf rockfish feeding on meso-
pelagic fauna, with consideration of the ecological implica-
tions. J. Fish. Res. Board Can. 26:2211-2215.
Phillips, J. B.
1964. Life history studies on ten species of rockfish (genus
Sabastodes). Calif. Dep. Fish Game, Fish Bull. 126, 70 p.
Quinn, T. J., II.
1979. The effects of school structure on line transect estima-
tors of abundance In G. P. Patil and M. L. Rosenzweig
(editors), Contemporary quantitative ecology and related
ecometrics, p. 473-491. Int. Coop. Publ. House, Fairland,
MD.
Seber, G. A. F.
1973. The estimation of animal abundance and related param-
eters. Hafner Press, N.Y., 506 p.
1980. Some recent advances in the estimation of animal abun-
dance Univ. Wash., Wash. Sea Grant Tech. Rep. 80-1, 101 p.
Thorne, R. E.
1977. A new digital hydroacoustic data processor and some
observations on herring in Alaska. J. Fish. Res. Board Can.
34:2288-2294.
310
POPULATION AND FISHERY CHARACTERISTICS OF
GULF MENHADEN, BREVOORTIA PATRONUS
Walter R. Nelson1 and Dean W. Ahrenholz2
ABSTRACT
Landing data from 1964 to 1978 for the purse seine fishery in the north-central Gulf of Mexico for gulf
menhaden, Brevoortia patronus, were analyzed to determine growth rate, yield-per-recruit and spawner-
recruit relationships, and maximum sustainable yield (MSY). Estimates of stock size, year-class size, and
rates of fishing were obtained from cohort analysis. The fishery is characterized by high rates of both
fishing and natural mortality. During the period studied, an average of 40% of the population of age-1
and older fish were taken by the fishery and 47% was lost to other causes annually. Although there was
substantial scatter about the fitted curve, a Ricker-type spawner-recruit relationship was found to be
suitable The number of age-1 recruits fluctuated annually between 7.5 and 25.4 billion during the period
studied. Maximum biomass of a year class is reached at an age of about 1.5 years. Yield-per-recruit estimates
were obtained for an array of fishing mortalities and ages of entry. A deterministic simulation model
incorporating growth, the spawner-recruit relationship, and age-specific rates of fishing provided an
estimate of MSY at 585,118 t with 127% of the current mean rate of fishing. Implications for the current
and future status of this fishery are discussed.
Gulf menhaden, Brevoortia patronus, are filter-feed-
ing, surface-schooling clupeids that are subjected to
an intensive purse seine fishery in the northern Gulf
of Mexico. Although annual landings have fluc-
tuated, there has been a general increase since the
inception of the modern fishery in 1946 to a high
of 820,000 metric tons (t) in 1978. The fishery con-
sists of about 80 refrigerated vessels serving 11
reduction plants at 6 ports in Mississippi and Loui-
siana. The fishing season is currently set by State
law from mid-April to mid-October. Although a
majority of the catch is taken off Louisiana and
Mississippi, vessels range west into eastern Texas
coastal waters and east to the coastal waters of the
Florida panhandle Vessels, aided by spotter aircraft,
land from 6,000 to 10,000 t/6-mo fishing season. Ex-
cellent background information and descriptions of
the fishery have been published by Christmas and
Etzold (1977) and Nicholson (1978).
Considerable literature exists on the general
biology of gulf menhaden (Reintjes et al. 1960; Rein-
tjes 1964; Reintjes and Keney 1975; Christmas and
Etzold 1977); however, information is scarce on the
population dynamics of gulf menhaden and on the
dynamics and impact of the fishery. Chapoton (1972)
'Southeast Fisheries Center Beaufort Laboratory, National
Marine Fisheries Service, NOAA, Beaufort, NC; present address:
Southeast Fisheries Center Miami Laboratory, National Marine
Fisheries Service, NOAA, 75 Virginia Beach Drive, Miami, FL
33149.
Southeast Fisheries Center Beaufort Laboratory, National
Marine Fisheries Service, NOAA, Beaufort, NC 28516-9722.
and Schaaf (1975a) estimated maximum sustainable
yield (MSY). Ahrenholz (1981) described recruitment
patterns and estimated natural and fishing mortality
rates from returns of tagged juvenile and adult
menhaden.
Gulf menhaden have a life history similar to many
other estuarine-dependent coastal species. Spawn-
ing takes place in coastal and offshore waters in the
winter (Christmas and Waller 19753; Lewis and
Roithmayr 1981). Larvae move onshore into Gulf
estuaries in winter and early spring, transform to
juveniles, and remain in the nursery areas until the
following fall. Juveniles move offshore during the
winter and back into coastal waters the following
summer. Spawning occurs for the first time at the
end of their second year.
A joint State-Federal-Industry plan developed for
gulf menhaden identified the lack of a reliable mea-
sure of effective effort and questionable MSY
estimates as major concerns in evaluating the gulf
menhaden stock and fishery (Christmas and Etzold
1977). Problems encountered in determining the
status of gulf menhaden stocks and estimating a
long-term yield from catch-effort data on schooling
species subjected to a purse seine fishery are com-
pounded by the "dynamic aggregation process"
described by Clark and Mangel (1979). Basically, they
3Christmas, J. Y, and R. S. Waller. 1975. Location and time
of menhaden spawning in the Gulf of Mexico. Unpubl. manuscr.,
20 p. Gulf Coast Research Laboratory, Ocean Springs, MS 39564.
Manuscript accepted July 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
311
FISHERY BULLETIN: VOL. 84, NO. 2
hypothesized that surface schooling species are more
susceptible to fishing effort than nonschooling
species, and indicators of abundance such as catch
and catch per unit effort (CPUE) are not reliable
when the "intrinsic schooling rate is greater than
the intrinsic (population) growth rate". Thus, severe
stock depletion could occur in the gulf menhaden
fishery before indications of such a situation were
evident from catch and CPUE data. The dynamic
aggregation process may be further aggravated
when the vessels are assisted by spotter aircraft
which greatly reduce search time.
We have attempted to estimate characteristics of
the gulf menhaden stock, such as population size,
biomass, growth rate, spawner-recruit relationship,
and to determine characteristics of the fishery, such
as fishing mortality, catchability coefficient, yield-
per-recruit, equilibrium yield levels, and MSY. These
characteristics were determined through application
of cohort analysis, yield-per-recruit and spawner-
recruit models, and a deterministic simulation model
of the Gulf of Mexico population and fishery. Our
overall objectives are to evaluate the status of the
gulf menhaden stock, determine the impact of the
fishery, and provide an outlook for the stock and
fishery for resource managers and the purse seine
fishing industry in the Gulf of Mexico.
GULF MENHADEN DATA BASE
The National Marine Fisheries Service (formerly
Bureau of Commercial Fisheries) has maintained a
sampling program for gulf menhaden since 1964.
Details of the sampling methodology are given by
Nicholson (1978) and Huntsman and Chapoton
(1973), and a description of the aging technique is
provided by Nicholson and Schaaf (1978). Vessel
landings by trip have been recorded, along with per-
tinent data on vessel size and characteristics. Overall
summaries of landings by year and nominal effort
(measured in vessel-ton-weeks) are available back to
1945, but the basis for the bulk of this analysis is
the catch and effort data (1964-79) and estimated
number of fish landed at age for these years (Table 1).
WEIGHT-LENGTH RELATIONSHIP
AND GROWTH
Estimates of growth rate are needed for yield
analyses and estimates of size at age are needed to
determine the spawner-recruit relationship. Al-
though some calculations use length and others
weight, all growth estimates were calculated for
length, and when required, weight was estimated
from the weight-length relationship.
For each age group, there was no major systematic
variation in the mean length over the 15 yr period
(Fig. 1). In addition, no density-dependent correla-
tions were detectable for mean length at age on
stock size or on year-class size, estimated from the
subsequent cohort analysis. Hence there appeared
to be little, if any, potential gain in estimate accuracy
by computing and using year-class specific growth
rates when reconstructing the historical population
biomass and average size at age for the subsequent
spawner-recruit analysis, or to incorporate a density-
dependent growth function in the subsequent popula-
tion simulations for total yield.
Estimates of overall mean length at age for each
quarter for the year classes that had passed com-
Table 1. — Catch, effort, and estimated number of gulf menhaden landed at age for the 1964-79 fishing
seasons (1964-78 for number at age).
Catch
(metric
No. of
Effort
(vessel-ton-
Number at age x
106
Year
tons x 103)
vessels'
weeks x 103)
0
1
2
3
4
Total
1964
409.4
76
272.9
6.3
3,135.6
1 ,365.2
108.1
3.9
4,619.1
1965
463.1
82
335.6
46.6
4,888.1
966.3
69.9
1.5
5,972.4
1966
359.1
80
381.3
46.8
3,126.8
850.2
30.5
0.5
4,054.8
1967
317.3
76
404.7
18.7
4,129.2
309.9
10.5
—
4,468.3
1968
373.5
69
382.3
35.4
3,311.5
850.0
27.0
0.2
4,224.1
1969
523.7
72
411.0
10.8
5,766.8
1,011.1
30.4
—
6,819.1
1970
548.1
73
400.0
49.2
3,256.4
2,197.2
34.4
—
5,537.2
1971
728.2
82
472.9
25.3
5,763.3
1,838.1
166.2
3.7
7,796.6
1972
501.7
75
447.5
17.6
3,146.3
1,615.6
68.7
4.4
4,852.6
1973
486.1
65
426.2
57.2
3,012.4
1,082.7
108.2
1.3
4,261.8
1974
578.6
71
485.5
20.0
3,747.3
1,399.0
60.2
—
5,226.5
1975
542.6
78
536.9
96.4
2,512.3
1,453.1
428.2
0.8
4,490.8
1976
561.2
81
575.9
1.8
4,517.7
1,273.1
190.2
—
5,982.8
1977
447.1
80
532.7
1.6
4,800.2
1,209.6
104.3
7.3
6,123.0
1978
820.0
80
574.3
0.0
6,784.7
2,578.8
48.3
3.6
9,415.4
1979
777.9
77
533.9
—
—
—
—
—
—
'Includes only vessels that fished 9 or more weeks.
312
NELSON and AHRENHOLZ: CHARACTERISTICS OF GULF MENHADEN
Figure 1— Mean length of gulf menhaden at
ages 1-3 taken from commercial landing sam-
ples (April- June), 1964-78.
E
E
I
I-
O
z
LU
—I
rr
O
Li.
<
LU
250r
200
150
100
of
J I
J I I L
J L
1964 65 66 67 68 69 70 71 72 73 74 75 76 77 78
YEAR
pletely through the fishery were used in the growth
computations (Table 2). The von Bertalanffy growth-
in length equation
lt = Loo(l - e
■W-L
')
(1)
where lt = fork length (mm) at time t (years),
Leo = theoretical length at t = infinity
(asymptote),
K = growth coefficient,
t0 = theoretical age when length = 0
was fitted to the data by the computer program
BGC3 (Abramson 1971). Although the data points
appear stepped between whole age units, they are
reasonably well described by the fitted curve (Fig. 2).
Table 2.— Mean length and number of
fish sampled at age from 1963 to 1974
year classes of gulf menhaden.
Mean fork
length
Age
(mm)
Number
1.125
121.7
59
1.375
148.3
43,284
1.625
160.5
57,286
1.875
161.3
1,538
2.125
—
—
2.375
182.9
16,687
2.625
190.6
16,452
2.875
194.4
260
3.125
—
—
3.375
210.5
1,063
3.625
216.4
1,368
3.875
220.2
14
4.125
—
—
4.375
227.8
16
4.625
227.5
32
4.875
—
—
E
E
X
t-
a
z
LU
_)
cr
O
LL
24U
200
160
120
S*
80
/
lt=252.893(l-e-°-4748(t+0-3585))
40
o
■ i
i . i . i . i . i i
'
"
i
D 0.5
1.0 1.5 2.0 2.5 3.0 3.5
4.0
4.5
5.0
AGE IN YEARS
Figure 2— Von Bertalanffy growth curve fitted to average length at age data for gulf menhaden
sampled from commercial landings, 1963-74 year classes.
313
FISHERY BULLETIN: VOL. 84, NO. 2
Weight-length regression coefficients were calcu-
lated for each of three 2-mo intervals for the major
portion of the fishing season for each year class,
1960-77. No systematic variation in the parameter
estimates was apparent within years by 2-mo inter-
vals, so the data were pooled between seasons and
years. An overall weight-length relationship was ob-
tained from a GM-functional regression (Ricker
1973) on the pooled data. The results are
log, w = 3.2669 log, I - 12.1851 (2)
where w = weight in g, and
I = fork length in mm.
The correlation coefficient (r) was 0.976 and the sam-
ple size was 168,397.
COHORT ANALYSIS
Estimates of mortality rates and population sizes
were obtained by using the Cohort Analysis tech-
nique developed by Murphy (1965) and later modified
by Tomlinson (1970). Calculations were made with
the computer program MURPHY (Tomlinson 1970).
This technique does not involve estimates of CPUE.
The backward estimation procedure was used. Since
the catch equations and general method of applica-
tion are given in Tomlinson's paper, discussion here
will be limited to the source and nature of input data
and parameters.
The calendar year was divided into four periods
(quarters) of approximately equal length:
Quarter 1 = 1 January to 3 April,
Quarter 2 = 4 April to 3 July,
Quarter 3 = 4 July to 3 October,
Quarter 4 = 4 October to 31 December.
Numbers of fish at each age landed quarterly were
sums of weekly estimates obtained by sampling
methods outlined by Nicholson (1978). Annual sum-
maries of these data were given earlier (Table 1).
An estimate of the annual rate of instantaneous
natural mortality (M) was obtained from an analysis
of mark-recapture data (Ahrenholz 1981). M, equal
to 1.1 (0.275 per quarter), was assumed to be con-
stant for all ages and seasons.
Because backward sequential computations, using
a range of trial estimates of input F (instantaneous
fishing mortality) for the oldest age, tend to con-
verge on the correct value of F for the youngest and
forward calculations tend to diverge (unless true
starting values are used), it is desirable to begin with
the oldest age for which reliable landing data are
available (Ricker 1975). Because of aging difficulties
(Nicholson and Schaaf 1978), we assumed that catch
estimates of older fish, mainly age 4, were not
reliable, hence for most year classes estimates of the
annual rate of instantaneous fishing mortality (F)
for age-2 fish were derived from catches of age 2 and
age 3 from
Fn = (log, Cn - log, Cn+1) - M
(3)
where C = annual catch in numbers at age (n) from
a given cohort.
Initial starting values of F for the oldest age group
landed in a year class were adjusted by trial and er-
ror until the sum of the quarterly Fs for age-2 fish
were virtually equal to the estimate of annual F2
derived from Equation (3). This technique was ap-
plicable for all year classes except 1960 and 1961,
where no 2-yr-old fish were available in the landing
data, the 1976 year class where no 3-yr-old fish were
available in the landing data, and the 1972 year class,
where the 2-yr-old fish apparently were not fully
recruited. For the 1960 and 1961 year classes, trial
and error adjustments were made to the starting F
value until the annual Fz estimate for the 1961 year
class and the annual F4 estimate of the 1960 year
class were virtually equal to the unweighted mean
F3 estimate derived from the sequential computa-
tions of the 1963-71 and 1973-75 year classes.
Similarly, the mean F2 estimate was used for the
1976 year class and the mean F3 estimate for the
1972 year class.
Estimates of number- at-age by quarter by year
class obtained from cohort analysis permitted the
reconstruction of population structure for the ex-
ploited gulf menhaden stock from 1964 to 1977
(Table 3). Numbers of newly recruited age-1 fish
varied as much as threefold between years. Because
age-1 fish were numerically the most abundant age
group each year, the population size fluctuated in
close concert with their numbers (Fig. 3).
Resultant age-specific annual Fs by fishing season
demonstrate that 1-yr-olds are incompletely re-
cruited to the fishery and that age 2's are fully re-
cruited (Table 4). These results are in accord with
those of Ahrenholz (1981), who concluded that fish
from more distant eastern and western, areas of the
Gulf of Mexico (Gulf) shifted toward the more heavily
fished central Gulf areas as they aged. The slightly
higher values for both the weighted and unweighted
mean F's for 3- and 4-yr-olds could be due to either
small numbers of fish from the most distant eastern
314
NELSON and AHRENHOLZ: CHARACTERISTICS OF GULF MENHADEN
Table 3.— Population size (in millions) of gulf
menhaden on 4 April estimated by cohort
analysis, 1964-77.
Age
Year
1
2
3
4
1964
8,189.2
2,048.0
156.8
5.5
1965
9,796.0
1,329.2
105.0
7.4
1966
5,703.8
1,111.9
41.9
5.2
1967
9,215.6
548.5
14.4
0.0
1968
9,256.7
1,249.0
47.6
0.3
1969
19,311.9
1,539.6
44.6
0.0
1970
12,454.5
3,817.6
59.4
0.0
1971
15,860.1
2,635.0
289.3
4.7
1972
9,580.3
2,704.4
97.0
25.6
1973
15,793.9
1,796.2
181.5
2.6
1974
15,107.1
3,849.3
99.6
0.0
1975
10,220.9
3,324.1
668.4
5.5
1976
11,467.8
2,216.2
435.6
0.0
1977
18,584.2
1,739.4
181.4
57.9
and western areas reaching the more intensively
fished waters, or simply a sampling variance. The
F estimates from cohort analysis for age-3 and age-4
fish are somewhat suspect, especially for age 4, since
the cohort analysis technique used (iterating to a
preset F2) actually makes the F3 and F4 estimates
of a forward computational nature, rather than
backward as for age 1. The divergent nature of the
estimates is clearly evident in the values for age 4,
although the mean value is realistic for subsequent
yield computations, and numbers of fish at this age
are of very low magnitude as well.
Because a year class is well represented in the
fishery for only 3 yr, a short time span is available
for the convergence of estimates of numbers and
fishing mortality. This short time span was ap-
25r
Figure 3— Population number of gulf menha-
den as of 4 April 1964-77, Estimated from
cohort analysis on 1960-76 year classes.
CO
c
o
LU
N
CO
O
I-
<
-J
a.
O
0.
■ ■ ' I I 1 1 1
1964 65 66 67 68 69 70 71 72 73 74 75 76 77
YEAR
Table 4.— Annual instantaneous fishing mortality rate (F)
for gulf menhaden for ages 1-3, by year, 1964-77, and fishing
mortality rate applied at age 4 (age 3 for year classes
without age-4 landings) to initiate the cohort analysis.
F
Year
Age 1
Age 2
Age 3
Age 4
1964
0.7182
1 .8706
1 .9547
1 .9504
1965
1 .0757
2.3576
1.9112
0.3546
1966
1.2431
3.2468
2.5992
0.1399
1967
0.8991
1 .3447
2.7786
0.0000
1968
0.6938
2.2323
1 .4032
110.6065
1969
0.5211
2.1553
1 .6225
0.0000
1970
0.4521
1 .4760
1 .4392
0.0000
1971
0.6681
2.2033
1 .3287
110.4097
1972
0.5740
1.6024
2.5195
0.2688
1973
0.3120
1.7933
2.0281
1.2313
1974
0.4140
0.6507
1 .7885
0.0000
1975
0.4287
0.9322
1 .9484
0.1950
1976
0.7860
1 .4030
0.9184
0.0000
1977
0.4375
2.1293
1 .4229
0.1923
Mean F
0.6588
1.8141
1 .8331
1.8106
(unweighted)
parently adequate, however, as cohort runs on the
year classes with 4-yr-olds in the landings, using
starting estimates of F for age 4 obtained from catch
curves, converged to very similar estimates to those
obtained by the analysis used here. Ulltang (1977)
emphasized that when F is high, convergence is
rapid.
The short-term impact of the fishery on the stock
can be assessed by comparing the estimated number-
at-age in the population for any given year with the
number-at-age landed by the fishery, or simply by
using the estimated rate of fishing and calculating
the exploitation rate (u) by
un = (Fn (1 - e-^W)Wn + M).
(4)
initial F set equal to 10.0.
From 1964 to 1977 the fishery took an average of
31% of the 1-yr-olds in the population and about 61%
of the older fish each year. At these exploitation rates
315
FISHERY BULLETIN: VOL. 84, NO. 2
the population loses 52% of the age-1 fish and 35%
of the older fish to natural mortality.
The short-term impact on the entire population
was determined by 1) calculating a mean F weighted
by the number of individuals taken by age for ages
1-3 and then estimating u by Equation (4) and 2)
directly comparing numbers landed with the recon-
structed population sizes. The average annual loss
of individuals from the population to the fishery was
about 40% by both methods. However, recruitment
is only partial at age 1, and u is much higher at older
ages. Natural mortality losses averaged about
47%/year for the overall population. In the absence
of fishing, annual losses to natural mortality would
be about 67% for all ages.
A measure of how a unit of fishing effort affects
the population is commonly quantified through its
effect on F. Traditionally this effect, the catchabil-
ity coefficient (q), is assumed to be a constant. The
total fishing effort times this constant should equal
F for the year:
F=qf
(5)
where / = a unit of fishing effort (here, a vessel-
ton-week).
if the catchability coefficients were independent of
this variable (Fig. 4). An inverse relationship was
noted, a situation which also exists for the Atlantic
menhaden (Schaaf 1975b). The data were fitted to
the power function to demonstrate the curvilinear
inverse relationship.
SPAWNER-RECRUIT RELATIONSHIP
The cohort analysis provides estimates of popula-
tion size at ages 1-4 from 1964 to 1977. All fish
mature by the end of their second year, and spawn-
ing apparently reaches a peak in December and
January (Lewis and Roithmayr 1981). Therefore,
estimates of number-at-age in the population as of
1 January were used to provide estimates of spawn-
ing stock size and subsequent recruitment (Table 6).
Spawning stock was identified as all fish that had
reached at least their second birthday by 1 January.
Lewis and Roithmayr also showed that length ac-
counted for a greater porportion of the variance in
fecundity than either age or weight. Our fecundity
estimates, assuming a 1:1 sex ratio, were based on
Lewis and Roithmayr's relationship:
log, E = -9.8719 + 3.8775 (log, I)
(6)
Estimates of q for the 1964-77 fishing years were
obtained by solving for q in the above equation for
the population F for ages 1-3 (i^.3) weighted by
number taken at age, and also for the population
total F (Table 5). The resultant g's are quite variable
(in excess of fourfold). Estimates of q were plotted
against corresponding population size to determine
where E = fecundity in number of eggs and
I = fork length in millimeters.
Because there was little variation in size at age
by year class, and the differences noted were not
related to population size, estimates of mean length-
at-age were obtained from the overall von Bertal-
Table 5. — Estimated gulf menhaden population size as of April 4, number caught by
year, population exploitation rate (u), estimated population fishing mortality rate (F),
population catchability coefficient (q) x 10"3, weighted annual mean fishing mortal-
ity rate from cohort analysis (^.3), and the corresponding Fv3 catchability coefficient
(q) x 10 "3 calculated from vessel-ton-weeks (Table 1), 1964-77.
Population
Number
size
(millions)
caught
(millions)
Population
Year
age 1-4
age 1-4
u
F
Qx10-3
K3
Q1.3XIO"3
1964
10,399.5
4,612.8
0.444
1.10
4.03
1 .0886
3.99
1965
11,237.6
5,925.8
0.527
1.46
4.35
1 .2946
3.86
1966
6,862.8
4,008.0
0.584
1.78
4.67
1 .6785
4.40
1967
9,778.5
4,449.6
0.455
1.14
2.82
0.9346
2.31
1968
10,553.6
4,188.7
0.397
0.93
2.46
1.0176
2.64
1969
20,896.1
6,808.3
0.326
0.70
1.70
0.7687
1.87
1970
16,331.5
5,488.0
0.336
0.73
1.83
0.8682
2.17
1971
18,789.1
7,771.3
0.414
0.99
2.09
1 .0455
2.21
1972
12,407.3
4,835.0
0.390
0.90
2.01
0.9456
2.11
1973
17,774.2
4,204.6
0.237
0.47
1.10
0.7377
1.73
1974
19,056.0
5,206.5
0.273
0.56
1.15
0.4935
1.02
1975
14,218.9
4,394.4
0.309
0.66
1.23
0.7433
1.38
1976
14,119.6
5,981.0
0.424
1.02
1.77
0.9215
1.60
1977
20,562.9
6,121.4
0.298
0.63
1.18
0.7890
1.48
316
NELSON and AHRENHOLZ: CHARACTERISTICS OF GULF MENHADEN
6r
n
i
O
X
4-
Z
UJ
o
LLI
o
o
>
b
m
<
i
o
i-
<
°0k
5 6
_i_
J_
_L
9 10 11 12 13 14 15 16 17 18 19 20 21
POPULATION SIZE (billions)
Figure 4— Catchability coefficients calculated from population fishing mor-
talities (open circles, dashed line), and from cohort annual weighted mean fish-
ing mortalities (dots, solid line) plotted on population number estimated as of
4 April, for the 1964-77 fishing seasons (see Table 5).
Table 6.— 1 January estimates of number of spawners, number of eggs produced by the spawn-
ing stock, biomass of the spawning stock, and number and biomass of recruits at age 1 for gulf
menhaden. Preliminary estimates in parentheses.
Total
No.
Spawning
Resultant
Recruitment
No. at age (
spawners
of eggs
biomass
recruitment
biomass
Year
2
3
4
(millions)
(trillions)
(t)
(millions)
(t)
1964
2,696.3
206.4
7.2
2,909.9
36.1
305,468
12,896.7
410,630
1965
1,749.9
138.2
9.7
1,897.8
23.7
200,150
7,519.5
239,421
1966
1,463.9
55.1
6.8
1,525.8
18.4
156,705
12,138.2
386,480
1967
722.2
19.0
—
741.2
8.8
75,118
12,186.7
388,025
1968
1,644.3
62.6
0.4
1 ,707.3
20.5
174,454
25,424.7
809,522
1969
2,026.9
58.7
—
2,085.6
24.8
211,752
16,396.8
522,074
1970
5,026.0
78.2
—
5,104.2
60.0
513,461
20,889.9
665,134
1971
3,472.8
382.4
6.2
3,861.4
49.0
412,808
12,618.5
401,773
1972
3,565.3
127.7
33.7
3,726.7
45.2
384,521
20,796.4
662,157
1973
2,365.8
239.0
3.4
2,608.2
32.8
277,323
19,889.0
633,266
1974
5,067.7
131.1
—
5,198.8
61.7
526,725
13,456.1
428,442
1975
4,376.3
879.9
7.3
5,263.5
70.5
588,668
(15,097.7)
(480,711)
1976
2,917.7
573.5
—
3,491.2
46.6
389,073
(24,466.7)
(779,020)
1977
(2,290.0)
238.8
76.2
(2,605.0)
(34.3)
(286,686)
1978
(5,258.5)
( 90.6)
19.2
(5,368.3)
(63.6)
(543,194)
anffy growth function presented earlier. Thus,
length-at-age estimates are taken as constants, and
differences in among year estimates of egg produc-
tion are due to differences in both total numbers and
age composition of the spawning stock (Table 6).
Similarly, the weight-length relationship was used
in conjunction with the mean length-at-age esti-
mates to obtain weight-at-age estimates for com-
putation of spawning and recruitment biomass (Table
6).
Least-square regressions of second and third
degree polynomials were run with numbers of re-
cruits on number of spawners to determine the
general shape of the spawner-recruit relationship.
Dome-shaped functions provided the least residual
sum of squares, indicating that a Ricker-type curve
(Ricker 1975) is appropriate A Ricker-type function
has been applied to Atlantic menhaden data (Nelson
et al. 1977), and the same criteria appear to apply
to gulf menhaden data, i.&, that there is a size-
dependent fecundity relationship and that adult
menhaden are filter feeders which are known to in-
gest their own eggs. Additionally, the calculation of
an index of density dependence, as detailed by
Cushing (1971) (loge recruitment regressed on loge
spawning stock), provides a slope of 0.159. This slope,
317
FISHERY BULLETIN: VOL. 84, NO. 2
plus the average fecundity of gulf menhaden (about
25,000 eggs/female) places the gulf menhaden
among Cushing's clupeoid groups which have a
slightly domed spawner-recruit curve Accordingly,
a spawner-recruite relationship was applied of the
form:
R = Se^ ~ 5>/s«
(7)
where R
S
e
Sr
= recruitment at age 1
= spawning stock size
= base of natural logarithm
= maximum equilibrium stock
= spawning stock size yielding maxi-
mum absolute recruitment.
The model, fitted by a nonlinear least squares
technique (Marquardt 1963), predicts an average
maximum recruitment of 18.4 billion individuals at
a spawning stock of 3.22 billion (Table 7). The curve
is a reasonably good fit (Fig. 5), considering the
variability inherent in clupeoid recruitment. Data
were available over a wide range of spawning stock
sizes and recruitment levels. Although recruitment
tended to fluctuate widely at lower spawning stock
sizes, estimates appear to converge at higher spawn-
ing stock levels, indicating the possibility of a strong
density-dependent response as spawning stock size
increases. The Ricker function appears to describe
the data, thus an estimate of spawning stock size
premits a general estimate of anticipated re-
cruitment at moderate to high numbers of
spawners.
Because fecundity increases with age and because
age structure of spawners varies from year to year,
estimates of the number of eggs produced should
provide a more accurate estimate of spawning stock
size than estimates of the numbers of spawners.
When the Ricker equation was fitted to number of
eggs and number of recruits, the estimate of op-
timum spawning stock size was similar to the
estimate based on the number of spawners and
recruits (Table 7) (SM of 39.66 trillion eggs = 2.3
billion spawners). The unrealistic replacement level
(Sr) of 283.32 trillion eggs was generated by scaling
factors involved in the comparison of unequal
spawner and recruit units (Ricker 1975). Applying
the function to spawning and recruitment biomass
also provided similar estimates of maximum recruit-
ment and optimum spawning stock size (Table 7,
Table 7. — Ricker spawner-recruit estimates of maximum equilibrium
stock (Sr), stock size for maximum recruitment (Sm), and recruit-
ment at Sm, for models incorporating number of spawners on
number of recruits, number of eggs on number of recruits, and
spawning biomass on recruitment biomass, 1964-76 year classes
of gulf menhaden.
Stock for
Maximum
maximum
equilibrium
recruitment
Recruitment
stock (Sf)
(Sm)
atSm
No. of spawners
on no. of
recruits 8.83 billion 3.22 billion 18.42 billion
No. of eggs
on no. of
recruits 283.32 trillion 39.66 trillion 18.48 billion
Spawning
biomass
on recruit
biomass 524,172 t 336,011 t 588,236 t
NUMBER OF SPAWNERS (billions)
Figure 5.— Ricker spawner-recruit relationship for number of spawners and recruits at
age 1, estimated as of 1 January, for the 1964-76 gulf menhaden year classes.
318
NELSON and AHRENHOLZ: CHARACTERISTICS OF GULF MENHADEN
Fig. 6). The maximum recruitment level of 588,236
t is equal to about 18.5 billion recruits. The optimum
spawning stock biomass of 336,011 t is equal to
about 3.2 billion spawners, assuming the age distri-
bution for the spawning stock is average. The func-
tion for biomass accounts for changes in age struc-
ture of the spawning stock and since age-2 fish
consistently represent over 90% of the spawners,
differences between plots of numbers and biomass
(Figs. 5, 6) are minor.
Spawning stock size has generally remained with-
in a range of potentially good recruitment and has
not undergone years of extreme highs or lows (Figs.
5, 6). Trends indicating a steady decrease or increase
in stock size and recruitment are not apparent, al-
though the general increased level of recruitment
in recent years may be part of a cyclic recruitment
fluctuation that is found in many stocks.
YIELD-PER-RECRUIT
We applied what is essentially a Ricker type yield-
per-recruit model that was initially developed to
evaluate a multiple-gear fishery (M-GE AR) and later
modified to accommodate a multiple-area fishery (M-
AREA) (Lenarz et al. 1974; Epperly et al. 19794).
Yield is summed by time intervals, and individual
weights and estimates of natural and fishing mor-
tality can be inserted for each interval (Ricker 1975).
An option developed by Epperly et al. (fn. 4) allows
4Epperly, S. P., W. H. Lenarz, L. T. Massey, and W. R. Nelson.
1979. A generalized computer program for yield per recruit
analysis of a migrating population with area specific growth and
mortality rates. Unpubl. manuscr., 14 p. Southeast Fisheries
Center Beaufort Laboratory, National Marine Fisheries Service,
NOAA, Beaufort, NC 28516.
for calculation of biomass within intervals by either
exponential or arithmetic means. We applied the
model in its simpliest form: one set of growth data
because the stock was not divided into subareas, con-
stant natural mortality rate, and the exponential
growth mode for biomass calculation. The year was
divided into quarters to simulate the seasonal nature
of the fishery (Table 8). Quarterly fishing mortality
rates were developed from the cohort analysis.
Estimates were obtained for periods of low popula-
tion size and high fishing mortality (1964-68), high
population size and low fishing mortality (1974-77),
and "average" population size and mortality
(1964-77) (Table 8). Age of entry into the fishery was
Table 8.— Input array of quarterly length (mm), weight (g), and
fishing mortality rates (F) used in the calculation of yield-per-recruit
of gulf menhaden under average fishing conditions (1964-77), years
of low stock size (1964-68), and years of high stock size (1974-
77).
Age
0.50
0.75
1.00
1.25
1.50
1.75
2.00
2.25
2.50
2.75
3.00
3.25
3.50
3.75
4.00
4.25
4.50
4.75
Months
W
F
(64-77)
F
(64-68)
July-Sept.
Oct.-Dec.
Jan. -Mar.
Apr.-June
July-Sept.
Oct.-Dec.
Jan. -Mar.
Apr.-June
July-Sept.
Oct.-Dec.
Jan.-Mar.
Apr.June
July-Sept.
Oct.-Dec.
Jan.-Mar.
Apr.-June
July-Sept.
Oct.-Dec.
84.7
103.5
120.2
135.1
148.2
160.0
170.4
179.6
187.8
195.1
201.6
207.3
212.4
216.9
221.0
224.5
227.7
230.5
10.1
19.5
31.8
46.6
63.2
81.0
99.5
118.2
136.8
154.9
172.3
188.9
204.5
219.1
232.7
245.2
256.7
267.2
0.0013
0.0003
0.0002
0.1850
0.4437
0.0299
0.0002
0.4478
1.2213
0.1448
0.0003
0.4500
1 .2722
0.1106
0.0000
0.1605
1.6501
0.0018
0.0001
0.0004
0.2677
0.6315
0.0264
0.0000
0.5652
1 .5858
0.0594
0.0000
0.5407
1.5752
0.0133
0.0000
0.3085
2.3018
F
(74-77)
0.0008
0.0005
0.0000
0.1244
0.3593
0.0329
0.0000
0.3683
0.8253
0.0852
0.0000
0.2966
1 .0670
0.1557
0.0000
0.0488
0.0480
CO
CO
< r
800r
600
1-
z
LU
o
40C
>
H
o
)
ft
CD
O
E
200
<r
68
76
600
SPAWNING BIOMASS (metric tons X 103)
Figure 6— Ricker spawner-recruit relationship for biomass of spawners and recruits at age 1,
estimated as of 1 January, for the 1964-76 gulf menhaden year classes.
319
FISHERY BULLETIN: VOL. 84, NO. 2
0.5 yr of age, the age at which gulf menhaden first
appear in the catch in extremely small numbers and
have a very low fishing mortality rata Fishing mor-
tality occurs principally during the 2d and 3d
quarters of the year (April- September) (Table 8).
Various multiples of the average fishing mortality
at each age were used to simulate effects of in-
creased or decreased fishing mortality (Table 9).
landings in the fishery of 487,736 1 by only 2.6% for
1964-77.
Yield-per-recruit for the years of higher and lower
levels of fishing mortality (Table 8) was estimated
to be 18.20 and 15.78 g under F-multiples of 1.00
and age of entry at 0.5. Trends were identical to
those for average 1964-77 conditions, and thus are
not presented in further detail.
Table 9. — Estimates of gulf menhaden yield-per-recruit (g) under average conditions of growth
and as multiples of average fishing mortality rate (F-multiple = 1.00), 1964-77, at varying age
of entry.
Age at
entry
Multiplier of fishing mortality
0.25 0.33 0.50 0.66 0.75
1.00
1.25
1.50
1.75 2.00
4.50
0.96
1.19
1.60
1.90
2.04
2.34
2.54
2.69
2.79
2.86
4.25
1.06
1.31
1.75
2.07
2.21
2.52
2.73
2.87
2.98
3.05
4.00
1.06
1.31
1.75
2.07
2.21
2.52
2.73
2.87
2.98
3.05
3.75
1.18
1.46
1.96
2.31
2.48
2.84
3.09
3.28
3.43
3.55
3.50
2.73
3.32
4.28
4.93
5.21
5.80
6.20
6.47
6.67
6.81
3.25
3.32
4.01
5.10
5.81
6.12
6.74
7.15
7.43
7.63
7.78
3.00
3.32
4.01
5.10
5.81
6.12
6.74
7.15
7.43
7.63
7.79
2.75
3.63
4.38
5.58
6.38
6.73
7.45
7.96
8.33
8.62
8.86
2.50
6.39
7.62
9.51
10.71
11.23
12.27
12.95
13.41
13.74
13.98
2.25
7.43
8.80
10.86
12.12
12.66
13.71
14.37
14.82
15.14
15.37
2.00
7.43
8.80
10.86
12.12
12.66
13.71
14.37
14.82
15.14
15.37
1.75
7.52
8.91
10.99
12.27
12.82
13.89
14.57
15.04
15.38
15.63
1.50
8.91
10.52
12.93
14.43
15.07
16.36
17.22
17.83
18.30
18.67
1.25
9.45
11.13
13.62
15.15
15.80
17.09
17.94
18.53
18.97
19.30
1.00
9.45
11.13
13.62
15.15
15.80
17.09
17.94
18.53
18.97
19.30
0.75
9.45
11.13
13.62
15.16
15.80
17.09
17.94
18.53
18.97
19.30
0.50
9.45
11.13
13.62
15.15
15.80
17.09
17.93
18.52
18.95
19.28
20i
The yield-per-recruit increases only slightly with
a delayed age-of-entry and then drops rapidly be-
cause of the high rate of natural mortality. The
model predicts maximum cohort biomass at an age
of 1.5, before gulf menhaden are fully recruited in-
to the fishery. The high natural mortality rate re-
quires that substantial fishing mortality be applied
at a young age if gulf menhaden are to be harvested
near their peak biomass.
A three-dimensional representation of yield-per-
recruit (Table 9) is helpful in depicting the seasonal
nature of the fishery (Fig. 7). Since most of the fish-
ing mortality on age-1, -2, and -3 fish is applied dur-
ing the 2d and 3d quarters (ages of X.25 and X.50),
the impact of delaying recruitment past those
quarters results in a sharp decline in yield-per-
recruit, due to the high rate of natural mortality.
Predicted catches based on yield-per-recruit were
compared with actual catch during 1964-77. Aver-
age recruitment at age 1 (16,030 billion), estimated
from the cohort analysis, was back calculated to age
0.5, the age of initial entry, and multiplied by the
17.09 g/recruit predicted by the model. The resul-
tant estimate of 474,829 t differs from the average
b
cr
o
HI
a.
a.
hi
a.
Q
_l
UJ
>
4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5
AGE AT ENTRY
Figure 7.— Yield-per-recruit of gulf menhaden under average con-
ditions of growth and with multiples of average fishing mortality
by 3-mo interval (F-multiple = 1.0) for the 1964-77 fishing seasons
(average conditions indicated by □).
320
NELSON and AHRENHOLZ: CHARACTERISTICS OF GULF MENHADEN
SUSTAINABLE YIELD AND
POPULATION SIMULATION
Production functions were developed from the
1946-79 catch and effort data to provide an estimate
of maximum sustainable yield (MSY) for gulf men-
haden. Application of a standard parabolic surplus
production model (Schaefer 1954, 1957) yields an
MSY estimate of 553,000 t at 555,000 vessel-ton-
weeks. Past updates of MSY for the Gulf fishery have
shown continual increases as additional years are
added. Chapoton (1972) estimated an MSY of
430,000 t for the 1946-70 period, and Schaafs
(1975a) estimate of 478,000 t included the 1971 and
1972 catch and effort.
For the years in which estimates of catchability
coefficient (q) were calculated (1964-77) nominal ef-
fort was adjusted to the mean population q of that
period. For that time period, mean catchability coef-
ficient was divided by the estimate of population F
each year, to provide an estimate of effort adjusted
for "average" conditions from 1964 to 1977.
A parabolic surplus production function was ap-
plied to the 1946-79 data set, with adjusted effort
used instead of nominal effort for 1964-77. The
results were similar to model results using nominal
effort with an estimated MSY of 541,904 t at an ef-
fort of 505,483 vessel-ton-weeks (Fig. 8). A general-
ized stock production model (PRODFIT) which
allows the shape of the curve to vary based on a least
squares fit to the data (Fox 1975) was also applied,
yielding an estimate of MSY of 636,886 t at an ef-
fort of 531,201 vessel-ton-weeks (Fig. 8).
The two curves provide estimates that vary by
about 95,000 1 with the PRODFIT model indicating
a sharp drop in yield after MSY is exceeded.
An estimate of MSY based on biological charac-
teristics should be more reliable than one based on
yield and nominal effort, particularly when there is
not a clear nominal effort-effective effort relation-
ship. Accordingly, we applied a population simula-
tion model (Walters 1969) for the 1964-77 period
which incorporated our estimates of growth,
spawner-recruit relationship, fishing mortality, and
natural mortality. This estimated the impact of fish-
ing mortality on stock and yield at an array of fish-
ing mortality rates. The model can also iterate to
MSY. Underlying assumptions of the Walters'
model are that the 1) spawner-recruit relationship
incorporated is realistic, 2) array of F's accurately
reflect the distribution of fishing effort and avail-
ability at age, and 3) time increment estimates of
weight are sufficiently brief to realistically estimate
both population and catch biomass during the
fishing periods. The model calculates population
biomass, yield, residual spawners of age 2 and
greater, and incoming recruitment. We used weight-
at-age data described in the section on average size
and growth (Equations (1) and (2)), and used the
spawner-recruit relationship developed for the
number of spawners and recruits (Equation (7)). The
instantaneous natural mortality rate was 1.1 as
discussed earlier. Fishing mortality could not
precisely mimic that for the fishery, because the
program requires either zero fishing mortality or a
constant fishing mortality for any within-year incre-
ment. However, it does allow for an array of multi-
pliers at a given fishing mortality, providing dif-
ferent F's for each age, if desired. Therefore, we
were able to vary fishing mortality by age, but used
either zero or a constant fishing mortality for
quarterly increments within each year. Since fishing
mortality was essentially zero on age-0 fish and was
inconsistent between years, a fishing mortality rate
of zero was applied to that age group. For age
groups 1-4, all of the fishing mortality was by defini-
tion imposed equally in quarters 2 and 3 (April- June,
July-September), and no fishing mortality was ap-
plied in quarters 1 and 4, even though we knew that
fishing mortality during the July- September period
was consistently higher than that observed for the
900r
800-
700-
m
O
^
600
X
CO
c
O
500
o
»-
♦-
«
E
400
I
O
1-
300
<
o
200
100-
0 100 200 300 400 500 600 700 800
EFFORT (Thousands of Vessel Ton Weeks)
Figure 8.— Parabolic (dashed line) and prodfit (solid line) surplus
production function models fitted to catch and effort data for the
gulf menhaden fishery from 1946 to 1979, with 1964-77 data being
estimates of effective effort, based on adjustments from calculated
catchability coefficients for those years.
321
FISHERY BULLETIN: VOL. 84, NO. 2
previous quarter (i.e., the same nominal effort was
applied to a smaller population). The result was that
yield was overestimated for April-June and under-
estimated for July-September, but estimated reason-
ably accurately for the season.
We attempted to simulate reality by using multi-
ples of the fishing mortality distribution that we
observed in the 1964-77 data base. Fishing mortal-
ity imposed to mimic current conditions was ob-
tained by taking the mean fishing mortality at age
by quarter from the cohort analysis conducted on
the 1960-76 year classes (1964-77 fishing years). The
mean mortality on ages 2-4 fish was used, along with
a mortality obtained from a scaling factor of 0.362
for age 1 (Table 10). Input population size to start
the simulation runs was the mean population num-
ber-at-age as of 1 January, the arbitrarily assigned
birth date of gulf menhaden. Those numbers were
16,030 million, 2,813 million, 227.9 million, and
10.78 million for ages 1-4. The model was run over
a range from 0 to 2.75 times the average fishing
mortality and was also used to iterate to MSY under
the current distribution of fishing mortality by age
(Table 10).
The overall catch-effort curve from multiple runs
indicates that the fishery is operating slightly before
the MSY level (Fig. 9, Table 10). At the currents-
multiple of 1.0, the fishery should sustain an average
yield of about 565,581 t, assuming no variance in
recruitment from the hypothetical spawner-recruit
curve.
The model predicts a MSY of about 585,118 t at
127% of the average fishing mortality for the
1964-77 fishing seasons. We feel that this model,
which incorporates a spawner-recruit relationship
and recruitment pattern plus growth and natural
mortality rates, provides a better estimate of long-
term MSY than does a model based on a simple
catch-effort production function. Considerable fluc-
tuation in yield will result from fluctuations in
recruitment, but the long-term MSY estimate
appears to be realistic, provided that the esti-
mated spawner-recruit relationship is valid and
that the basic pattern of recruitment remains
unchanged.
The Walters' model also identifies the level of
fishing mortality at which the population is no longer
sustainable, i.e., a biological break-even point. The
extinction point occurs at an F- multiple of 2.50
(150% greater than current fishing mortality), al-
though the model indicates that such extinction
would involve a gradual decline over a period of
many years, again assuming that "average" condi-
tions prevailed (Fig. 9). Increasing the fishing mor-
tality beyond an F-multiple of 2.50 results in a more
rapid rate of extinction (Table 10).
Results of low and high F-multiple levels show
steep slopes on the ascending and descending limbs
of the production function curve (Fig. 9). The
ascending limb behaves similarly to the curves in
the yield-per-recruit model as fishing mortality rates
go from low to current levels (Fig. 7). At mortality
rates higher than current levels, however, the yield-
per-recruit model cannot be used to evaluate poten-
tial yield because of the impact of heavy fishing
mortality on the spawning stock and the subsequent
reduction in recruitment. For example, under the
average recruitment level of 16.03 billion fish at age
Table 10. — Annual age-specific fishing mortality rates for gulf menhaden, ex-
pressed as multiples of the average fishing mortality rate at age, 1964-77, (F-
multiple = 1.00), actual fishing mortality rates at age used in the population
simulation model, sustainable yield, population biomass, and years to
stabilization.
f.
Actual F at age
Sustainable
yield level
(t)
Population
biomass
(t)
Years
to stabi-
lization
multiple
0
1
2-4
0
0
0
0
0
1 ,268,348
97
0.25
0
0.1647
0.4550
266,878
1,151,345
53
0.50
0
0.3294
09100
419,813
1,072,885
35
0.75
0
0.4941
1 .3650
512,568
1,009,288
27
1.00
0
0.6588
1 .8200
565,581
945,740
8
1.25
0
0.8236
2.2750
585,010
871,695
20
1 .27 (MSY)
0
0.8367
2.3114
585,118
865,300
22
1.50
0
0.9883
2.7300
569,823
778,012
32
1.75
0
1.1530
3.1850
514,388
655,278
42
2.00
0
1.3177
3.6400
409,304
492,702
78
2.25
0
1 .4824
4.0950
241,462
277,288
210
2.50
0
1 .6471
4.5500
0
0
1>300
2.75
0
1.8118
5.0050
0
0
'250
1To extinction.
322
NELSON and AHRENHOLZ: CHARACTERISTICS OF GULF MENHADEN
1 (28.34 billion at age 0.5) and an F-multiple of 2.00,
the yield-per-recruit model predicts a total yield of
546,395 t; the population simulation model predicts
a gradual decline from current levels and stabiliza-
tion at about 409,304 t. Thus, when using average
recruitment levels and yield-per-recruit results,
estimates of yield at F-multiple levels higher than
about 1.75 times the average fishing mortality for
the 1964-77 period will be unrealistic.
The impact of increasing levels of fishing mortality
on the stock is also reflected in estimates of popula-
tion biomass under an array of F-multiples (Table
10). Biomass estimates were based on predicted
population size as of 1 January (i.e., after recruit-
ment and before application of fishing mortality).
These estimates show a pre-exploitation population
biomass exceeding 1.268 million t, followed by an
accelerating decline as increased fishing mortality
takes progressively larger fractions of the popula-
tion and disproportionately larger fractions of older
and heavier fish.
STATUS AND OUTLOOK FOR
THE GULF MENHADEN FISHERY
The gulf menhaden population appears to be
healthy, highly productive, and capable of supporting
yearly harvests exceeding 500,000 t, although con-
siderable variation can be expected. It has shown a
general increase in abundance through the period
covered in this report, although this increase
may be a portion of a general cycle of this clupeid
stock.
The high natural mortality rate indicates that fish-
ing mortality has to be applied at a fairly high rate
and on young fish to avoid loss of surplus biomass.
Peak cohort biomass is reached at an age of 1.5 yr.
It is not all available to the fishery, because age-1
fish are only partially recruited. Partial recruitment
appears to have some benefit in that it affords some
protection for the spawning stock.
Recruitment fluctuation appears to be greater at
low spawning stock sizes. Initial spawning before full
recruitment would assure moderate to high levels of
recruitment and reduce chances for large recruit-
ment fluctuation. Therefore, if recruitment failure
were to occur, it would likely arise from biotic or en-
vironmental factors rather than from excessive
fishing mortality.
Significant increases in fishing mortality are
unlikely to occur, given the present distribution and
operating procedure of the fishery, unless there is
a series of recruitment failures. The current fleet of
about 80 purse seine vessels appears to be more than
adequate to harvest the recruited gulf menhaden
stock during years of low to moderate stock size, and
700-
600-
n
o
500
X
(0
c
o
•-
400
o
—
a
F
300
•— '
D
-1
UJ
>
200
100-
025 O50
"0775 1^0 T725 175(
F-MULTIPLE
F00 05 T50
Figure 9— Sustainable yield predicted by a deterministic population simulation model of the
gulf menhaden fishery at multiples of the average fishing mortality (F-multiple = 1.00) for the
1964-77 fishing season (see Table 10 for scaling values).
323
FISHERY BULLETIN: VOL. 84, NO. 2
capable of taking advantage of those years when a
large harvestable stock is available (1971, 1978, and
1979). Total mortality rates (averaging 83% for age-1
fish and 95% for ages 2-4 fish) are extremely high.
Major expansions of the fleet and processing facil-
ities necessary to substantially increase the fishery's
share of population biomass would require enormous
capital investment. Based on results of the simula-
tion model, large increases in fishing effort would
also result in an overall average decline in landings
that would likely be followed by an economically
forced reduction in effort. Under present circum-
stances, we do not envision the sustained intensifica-
tion of effort necessary to drive the gulf menhaden
stock to biological extinction.
The simulation model estimates that the effort cur-
rently applied in the fishery is probably very close
to that which is necessary to produce MSY (Fig. 9),
while it exceeds the necessary level in the catch-
effort production function (Fig. 8). Assuming that
the simulation model reasonably approximates
average conditions, some increase in overall yield
could be obtained through a modest increase in
effort, which has in fact occurred in more recent
years.
Based on recruitment levels for 1964-77, it is evi-
dent that considerable variation will occur around
a long-term sustainable yield level, regardless of the
level of fishing mortality. We varied recruitment level
in the population simulation model through periods
of high (25 billion) and low (10 billion) levels of
recruitment to provide estimates of the yield from
the fishery under good and poor recruitment
regimes, and to observe the rate of response to
recruitment changes. The results range from an ap-
proximate high of 757,000 t to a low of 303,000 t at
the high and low recruitment levels (Fig. 10). Since
only age-1 and age-2 fish predominate in the fishery,
only 2 years were required for the full impact of a
change in recruitment to be shown, with a majority
of the impact occurring in the first year. We then
allowed the average spawner-recruit relationship to
operate, stabilizing yield at 565,580 t. Actual low
yield predictions are probably underestimated, in
that fishing mortality increases in years of low stock
size, and the fishery would produce higher yield than
through the fishing mortality imposed under average
conditions. Nevertheless, these extremes are near
the actual ranges in yield observed in the fishery dur-
ing the study period (316,100-820,000 t) and should
provide reasonable estimates of mean yield and
range expected in future years.
Since considerable variation does exist around the
spawner-recruit curve and simulations were all con-
ducted in deterministic fashion, the model was run
with recruitment varying randomly between the
recruitment extremes calculated from our data set
(7.5 billion-25.0 billion). The results of that simula-
tion (Fig. 10) provide a long-term (50 yr) average of
467,459 t, but it varies from 718,000 to 263,000 t.
We anticipate that the fishery will continue to
operate somewhat in this fashion, unless there is a
cyclic environmental or biological influence on
recruitment.
i,uoo-
*■■-»
n
O
800-
•*■
X
■
(O
c
600-
o
.
t^
+■*
F
400-
*■ —
o
_i
LU
>
200-
\/ b. ' '
V/fl. -0- O -6- -O- O -D- O^-O^-oVo
10
15
20
25
30
35
40
45
50
YEARS
Figure 10.— Annual yield of the gulf menhaden fishery projected by the population simulation
model when upper and lower values of recruitment from the 1964-77 year classes are inserted
(dashed line) and when recruitment varies randomly within limits of observed recruitment for
the same data set (solid line).
324
NELSON and AHRENHOLZ: CHARACTERISTICS OF GULF MENHADEN
SUMMARY
The fishery for gulf menhaden appears to be at
parity with the stock. There is ample capacity to
harvest available biomass and segments of the stock
are not available to the fishery until after spawning
has occurred. The fishery appears to be near the level
of estimated maximum sustainable yield, but will be
subject to wide ranges in annual yield. Substantial-
ly increased effort will likely reduce long-term
average yield, but should not drive the stock to
biological extinction. Maintenance of current catch
and stock conditions is dependent on the biology of
gulf menhaden, the pattern of recruitment, and on
maintaining the current fishing strategy. Major
changes in the operation of the fishery, such as an
expansion of effort east and west of the present
range, or offshore on winter spawning concentra-
tions, will change the basis on which these analyses
were formulated, and would have consequences
which are not predictable at this time
LITERATURE CITED
Abramson, N. J.
1971. Computer programs for fish stock assessment. FAO
Fish. Tech. Pap. 101, 154 p.
Ahrenholz, D. W.
1981. Recruitment and exploitation of Gulf menhaden,
Brevoortia patronus. Fish. Bull., U.S. 79:325-335.
Chapoton, R. B.
1972. The future of the Gulf menhaden, the United States'
largest fishery. Proc Gulf Caribb. Fish. Inst. 24:134-143.
Christmas, J. Y., Jr., and D. J. Etzold.
1977. The menhaden fishery of the Gulf of Mexico United
States: a regional management plan. Gulf Coast Res. Lab.
Tech. Rep. Ser. 1, 53 p.
Clark, C. W., and M. Mangel.
1979. Aggregation and fishery dynamics: a theoretical study
of schooling and the purse seine tuna fisheries. Fish. Bull.,
U.S. 77:317-337.
Cushing, D. H.
1971. The dependence of recruitment on parent stock in dif-
ferent groups of fishes. J. Cons. Int. Explor. Mer 33:340-362.
Fox, W. W., JR.
1975. Fitting the generalized stock production model by least-
squares and equilibrium approximation. Fish. Bull, U.S.
73:23-37.
Huntsman, G. R., and R. B. Chapoton.
1973. Biostatistical data acquisition in the menhaden fisheries.
Trans. Am. Fish. Soc 102:452-456.
Lenarz, W. H., W. W. Fox, Jr., G. T Sakagawa, and B. J. Roth-
child.
1974. An examination of the yield per recruit basis for a
minimum size regulation for Atlantic yellowfin tuna, Thun-
nus albacares. Fish. Bull., U.S. 72:37-61.
Lewis, R. M., and C. M. Roithmayr.
1981. Spawning and sexual maturity of Gulf menhaden
Brevoortia patronus. Fish. Bull., U.S. 78:947-951.
Marquardt, D. W.
1963. An algorithm for least-squares estimation of nonlinear
parameters. SIAM J. App. Math. 11:431-441.
Murphy, G. I.
1965. A solution of the catch equation. J. Fish. Res. Board
Can. 22:191-202.
Nelson, W. R., M. C. Ingham, and W. E. Schaaf.
1977. Larval transport and year-class strength of Atlantic
menhaden, Brevoortia tyr -annus. Fish. Bull., U.S. 75:23-41.
Nicholson, W. R.
1978. Gulf menhaden, Brevoortia patronus, purse seine
fishery: catch, fishing activity, and age and size composition,
1964-73. US. Dep. Commer., NOAA Tech. Rep. NMFS
SSRF 722, 8 p.
Nicholson, W. R., and W. E. Schaaf.
1978. Aging of Gulf menhaden, Brevoortia patronus. Fish.
Bull., U.S. 315-322.
Reintjes, J. W.
1964. Annotated bibliography on biology of menhadens and
menhadenlike fishes of the world. US. Fish. Wildl. Serv.,
Fish. Bull. 63:531-549.
Reintjes, J. W., and P. M. Keney.
1975. Annotated bibliography on the biology of the
menhadens, genus Brevoortia, 1963-1973. US. Dep. Com-
mer., NOAA Tech. Rep. NMFS SSRF 687, 92 p.
Reintjes, J W., J. Y. Christmas, Jr., and R. A. Collins.
1960. Annotated bibliography on biology of American men-
haden. U.S. Fish Wildl. Serv., Fish. Bull. 60:297-322.
Ricker, W. E.
1973. Linear regressions in fishery research. J. Fish. Res.
Board Can. 30:409-434.
1975. Computation and interpretation of biological statistics
offish populations. Bull. Fish. Res. Board Can. 191, 382 p.
Schaaf, W. E.
1975a Status of the Gulf and Atlantic menhaden fisheries and
implications for resource management. Mar. Fish. Rev.
37(9):l-9.
1975b. Fish population models: potential and actual links to
ecological models. In C. S. Russell (editor), Ecological
modeling in a resource management framework, p.
211-239. Resources for the Future, Washington, D.C.
Schaefer, M. B.
1954. Some aspects of the dynamics of populations important
to the management of the commercial marine fisheries.
Inter-Am. Trop. Tuna Comm. Bull. 1:27-56.
1957. A study of the dynamics of the fishery for yellowfin tuna
in the eastern tropical Pacific Ocean. Inter-Am. Trop. Tuna
Comm. Bull. 2:247-268.
Tomlinson, P. K.
1970. A generalization of the Murphy catch equation. J. Fish.
Res. Board Can. 27:821-825.
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1977. Sources of errors in and limitations of virtual popula-
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1969. A generalized computer simulation model for fish
population studies. Trans. Am. Fish. Soc 98:505-512.
325
LENGTH-WEIGHT RELATIONSHIPS OF
BLUE, PARALITHODES PLATYPUS, AND GOLDEN,
LITHODES AEQUISPINA, KING CRABS PARASITIZED BY
THE RHIZOCEPHALAN, BRIAROSACCUS CALLOSUS BOSCHMA
Clayton R. Hawkes, Theodore R. Meyers, and Thomas C. Shirley1
ABSTRACT
Length-weight relationships and condition factors of nonparasitized blue king crabs, Paralithodes platypus,
and golden king crabs, Lithodes aequispina, in southeastern Alaska were compared with crabs parasi-
tized by the rhizocephalan, Briarosaccus callosus. Species, sex, and shell condition were considered in
all analyses. Parasitized male blue king crabs and parasitized male golden king crabs weighed significant-
ly less than nonparasitized individuals. Golden king crabs may be more resistant to infection and the ef-
fects of B. callosus parasitism than blue king crabs. They had a lower prevalence of infection, and the
percent difference between the body mass of parasitized and nonparasitized crabs was considerably less.
In both crab hosts the prevalence of infection was greater in samples where sublegal or smaller size classes
of adults were included in analyses, suggesting that crab growth was reduced by the parasite
A parasite of lithodid crab species in Alaska is the
rhizocephalan barnacle, Briarosaccus callosus
Boschma (Boschma and Haynes 1969; Boschma
1970; McMullen and Yoshihara 1970; Somerton 1981;
Hawkes et al. 1985). The parasite's distribution in
Alaskan waters, its life history, and its effects on
king crab hosts are almost unknown except that
parasitized crabs become castrated (Boschma and
Haynes 1969; McMullen and Yoshihara 1970). The
prevalence of this barnacle parasite varies between
areas and species and is especially high in south-
eastern Alaska. Parasitism by B. callosus might
decrease the productivity of king crab stocks
through sterilization and may also reduce crab
growth rates. Therefore, parasitized crabs of the
same size as nonparasitized crabs may weigh less.
In this study we examined the influence of B. callosus
on the length-weight relationships and condition fac-
tors of parasitized and nonparasitized blue king crab,
Paralithodes platypus, and golden king crab, Li-
thodes aequispina.
MATERIALS AND METHODS
Two methods were used to compare the growth of
parasitized and nonparasitized crabs. A Fulton's con-
dition factor (w/ls x 10 ~4, where w = weight in
grams and I = carapace length in mm) was used for
'School of Fisheries and Science, University of Alaska, Juneau,
11120 Glacier Highway, Juneau, AK 99801.
comparing different individuals of the same species
(Ricker 1975). This method assumes that all body
parts grow isometrically. The second method used
for comparison assumes allometric growth, where
different body parts grow at different rates. Con-
stants were determined empirically by linear regres-
sion using the model, w = ALB, and logarithms of
the carapace lengths and body weights (Everhart et
al. 1976, p. 70-71). The length-weight relationships
of parasitized and nonparasitized crabs were com-
pared with analysis of covariance (ANCOVA). All
mean values (X) are given ± 1 standard deviation.
Probabilities <0.05 are considered significant and
those <0.01 are considered highly significant.
The analysis of length-weight relationships was
based on wet weights taken in the field (nearest 25
g) and in the laboratory (nearest gram). Crabs with
missing or partially regenerated appendages were
not weighed. Carapace lengths were measured to the
nearest 1 mm (Wallace et al. 1949). Shell condition
was classified according to a four point scale (Somer-
ton and Macintosh 1983). A new shell condition is
found in crabs that have recently molted, and skip-
molt crabs are those that have not molted within the
last year. Skipmolts or old shell crabs were identified
by worn spines and dactyl tips and accumulations
of shell epifauna. Infections were diagnosed gross-
ly by the presence of externae or scars, indicative
of lost externae. A scar is a short chitinous brown
pedicel from which an externa was attached and pro-
trudes from underneath the abdomen.
Manuscript accepted July 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
327
riontni Dui_,j_in,in\: vul. 04, inu. z
Blue King Crab
Male and female blue king crab of various sizes
from Muir and Adams Inlets in Glacier Bay (Fig. 1)
were measured, weighed, and examined for B.
callosus by the authors in March 1984. Commercial
gear was used but with modified escape ports to pre-
vent loss of juvenile crabs. Data on large male blue
king crabs from Lynn Canal and Glacier Bay were
also gathered at dockside areas before sale to
processors or the public Since state regulations for
southeastern Alaska restrict the commercial harvest
of blue king crabs to males M65 mm in carapace
width, all commercial samples, therefore, excluded
females and smaller adult males.
Golden King Crabs
Male and female golden king crabs of various sizes
were collected by the authors from Lynn Canal near
Haines, AK (Fig. 1), using standard pot gear in May
1984. Commercial catches in November 1983 pro-
vided legal sized (M78 mm carapace width) males.
RESULTS
The prevalences of B. callosus in the commercial
catches of male blue king crabs were 6.3% and 11.6%
for Lynn Canal and Glacier Bay, respectively. Sam-
ples from Glacier Bay, which contained males and
females of all sizes, had a prevalence of 76%. The
prevalence in varisized male and female L. aequi-
spina collected from the Haines area was 20%.
Linear length-weight relationships of log trans-
formed data best defined our data, since no trends
were present in the residuals (differences between
predicted lines and actual data) of parasitized or non-
parasitized crabs.
Figure 1.— Sampling sites of blue, Paralithodes platypus, and golden, Lithodes aequispina, king crabs in south-
eastern Alaska.
328
HAWKES ET AL.: RHIZOCEPHALAN PARASITISM OF ALASKA KING CRAB
Blue King Crab
Glacier Bay and Lynn Canal blue king crab data
were pooled. The populations were considered to be
identical because the two groups were regarded as
having the same linear relationship (ANCOVA).
Smaller crabs (<134 mm in carapace length) not
common to data sets from both areas and skipmolts
were eliminated from this analysis.
Significantly (chi-square test) more skipmolts were
found among the nonparasitized crabs (45/237) than
the parasitized crabs (9/131). Because skipmolts tend
to be heavier than new shell crabs (Somerton and
Macintosh 1983), skipmolting was analyzed as a
possible source of bias. In male blue king crabs the
new shell crabs had a higher mean weight than the
skipmolts at greater carapace lengths, while the
skipmolts had a higher mean weight at the smaller
lengths (Fig. 2). Although individual linear relation-
ships did not describe the data as well as a common
line, the skipmolts were eliminated from further
analyses of both blue and golden king crab data.
Subsequently, in the length-weight relationships of
male blue king crabs pooled from both areas, with
small crabs represented in each group, the nonpara-
sitized crabs were heavier at a highly significant level
than the parasitized crabs (ANCOVA) (Fig. 3). Non-
parasitized males were 8.7% heavier than parasitized
crabs. Nonparasitized male blue king crabs also had
a significantly (£-test) higher condition factor (8.5 ±
0.8) than parasitized crabs (7.2 + 0.6), indicating that
nonparasitized crabs were heavier for a given length.
Condition factor did not vary with size in non-
parasitized blue king crabs but the slope was sig-
nificant and negative for the parasitized crabs. This
indicates that the condition factor of parasitized blue
king crabs decreased with increased size
Only five nonparasitized female blue king crabs
were available for length-weight relationships and
condition factor comparisons. More samples are
needed for further analysis of female blue king crabs.
Golden King Crabs
Males with carapace lengths common to both para-
sitized and nonparasitized crabs, 117 to 159 mm, pro-
vided linear relationships that were parallel and
significantly different (Fig. 4). Briarosaccus callosus
was not present in any of the large commercial-size
crabs sampled in 1983; therefore, these samples were
excluded from analysis. The percent weight dif-
ference between parasitized and nonparasitized male
golden king crabs was about 2.6%. Weight conver-
sion in parasitized male P. platypus of similar sizes
4000-
3500
O) 3000
O) 2500
2000J
Old Shell
lognY = -5.04 + 2.60loghX
r*=0.70
New Shell
lognY=-6.54 +2.89lognX
H =0.68
n i 181
130
135
140
^45 150 15JF
Length (mm)
160
Figure 2— Length-weight linear relationships of new shell and skipmolt nonparasitized male
Paralithodes platypus.
329
FISHERY BULLETIN: VOL. 84, NO. 2
O)
'3
5
4000
3000
2000
1000
Nonparasitized
I09.Y--
lognX
100 110 120 130 140 ISO 160 170 180
Length (mm)
Figure 3— Length-weight linear relationships of parasitized and nonparasitized male
Paralithodes platypus with skipmolts eliminated.
2500
^ 2000
O)
O) 1500
1000
log,
U
150
160
120 130 140
Length (mm)
Figure 4— Length-weight linear relationships of parasitized and nonparasitized male Lithodes
aequispina after elimination of 1983 data.
330
HAWKES ET AL.: RHIZOCEPHALAN PARASITISM OF ALASKA KING CRAB
was inhibited considerably more than in parasitized
male L. aequispina. The condition factor for non-
parasitized male L. aequispina (6.5 ± 0.5) was also
greater at a highly significant level than for male
parasitized crabs (6.1 ± 0.4). The condition factor
in parasitized and nonparasitized male golden king
crabs did not vary significantly with size
Nonparasitized female L. aequispina (n = 77) were
heavier than parasitized females (n = 43) over most
of the length range The linear relationships were
significantly different but not parallel, preventing
a comparison of the intercepts. Condition factors
were not significantly different between the
parasitized (5.9 + 0.5) and nonparasitized (5.7 + 0.4)
females. Condition factors varied significantly with
size and in the nonparasitized crabs but not in the
parasitized crabs.
DISCUSSION
Weights and, consequently, condition factors were
significantly lower in male blue and golden king
crabs parasitized by B. callosus. A difference in mean
weight was also present in female blue king crabs
that were parasitized, although an adequate com-
parable sample size of nonparasitized females was
not available The prevalence of the parasite was con-
siderably greater in king crab populations where sub-
legal or smaller size classes of adult crabs were in-
cluded in the sample number. In blue king crabs from
Glacier Bay, the inclusion of females in the sample
also raised prevalence figures since females had a
significantly higher prevalence of barnacle para-
sitism than male crabs. A potential reason for in-
creased barnacle prevalence in smaller crabs could
include differential mortality such that fewer
parasitized crabs survive to larger size classes. Other
explanations include reduced molting frequencies,
reduced number of instars and/or reduced growth
represented by a reduction in relative molt increment
(Hawkes et al. in press). However, reduced weights
in parasitized crabs within the same size classes as
nonparasitized individuals suggest that growth of the
host crab is decreased by B. callosus. The higher
parasite prevalence in smaller crabs also supports
this conclusion.
Parasitized crabs may develop significantly less
body tissue after molting, which is likely to be a
cumulative effect occurring over more than one
season. Although the complete life history of B.
callosus is unknown, other species of Rhizocephala
are known to require at least 9 to 12 mo to reach
reproductive maturity and develop an externa in host
crabs (Ritchie and H0eg 1981). In males that be-
come castrated and weight loss of testes is insignif-
icant in total body mass (0.2%) and does not account
for the weight difference observed. Also testes weigh
less than the interna and externa of the parasite In
female king crabs a considerable amount of the wet
body weight can be attributed to the egg clutch and
ovaries. Consequently, gonadal atrophy, nonovigerous
conditions and reduced somatic growth rates all may
account for the lesser weights observed in parasi-
tized female king crabs.
The percentages of weight difference between
parasitized and nonparasitized males was con-
siderably different between the two species of king
crabs. Golden king crab was less affected by the
parasite, sustaining less growth inhibition due to bar-
nacle parasitism than parasitized blue king crabs.
Parasitized golden king crabs have significantly
higher hemolymph protein concentrations in com-
parison to either their nonparasitized conspecifics
or parasitized blue king crabs. The additional pro-
tein may be attributed to the presence of lectins,
specific carbohydrate-binding proteins suspected of
playing a role in crustacean immunity (Shirley et al.
1985).
If we are correct, reduced crab growth as an ef-
fect of B. callosus parasitism would conflict with data
from other peltogastrid rhizocephalans (O'Brien and
Van Wyk 1985). Other rhizocephalan species tend
to be more prevalent on larger crab hosts, making
enhanced growth or enhanced survivorship a plaus-
ible effect of parasitism. Another explanation is that
parasitized crabs have less somatic growth and, as
a result, have fewer molts. Molting is a time of
greatest mortality for most decapods, and those with
lower molting frequencies would have greater sur-
vival. The probability of infection may also be greater
in certain size classes. Behavioral differences or
sampling bias could affect the parasite's relative fre-
quency within the host population. Sacculinidae ap-
pear to be distributed differently within host popula-
tions (O'Brien and Van Wyk 1985). Pugettia producta
is a majid crab from California and does not molt
after reaching maturity. When parasitized by the
rhizocephalan Heterosaccus californicus, there is no
significant effect on molt increments of juveniles and
the pubertal molt increment is not affected in adults.
However, P. producta that are parasitized pass
through fewer instars before reaching maturity, and
the mean size of these individuals is significantly less
than in nonparasitized crabs (O'Brien 1984). Blue
crabs, Callinectes sapidus, also have retarded growth
when parasitized by Loxothylacus texanus, with most
adults appearing as miniature adult females (Over-
street 1978).
331
FISHERY BULLETIN: VOL. 84, NO. 2
Prevalence of the parasite as a function of host size
and field length-weight comparisons are still only in-
direct measurements of host growth. Consequently,
further laboratory studies measuring growth directly
in parasitized king crabs are needed to positively
prove our hypothesis.
ACKNOWLEDGMENTS
We thank R. Hakala of the FV Fortune and J.
Donahue of the FV Stormfront for assistance with
field sampling and use of their vessels. Steve Ignell
of the National Marine Fisheries Service's Auke Bay
Laboratory was also very helpful as a consultant on
statistical procedures. Funding was received from
the Research Council of the University of Alaska,
Juneau, and the Alaska Fisheries Research Center
of the University of Alaska (Project number RC/
84-04). A research fellowship was provided by Alaska
Sea Grant for the senior author (CRH).
LITERATURE CITED
BOSCHMA, H.
1970. Notes on Rhizocephala of the genus Briarosaceus, with
a description of a new species. Proc, K. Ned. Akad. Wet.
C73:233-242.
BOSCHMA, H., AND E. HAYNES.
1969. Occurrence of the rhizocephalan Briarosaceus callosus
Boschma in the king crab Paralithodes camtschatica
(Tilesius) in the Northeast Pacific Ocean. Crustaceana 16:
97-98.
EVERHART, W. H., A. W. ElPPER, AND W. D. YOUNGS.
1976. Principles of fishery science Comstock Publ. Assoc.,
Ithaca, N.Y., 288 p.
Hawkes, C. R., T. R. Meyers, and T. C. Shirley.
1985. Parasitism of the blue king crab, Paralithodes platypus,
by the rhizocephalan Briarosaceus callosus Boschma. J. In-
vertebr. Pathol. 45:252-253.
In press. Growth of Alaskan blue king crabs, Paralithodes
platypus (Brandt), parasitized by the rhizocephalan Briaro-
saceus callosus Boschma. Crustaceana.
MCMULLEN, J. C, AND H. T. YOSHIHARA.
1970. An incidence of parasitism of deepwater king crab,
Lithodes aequispina, by the barnacle Briarosaceus callosus.
J. Fish. Res. Board Can. 27:818-821.
O'Brien, J.
1984. Precocious maturity of the majid crab, Pugettia produc-
ta, parasitized by the rhizocephalan barnacle, Heterosaccus
californicus. Biol. Bull. 166:384-395.
O'Brien, J., and P. Van Wyk.
1985. Effects of crustacean parasitic castrators (epicaridean
isopods and rhizocephalan barnacles) on growth of crusta-
cean hosts. In A. Wenner (editor), Crustacean issues 3, Fac-
tors in adult growth, p. 191-218. A.A. Balkema Pubis., Rot-
terdam, Neth.
Overstreet, R. M.
1978. Marine maladies? Worms, germs, and other symbionts
from the Northern Gulf of Mexico. Miss. -Ala. Sea Grant
Consortium, MASGP -78-021, 140 p.
RlCKER, W. E.
1975. Computation, and interpretation of biological statistics
of fish populations. J. Fish. Res. Board Can. Bull. 191, 382 p.
Ritchie, L. E., and J. T. H6eg.
1981. The life history of Lemaeodiscus porcellanae (Cirri-
pedia: Rhizocephala) and co-evolution with its procellanid
host. J. Crustacean Biol. 1:334-347.
Shirley, S. M., T. C. Shirley, and T. R. Meyers.
1985. Hemolymph studies of blue (Paralithodes platypus) and
golden (Lithodes aequispina) king crab parasitized by the
rhizocephalan barnacle, Briarosaceus callosus. In Pro-
ceedings of the International King Crab Symposium, p.
341-352. Alaska Sea Grant Rep. 85-12.
SOMERTON, D. A.
1981. Contribution to the life history of the deep-sea king
crab, Lithodes couesi, in the Gulf of Alaska. Fish. Bull., U.S.
79:259-269.
SOMERTON, D. A., AND R. A. MACINTOSH.
1983. Weight-size relationships for three populations in Alaska
of the blue king crab, Paralithodes platypus (Brandt, 1850)
(Decapoda, Lithodidae). Crustaceana 45:169-175.
Wallace, M., C. J. Pertuit, and A. R. Hvatum.
1949. Contribution to the biology of the king crab, Para-
lithodes camtschatica Tilesius. U.S. Fish. Wildl. Serv. Leafl.
340, 50 p.
332
DISTRIBUTION AND ABUNDANCE OF COMMON DOLPHIN,
DELPHINUS DELPHIS, IN THE SOUTHERN CALIFORNIA BIGHT:
A QUANTITATIVE ASSESSMENT BASED UPON AERIAL TRANSECT DATA
Thomas P. Dohl, Michael L. Bonnell, and R. Glenn Ford1
ABSTRACT
On 35 aerial transect surveys of the Southern California Bight, 157 sightings of common dolphin,
Delphinus delphis, schools were observed and mapped for distributional analysis. Sightings were pooled
into 30' of latitude by 30' of longitude sampling quadrats, and density estimates were obtained by fitting
a Fourier series to a frequency distribution of perpendicular sighting distances. Two distinct seasonal
distributions are represented by density contour maps: a winter-spring distribution when schools were
confined to the easternmost and warmest waters of the area, and a summer-autumn distribution when
schools were widespread. Mean seasonal population estimates were 15,448 for winter-spring and 57,270
for summer-autumn (cv of 0.36 and 0.17, respectively). During the warmer water months, the common
dolphin population expands its use of the Southern California Bight. They enter from the south, apparently
following the major undersea ridges and escarpments, and flow through the Southern California Bight
in a generalized counterclockwise fashion. Observational evidence suggests that there is mixing of both
the nearshore and pelagic forms of this species in the offshore waters over the Santa Rosa-Cortes Ridge
and Patton Escarpment.
The common dolphin, Delphinus delphis, is the most
abundant cetacean in the waters of the Southern
California Bight (SCB). On an annual basis the num-
bers of common dolphins exceed, on average, the
combined total of all other cetaceans in this area by
2.75 times (Dohl et al. 1980).
Common dolphins inhabit subtropical waters of
Mexico and the SCB throughout the year (Norris
and Prescott 1961). Density estimates for this
species and other dolphins (Stenella sp.) in waters
offshore of Mexico and Central America were
calculated by the National Marine Fisheries Service
in 1974 (Smith 1981). The distribution of common
dolphins in the eastern parts of the Southern Califor-
nia Bight was described by Evans (1975).
In order to understand the role of the common
dolphin in the ecology of the SCB and to understand
when and where this population is mostly vulnerable
to human activities, we have constructed a spatial-
seasonal distributional model with two aims: 1) to
generate population estimates for the entire area
and 2) to describe the general features of seasonal
distribution patterns. This is the first study to ex-
amine the spatial heterogeneity of common dolphin
distribution in the SCB and to generate confidence
limits for density and seasonal mean population size
estimates.
'Institute for Marine Sciences, University of California, Santa
Cruz, CA 95064.
Manuscript accepted July 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
From April 1975 through March 1978, nearly
110,000 nmi (200,000 km) of combined aerial and
ship surveys were conducted within the SCB for the
Department of the Interior, Bureau of Land Man-
agement (now the Minerals Management Service).
During this marine mammal and seabird study, a
total of 505 schools of 134,675 Delphinus delphis
were recorded.
This paper is primarily concerned with one subset
of the 3 yr, common dolphin sighting data base. To
avoid the statistical pitfalls of pooling data obtained
from a variety of platforms performing their mis-
sions at different speeds, at different altitudes, and
over varying portions of the study area, we re-
stricted these analyses to 35 monthly flights flown
at 1,000 ft above sea level (ASL). Each of these
surveys required about 15 overwater flight hours
and covered about 1,350 nmi (2,500 km) of track-
line. All species of cetaceans encountered were
recorded as to location, number, behavior, direction
of movement, and number of juveniles. Common
dolphins were encountered 157 times in this flight
series, for a total of 46,153 animals or 69% of all
cetaceans observed.
The results of the distributional study and accom-
panying figures were derived from the 1,000 ft ASL
aerial survey data defined above. However, material
in the Discussion section draws upon observations
made from all survey platforms used during this
study.
333
FISHERY BULLETIN: VOL. 84, NO. 2
METHODS
Aerial surveys were flown at an altitude of 1,000
ft ASL (328 m) at about 90 kn (167 km/h) in a high-
wing, twin-engine Cessna2 337. The crew consisted
of a pilot and three experienced marine mammal
observers, one acting as recorder. Surveys were
flown along 15 parallel, predetermined tracklines,
separated by 15 nmi and extending from the shore
to a maximum distance of 100 nmi (185 km; Fig. 1).
Tracklines were oriented from northeast to south-
west and were roughly perpendicular to the shore-
line, as well as to most major features of submarine
topography in the study area. Whenever possible, all
transect lines were surveyed on each 3-d flight.
Transect lines were not replicated on a single survey,
nor were they flown in a predetermined order or
direction. The first line flown on a given day was oc-
casionally dictated by weather or military activity
in the area; subsequent lines were chosen to optimize
coverage and simplify logistics.
Observers searched unbounded corridors on each
side of the aircraft trackline Sightings were recorded
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
and coded for computer entry at the time of occur-
rence The aircraft was diverted to circle those
schools located off the trackline for positive iden-
tification, animal count, and photographs. The total
animal count recorded for each school was a consen-
sus of the observers on board, derived from multi-
ple orbits of the school. Any additional sightings ob-
tained while "off transect" were not included in later
density calculations due to the possibility that the
secondary sighting was prompted by the first. All
transect segments where observer effectiveness
might have been hampered by fog and/or sea state
were deleted from the data base; only transect seg-
ments where visibility exceeded 1 nmi and the sea
state was Beaufort 3 (few, scattered whitecaps) or
less were retained.
Aerial photographs were used to validate observ-
er estimates of school size. The aerial photographs
were taken on 9" x 9" film from a vertically mounted
camera and on 4" x 5" and 35 mm films in hand-
held cameras for oblique views. The large, 9" x 9"
vertical photographs soon proved to be the most
useful and were used almost exclusively for count
verification. Observer counts and film counts on
average-sized schools (up to 100 animals) varied only
slightly, but not in a consistent manner. The 3-5%
121
120"
119"
118"
117"
SOUTHERN CALIFORNIA BIGHT I
n 120 119" 118"
Figure 1.— Map of the Southern California Bight study area showing aerial survey tracklines.
334
DOHL ET AL.: COMMON DOLPHIN DISTRIBUTION AND ABUNDANCE
variations in counts occurred randomly, with no pat-
tern to indicate in which method the higher counts
would occur. Small schools of <100 animals repre-
sented most of the sightings (53%). In medium-sized
schools, up to 300 animals, the variation was higher
(about 11%), and the photographs indicated probable
observer underestimation in 62% of the counts. The
largest underestimates occurred in large schools,
>300 animals, and were found in 76% of the observ-
er counts. These underestimates ranged up to 30%
in some circumstances. Within the large-school
category, two subcategories became evident: 1) Dis-
persed schools with multiple discrete subgroups of
animals gave the observers less of a problem than
2) the tightly grouped, rapidly moving, compact
schools. The dispersed large schools yielded under-
estimate values in the range of 14-16%, while the
compact, large groups were usually 21-23%. Ex-
tremely large schools of over 1,000 animals were
responsible for the highest error values of up to 30%;
these schools accounted for only 6.6% of total
sightings.
Generally, we found that aerial estimates were
lower than numbers based on photographs and that
the larger the school, the higher the difference. We
attribute some of the difference to the time lag be-
tween when the count was made while circling the
school and the photo run over the center of the
school. Results of photo runs made either before or
after the counting effort did not vary significantly,
but occasionally, continued circling scattered larger
schools into several smaller subgroups.
Sea surface glare affected observation efficiency
to some degree on about 10% of all survey days. Due
to the orientation of transect lines, glare conditions
could impair the search ability of only the left-side
observer on southwest-bound legs (up to 26% of total
search effort per survey day). Holt (19843) found
density estimates of dolphin schools to be 39% lower
under poor sun conditions than during good sun con-
ditions. Using his figure, we calculate that our over-
all seasonal density estimates might be low by about
1%. Because of the lack of any systematic bias
resulting from glare affecting density estimates in
one particular region or season more than another,
we made no corrections to adjust for this slight
underestimate.
The perpendicular distance from the trackline to
the sighting was calculated from the declination
angle obtained using a hand-held inclinometer. Per-
pendicular distances were recorded for 112 sightings
of common dolphin schools, representing 74.2% of
all sightings used in density calculations.
Distributional Model
Inspection of the first year's common dolphin
sighting numbers and plots of monthly distribution
indicated seasonal fluctuations of residency within
the Southern California Bight.
Examination of the 3-yr database showed two
distinct seasons of occupancy for the species in the
SCB (Fig. 2). A comparison of the two sets of data
on a monthly basis show a significant statistical dif-
ference (^(1,34) = 7.66, P < 0.01). In view of these
observations, two seasons were defined for the
development of the distributional model: a summer-
autumn season (July through December) when com-
mon dolphin sightings were widespread in the SCB,
and a winter-spring season (January through June)
when most schools were confined to the southeast-
ern portion of the surveyed area. Common dolphin
sightings were assigned by their latitude and longi-
tude to 30' x 30' grid-cells (sampling quadrats)
centered on degree and half-degree lines of latitude
and longitude. Data were pooled to provide seasonal
estimates of common dolphin abundance for each
30' x 30' grid-cell. The estimate of density of groups
in cell i, Dh was calculated from the relationship:
Di = nlf{Q>)IZLl (Burnham et al. 1980)
(1)
3Holt, R. S. 1984. Testing the validity of line transect theory
to estimate density of dolphin schools. U.S. Dep. Commer.,
NOAA Admin. Rep., NMFS-SWFC LJ-84:31, 56 p.
where n{ is the number of groups encountered, /(0)
is the probability density function of perpendicular
distances evaluated at the ^-intercept, and h% is the
sum of all transect lengths in cell i contributing to
the seasonal estimate. The value of the f(0) term
was calculated using the nonparametric Fourier-
series estimator of Crain et al. 1978 (see Burnham
et al. 1980 for a complete discussion of this esti-
mator). Computations were made employing the
program TRANSECT (Laake et al. 1979). For calcu-
lation of the/(0) term, the perpendicular distance
of each sighting was reduced by one-half the width
of the exclusion area under the aircraft, where
visibility was obstructed by the fuselage (total ex-
clusion area = 530 ft at 1,000 ft ASL). This ap-
proach, in effect, moves the transect centerline out-
board to the point of nearest possible sighting
distance— a point where it is assumed that all
animals present will be seen and counted. The ques-
tion of how to deal with the problem of restricted
downward visibility and line transect theory has
been considered by others; however, the best treat-
335
FISHERY BULLETIN: VOL. 84, NO. 2
7000
6000
5000
4000
3000
2000
1000
1 = Winter (Jan., Feb., March)
2 = Spring (April, May, June)
3 - Summer (July, Aug., Sept.)
4 = Autumn (Oct., Nov., Dec.)
Figure 2.— Comparison of total counts of common dolphins on aerial surveys of the
Southern California Bight by season, 1975-78.
ment of the subject, in print, is found in two papers
by Leatherwood et al. (1982, 1983).
Because sample size was small in each grid-cell
and in each season, data were combined to calculate
a single value of f(0). The pooling of data was based
on the assumption that the sightability of common
dolphin groups did not vary between seasons or be-
tween regions of the surveyed area. Violation of this
assumption would lead to biases in the estimates of
relative densities between seasons or regions, al-
though it would not necessarily effect mean popula-
tion size estimates. The assumption of seasonal
homogeneity was tested using a single classification
ANOVA (two groups, unequal samples; Sokal and
Rohlf 1969, p. 208). No significant difference be-
tween the distribution of perpendicular sighting
distances collected in summer-autumn and winter-
spring seasons was found (F1(111 = 2.01, P = 0.18).
The same test was used to compare frequency
distributions with distance of sightings collected in
calmer inshore waters, with sightings collected in
rougher offshore waters, since this seemed to be the
most likely source of bias in sightability. No signifi-
cant difference was found between the distribution
of perpendicular sighting distances in the two sub-
regions (F1>108 = 1.78, P = 0.20).
The rescaled frequency distribution of perpendi-
cular sighting distance is shown in Figure 3. The
probability density function, f(x), is from a three-
term, Fourier-series model, which provides the best
fit to these data (x2 = 6.026, df = 3, P = 0.11).
Data were truncated at 6,600 ft in order to remove
two extreme values. Intervals were specified, by in-
spection of the data, in order to smooth the func-
tion and minimize the effects of "heaping" in per-
pendicular distance measurements (Burnham et al.
1980, p. 47).
For estimation of common dolphin density (ani-
mals/km2) in a given grid-cell for a given season,
we multiplied the density of groups in a given cell
336
DOHL ET AL.: COMMON DOLPHIN DISTRIBUTION AND ABUNDANCE
by the mean group size throughout the SCB ob-
tained for that season. The small sample size in any
cell and the very large variability in the size of
groups necessitated pooling of all sightings within
a season to calculate mean group size. The mean
group size in summer and autumn was 338 ± 38 SE
(n = 115), while that of winter and spring was 231
± 73 SE (n = 36). While not significantly different
(^1,149 = 1-42, P > 0.25), we used separate mean
group size in calculations of seasonal abundance. We
tested the assumption that mean group size in each
season was constant throughout the SCB, using a
bootstrap procedure (Efron 1982). For a given
season, cell i contained n{ observations of groups
of mean size s{. For each cell i, we randomly drew
10,000 sets of values of size n{ from the group size
distribution based on all observations recorded in
that season, computed the mean of this subsample,
and formed a frequency distribution of these mean
values. If the percentile ranking of the observed
mean group size in cell i was >97.5% or <2.5%,
s, was assumed to be a nonrandom sample. For the
summer-autumn season, only 1 cell of the 26 cells
containing observations of common dolphins had
means which differed significantly from the rest of
the surveyed area. Similarly, for the winter-spring
season, only 1 cell in 10 showed a significant dif-
N = 112
.13 .27 .40 .67 .94
DISTANCE IN KM
1.22 1.48
Figure 3.— Probability density function f(X) fit to histogram of
sighting frequency and perpendicular distance (rescaled; see text).
ference from the overall group size distribution.
Therefore, group size homogeneity was assumed for
these data, and a single seasonal value of mean
group size (s) was used in all calculations of cell
density for each season.
If f(0) and s may be assumed to be homogeneous,
the remaining source of between-cell variability is
the density of groups. We tested the hypothesis that
the density of groups is homogeneous through the
SCB as follows: taking the mean number of sight-
ings of common dolphin schools per kilometer of
transect for the entire surveyed area, A*. We com-
puted the expected number of cells containing a
specified number of sightings of groups, using the
formula:
[Expected number of cells with k sightings] =
1 e-rL. (A*L^
(2)
i=i
where m is the total number of cells sampled, k is
the specified number of sightings of groups, and L%
is the length of trackline surveyed in cell i. The ex-
pected number of cells containing k sightings were
compared with the observed number for all k using
a chi-square test. No significant spatial heteroge-
neity was evident for data collected in summer and
autumn (x2 = 5.06, df = 5, P > 0.5). However, the
winter and spring distribution showed clear heter-
ogeneity in the density of groups by cell (x2 =
12.85, df = 3, P < 0.005).
We used the method of Chernoff and Moses (1959)
to place confidence limits on the estimate of the
number of groups per km of transect in cell i, A;
(see also Clopper and Pearson 1934). We used a com-
puter program which finds a density value, r1( such
that the probability of observing n% or more groups
in a transect segment of length L{ is 0.025; this is
the lower confidence bound on A,. Similarly, we find
a density value, r2, such that the probability of ob-
serving n{ or fewer groups is 0.025; this forms the
upper bound on A^. Tx and V2 are defined as satis-
fying the equations:
and
k = n.
k = n
k\
= 0.025
(3)
2. \J_±L = o>025.
*=o
k\
(4)
337
FISHERY BULLETIN: VOL. 84, NO. 2
Such confidence limits are asymmetric about Xx and
decrease in size with increasing transect coverage.
They have the important properties that r2, the up-
per limit, tends to be large when the transect length
L; is small, even when the number of groups ob-
served is zero, and the lower limit r1 is bounded by
zero.
Population size estimates were made for each cell
i in each season from the relationship N{ = D{ • s
• A{, where N{ is the cell population, Dt is the
estimated density of groups based on Equation (1)
(groups/km2), s is the seasonal mean group size,
and A{ is the open-water area of cell i. Total
population size in each season, (N), was estimated
as from the sum of populations in each cell, and from
the theoretical formula:
-T w/(0) _ .
N = J -s-A
2L
(5)
where n is the total number of groups observed, L
is the total transect length, s is the seasonal mean
group size, and A is the areal extent of the study
area. The variance of N was estimated from the rela-
tionship (K. Burnham4).
var (N) = A2 ■ var 0,)
(6)
where var 0t) = 0,)2
var(s)
(E(i)f
var(n) var(/"(0))
(E(n)f (£(A0)))2
+
. The variance of n was calculated assum-
ing that n had a Poisson distribution; if this assump-
tion holds, var(n) = n (Burnham et al. 1980).
The variance of /(0) was calculated by program
TRANSECT, using the method of Burnham et al.
(1980). Variance of s was estimated as the standard
error of the mean group size. The formula for
variance requires that/(0) and s be independent, an
assumption that may be violated due to the diff eren-
4K. Burnham, Department of Statistics, School of Physical and
Mathematical Sciences, North Carolina State University, Raleigh,
NC 27650-5457, pers. coramun.
Figure 4.— Common dolphin distribution in the Southern California Bight, winter and spring, 1975-78. Density contours show
animals/km2.
338
DOHL ET AL.: COMMON DOLPHIN DISTRIBUTION AND ABUNDANCE
tial sightability of large and small groups (discussed
below). Because we could not be sure that the
assumptions of the theoretical formula were met,
we also calculated the variance of population size
for the summer-autumn season, using a jackknife
estimator (Miller 1974; Burnham et al. 1980).
Pseudovalues of the area-wide population were
generated by sequentially deleting pairs of surveys
from the database. All sources of variance were con-
sidered in estimation of total variance: /(0), mean
group size, and spatial variability of sightings.
Because of the small number of perpendicular sight-
ing distances for winter-spring season (31), we were
unable to obtain a stable value of /(0), thus pre-
cluding the estimation of jackknife variance of that
season.
Distribution maps were prepared using Surface
Display Library software (Dynamic Graphics, Inc.,
Berkeley, CA). Contour lines, generated by linear
interpolation between density values assigned to
grid-cell centerpoints, were smoothed using a cubic
spline function.
RESULTS
Two distinct seasonal distributions were found for
common dolphins in the Southern California Bight
(SCB). In winter and spring months (January
through June), common dolphin sightings were
almost completely confined to the eastern part of
the SCB (Fig. 4). Within the area occupied, three
cells in the southernmost rank and one shore-
bounded cell north of San Diego showed significantly
higher density than the overall seasonal mean (P >
0.95 in all cases). In summer and autumn months
(July through December), common dolphin sightings
were widespread from Rodriguez Seamount and the
Patton Escarpment in the west to the mainland
shore in the east (Fig. 5). Cell density estimates in
this season were relatively homogeneous through-
out the area. Only a single cell in the San Diego
Basin could be shown to be significantly higher than
the seasonal mean at the P > 0.95 level. Neverthe-
less, we believe that the clustering of moderately
high-density cells east of Santa Catalina and San
Figure 5.-Common dolphin distribution in the Southern California Bight, summer and fall, 1975-78. Density contours show
animals/km2.
339
FISHERY BULLETIN: VOL. 84, NO. 2
Clemente Islands and west of San Nicolas Island
represents a real distributional pattern.
Cell-density estimates and 95% confidence limits
are provided in Tables 1 and 2. Confidence limits
were calculated considering only sampling error due
to number of groups sighted (Equations (3) and (4))
and not uncertainty in/(0) or mean group size. Sam-
pling error associated with the number of groups
sighted was the dominant source of variation in cell-
by-cell estimates of density, typically exceeding
variance of the/(0) term by three times and variance
associated with mean group size by five times. It
should be remembered that the density estimates
are mean values computed from pooled data col-
lected over a several month period in 3 successive
years.
From these density estimates, we computed
seasonal mean population size estimates. By cal-
culating population size as the sum of the numbers
in each 30' x 30' cell, we estimate a winter-spring
population of 15,448 animals. This figure is a mean
population occurring in the months of January
through June and includes months of higher and
lower numbers. Using Equation (5), we calculate a
theoretical winter-spring population size of 18,933
animals. This second estimate for the SCB, based
on pooled data, may be high because survey effort
was 6.7% greater in the higher density parts of the
study area in winter and spring. Based on Equation
(6), the coefficient of variation of the winter-spring
population was 36%. The coefficients of variation
for number of groups, f(0), and mean group size
were 16%, 8%, and 31%, respectively. The relatively
large variability in mean group size was due to a
Table 1.— Relative abundance of common dolphins in the winter and spring. Mean density (animals/
km2) is provided for each 30' x 30' cell; latitude and longitude indicate center point of cell. Upper and
lower values are 95% confidence limits derived from the spatial variability of sightings along aerial transect
lines.
121 °00'
120°30'
120°00'
119°30'
119°00'
118°30'
118°00'
117°30'
7.41
1.71
1.33
2.42
34°30'
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
3.42
1.05
0.81
0.62
0.86
1.28
34°00'
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
5.32
1.19
0.90
1.05
0.48
1.09
1.81
33°30'
0.00
0.00
0.00
0.19
0.10
0.43
0.00
0.00
0.00
0.00
0.05
0.00
0.19
0.00
4.89
1.71
0.76
1.14
1.38
2.00
33°00'
0.00
0.48
0.00
0.33
0.48
0.95
0.00
0.14
0.00
0.10
0.19
0.48
1.24
0.71
1.95
2.57
2.80
32°30'
0.00
0.00
0.76
1.09
1.38
0.00
0.00
0.33
0.48
0.67
Table 2.— Relative abundance of common dolphins in the summer and fall. Mean density (animals/km2)
is provided for each 30' x 30' cell; latitude and longitude indicate the center point of cell. Upper and
lower values are 95% confidence limits derived from the spatial variability of sightings along aerial transect
lines.
121°00' 120°30' 120°00'
119°30'
119°00' 118°30' 118°00' 117°30'
34°30'
34°00'
33°30'
33°00'
32°30'
3.53
1.45
1.32
3.12
0.00
0.00
0.00
0.05
0.00
0.00
0.00
0.14
1.80
1.04
1.25
1.52
2.15
2.08
0.35
0.21
0.35
0.62
0.83
0.35
0.07
0.07
0.07
0.28
0.35
0.07
5.82
2.70
1.73
2.70
2.15
1.25
2.56
1.04
1.04
0.62
1.25
1.25
1.42
0.48
0.28
0.42
0.21
0.55
0.76
0.14
0.14
4.92
2.29
2.91
2.56
4.09
2.98
1.66
0.76
1.32
1.25
2.56
1.66
0.62
0.28
0.62
0.62
1.59
0.90
2.49
2.08
1.94
3.39
3.12
0.69
0.83
0.69
1.45
1.66
0.21
0.35
0.21
0.62
0.90
340
DOHL ET AL.: COMMON DOLPHIN DISTRIBUTION AND ABUNDANCE
single sighting of 2,450 animals; we choose not to
treat this observation as an outlier because the oc-
casional occurrence of very large groups is typical
of this species.
For the summer-autumn season of greatest abun-
dance, the stock size estimate based on summing in-
dividual cell populations and the estimate derived
from Equation (5) were 57,270 and 46,675, respec-
tively. The theoretical estimate based on pooled data
may be low because survey effort was 7.8% greater
in the lower density parts of the study area in the
summer-autumn season (i.e., the offshore waters in
the west). The coefficient of variation computed
from the theoretical variance formula (Equation (6))
was 17%. Coefficients of variation for number of
groups, /(0), and mean group size were 9%, 8%, and
11%, respectively. The jackknife estimator gave a
higher coefficient of variation for population size of
27%. Components of this estimate for number of
groups, /(0), and mean group size were 15%, 18%,
and 14%, respectively. Differences between the two
types of estimators may be due, in part, to the in-
herently conservative nature of the jackknife (Efron
1982), but probably result primarily from within-
survey correlation of variables. In addition, the jack-
knife estimate of /(0) relied on a smaller subset of
sighting distances measured only during summer-
autumn surveys (n = 81).
DISCUSSION
Even in an area as heavily utilized as the South-
ern California Bight, sightings of common dolphin
schools are not common events. For this reason it
was necessary to pool aerial survey data collected
over several months in each of three years to
describe their distribution in statistical terms. The
two seasonal views of common dolphin distribution
in the SCB are shown for contrast in Figures 4 and
5. It is apparent that the population makes season-
ally greater use of the SCB in summer and autumn
months. The months of greatest numbers, based on
sightings per km of trackline, were September
through November. During these months, the popu-
lation far exceeds the mean value of 57,000 and
probably approaches 100,000 animals.
A potential source of bias in our mean population
size estimates was the differential sightability of
groups of various sizes. The detection function for
common dolphin sightings declined sharply beyond
about 1,650 ft (500 m), suggesting that mostly large
or conspicuous groups were seen at relatively great
distances. The Fourier estimator is robust to varia-
tion in sighting efficiency (Burnham et al. 1980). For
comparison, the/(0) term of 2.29 for common dol-
phins was quite close to the/(0) estimate of 2.16
more recently obtained for 136 sightings of Pacific
white-sided dolphin schools on aerial surveys off-
shore of central and northern California (Dohl et al.
1983). However, variable sighting effectiveness may
also bias the estimation of mean group size. Holt and
Powers (1982) found that smaller groups of dolphins
were more likely to be missed on aerial surveys than
larger groups, resulting in a 25% overestimation of
mean group size. For our data on common dolphins,
we did not find a significant difference in mean
group size between sightings within the first 1,650
ft and beyond due to high variability in sightings size
(213 ± 46 SE, n = 65, compared with 308 ± 49 SE,
n = 50; Fin3 = 1.94, P = 0.18). Nevertheless, our
calculations show that stratification of mean group
size by distance from the trackline (< 1,650 ft and
>1,650 ft) would result in an 18% decrease in mean
density values.
The distribution shown for summer and autumn
can be viewed as a composite of monthly distribu-
tions. Common dolphin distribution expands from
the southeast into the central and western parts of
the SCB in late spring and early summer and
recedes toward the east and south in late autumn
and early winter. Common dolphin movement into
and out of the SCB appears to be temperature
related. As sea surface temperatures (SST) rise in
late spring-early summer, animals begin to be
sighted more often along the Coronado Escarpment.
Peak numbers of common dolphins were found in
open water regions of the SCB 3-5 wk after intru-
sion of the warmer waters. During cool-water
months, when SSTs down to 10.0°C were recorded
and the SCB-wide mean was 14.6°C, no animals
were observed in waters cooler than 14.0° C.
Distributional patterns of the common dolphin
within the SCB may be changing. Hui (1979) ana-
lyzed data collected on Naval Ocean Systems Center
(NOSC) surveys from 1968 through 1976 and
showed no common dolphin sightings north of Point
Vincente (lat. 33°45'N) or west of approximately
San Nicolas Island. Our surveys in summer and
autumn months found 29.9% of all sightings and
30.8% of all animals occurred in the northern and
western portion of the SCB— an area largely un-
sampled by the NOSC surveys. Hui's results agreed
with those of Evan's (1975), who found only a small
fraction of the total sightings recorded on aerial and
shipboard surveys to occur in this northern and
western portion of the SCB; however, aerial sam-
pling effort in Evan's earlier study also favored the
inshore and southern portions of the SCB.
341
FISHERY BULLETIN: VOL. 84, NO. 2
Based upon the distribution of sightings on our
bimonthly aerial surveys, movement of common
dolphins into the SCB appeared to follow the net-
work of escarpments and seamounts noted by Evans
(1971). The major corridor was along the Coronado
Escarpment to Thirty-Mile Bank, up to the Cata-
lina Escarpment, around both sides of Santa Cata-
lina Island, along the western margins of the San
Pedro and Santa Monica basins to Santa Cruz and
Santa Rosa Islands (Fig. 1). The population front
then advanced westward along the southern margin
of these islands until reaching the Santa Rosa-Cortes
Ridge where it shifted south, spreading out along
the western slope of this prominant underwater
feature. Some elements of this influx stopped and
along the way, increasing summer-autumn popula-
tions significantly in the San Pedro Channel, Gulf
of Santa Catalina, and, to a lesser extent, in near-
shore waters from Dana Point to La Jolla. A sec-
ondary pathway was from Forty-Mile Bank in the
south, up the San Clemente Escarpment west of San
Clemente Island to reach the Santa Rosa-Cortes
Ridge area.
During periods of peak occupancy common
dolphin sightings west of long. 119°W were dis-
tributed along the western slope of the Santa Rose-
Cortes Ridge centered at lat. 33°00'N, long.
120°00'W. As waters cooled, the distributional
center shifted eastward to locate over the eastern
slope of the Santa Rosa-Cortes Ridge at 33°00'N,
119°20'W, while a smaller element moved north-
westerly to a new location around 33°30'N,
120°30'W. With continued cooling of the western
waters, the majority of the animals along the east-
ern edge of the Ridge appeared to move southeast-
erly to merge with existent populations south and
east of San Clemente Island. The remaining small
number of animals wintering-over moved westward,
centering near 33°00'N, 119°30'W, south of San
Nicolas Island.
The destination of common dolphins that moved
northwesterly from the summering grounds over
the western edge of the Santa Rosa-Cortes Ridge
is unknown. However, several pieces of incomplete
evidence lead us to believe that they are part of a
"pelagic" population that returns in late autumn or
early winter to offshore waters over the Rodriguez
Seamount or Patton Escarpment. During several
midsummer ship surveys and three aerial surveys
of offshore waters over the Patton Escarpment and
San Juan Seamount, we recorded sightings of large
schools of robust-bodied, brilliantly marked,
"pelagic" common dolphins. On two occasions, our
crew on the catch boat head-netted, brought on
board, photographed, measured, tagged, freeze-
branded, and released, examples of these "pelagic"
animals from within schools containing predom-
inantly the paler, smaller, nearshore variety of
Delphinus. Ships' logs indicate that the presence of
these "pelagic" animals increased with distance
from shore, and percentages as high as 50% were
found in mixed schools of common dolphins at the
western boundary of catch trips, usually south of
lat. 33°45'N and west of long. 120°00'W. West of
the Patton Escarpment, mixed schools were not
noted, and the few schools encountered contained
only "pelagic" animals (Dohl unpubl. data).
In summary, this study establishes an extended
distributional range of the common dolphin within
the SCB, identifies areas of significantly greater
seasonal use, and provides seasonal mean popula-
tion estimates. Our results confirm the findings of
earlier studies that common dolphins move into the
SCB following major features of underwater topog-
raphy in response to increasing seasonal water
temperatures. Observations on surveys also seem
to indicate that most of the population moves
through the SCB in a generalized counterclockwise
direction, and that the western summer-autumn
population is augmented by an influx of "pelagic"
animals from far offshore.
ACKNOWLEDGMENTS
The original data for this paper were collected
under contract to the University of California, Santa
Cruz, from the Minerals Management Service
(formerly a part of Bureau of Land Management),
U.S. Department of the Interior.
The analysis of these data and the development
of the distributional model described here were sup-
ported by Woodward-Clyde Consultants (WCC),
Walnut Creek, CA, by a contract from the Minerals
Management Service, Department of the Interior.
We are grateful to the many individuals involved
in the collection of these data: J. D. Bryant, R. C.
Guess, J. D. Hall, L. J. Hobbs, M. W. Honig, K. S.
Norris, and P. N. Sund. We also thank T. P. Win-
field and R. K. Christiansen at WCC for technical
assistance, and particularly K. P. Burnham, T. D.
Smith, and R. S. Holt for valuable assistance and
comments on the manuscript.
LITERATURE CITED
Burnham, K. P., D. R. Anderson, and J. L. Laake.
1980. Estimation of density from line transect sampling of
biological populations. J. Wildl. Manage. Manage. Monogr.
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72, 202 p.
Chernoff, H., and L. E. Moses.
1959. Elementary decision theory. John Wiley and Sons,
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Clopper, C, and E. S. Pearson.
1934. The use of confidence or fiducial limits illustrated in
the case of the binomial. Biometrika 26:404-413.
Crain, B. R., K. P. Burnham, D. R. Anderson, and J. L. Laake.
1978. A Fourier-series estimator of population density for line
transect sampling. Utah State Univ. Press, Logan, 25 p.
Dohl, T. P., K. S. Norris, R. C. Guess, J. D. Bryant, and
M. W. Honig.
1980. Cetacea of the Southern California Bight. Part II of
summary of marine mammal and seabird surveys of the
Southern Calfiornia Bight Area, 1975-1978. Final Report
to the Bureau of Land Management, 414 p. [Available at
U.S. Dep. Commer., Natl. Tech. Inf. Serv., Springfield, VA
as NTIS Rep. #PB81248189.]
Dohl, T. P., R. C. Guess, M. L. Duman, and R. C. Helm.
1983. Cetaceans of central and northern California,
1980-1983: Status, abundance, and distribution. Final
report to the Minerals Management Service, Contract #14-
12-0001-29090, 284 p.
Efron, B.
1982. The jackknife, the bootstrap, and other resampling
plans. The Society for Industrial and Applied Mathematics,
Philadelphia, PA.
Evans, W. E.
1971. Orientation behavior of delphinids: radio-telemetric
studies. Ann. New York Acad. Sci. 188:142-160.
1975. Distribution, differentiation of populations, and other
aspects of the natural history of Delphimcs delphis Linneaus
in the northeastern Pacific. Ph.D. Thesis, Univ. California,
Los Angeles, 164 p.
Holt, R. S., and J. E. Powers.
1982. Abundance estimation of dolphin stocks involved in the
eastern tropical Pacific yellowfin tuna fishery determined
from aerial and ship surveys to 1979. U.S. Dep. Commer.,
NOAA Tech. Memo. NMFS-SWFC-23, 95 p.
Hui, C. A.
1979. Undersea topography and distribution of dolphins of
the genus Delphinus in the Southern California Bight. J.
Mammal. 60:521-527.
Laake, J. L., K. P. Burnham, and D. R. Anderson.
1979. User's manual for program TRANSECT. Utah State
Univ. Press, Logan, 26 p.
Leatherwood, S., A. E. Bowles, and R. R. Reeves.
1983. Endangered whales of the eastern Bering Sea and
Shelikof Strait, Alaska: Results of aerial surveys, April 1982
through April 1983, with notes on other marine mammals
seen. Final report to NOAA/OCSEAP, Juneau, AK.
Leatherwood, S., I. T. Show, Jr., R. R. Reeves, and M. B.
Wright.
1982. Proposed modification of transect models to estimate
population size from aircraft with obstructed downward
visibility. Int. Whaling Comm. 32:577-580.
Miller, R. G.
1974. The jackknife— a review. Biometrika 61:1-15.
Norris, K. S., and J. H. Prescott.
1961. Observations on Pacific cetaceans of California and
Mexican waters. Univ. Calif. Publ. Zool. 63:291-402.
Smith, T. D.
1981 . Line-transect techniques for estimating density of por-
poise schools. J. Wildl. Manage. 45:650-657.
SOKAL, R. R., AND F. J. ROHLF.
1969. Biometry. W. H. Freeman and Co., San Franc, 776
P-
343
CETACEAN HIGH-USE HABITATS OF
THE NORTHEAST UNITED STATES CONTINENTAL SHELF1
Robert D. Kenney and Howard E. Winn2
ABSTRACT
Results of the Cetacean and Turtle Assessment Program previously demonstrated at a qualitative level
that specific areas of the continental shelf waters off the northeastern U.S. coast consistently showed
high-density utilization by several cetacean species. We have quantified, on a multispecies basis and with
adjustment for level of survey effort, the intensity of habitat use by whales and dolphins, and defined
areas of expecially high-intensity utilization. The results demonstrate that the area off the northeast United
States, which is used most intensively as cetacean habitat, is the western margin of the Gulf of Maine,
from the Great South Channel to Stellwagen Bank and Jeffreys Ledge Secondary high-use areas include
the continental shelf edge and the region around the eastern end of Georges Bank. High-use areas for
piscivorous cetaceans are concentrated mainly in the western Gulf of Maine and secondarily at mid-shelf
east of the Chesapeake region, for planktivores in the western Gulf of Maine and the southwestern and
eastern portions of Georges Bank, and for teuthivores along the edge of the shelf. In general, habitat
use by cetaceans is highest in spring and summer, and lowest in fall and winter.
From October 1978 through January 1982, the Ceta-
cean and Turtle Assessment Program (CETAP) at
the University of Rhode Island conducted surveys
of the waters of the U.S. continental shelf from Cape
Hatteras, NC, to the northern Gulf of Maine. The
purpose of these surveys was to provide data on the
distribution and abundance of whales, dolphins, and
sea turtles inhabiting the northeast shelf for input
to decision-making relative to offshore oil and gas
resource development. Twenty-six species of ceta-
ceans were observed during the study, and their
distributions have been described in some detail
(CETAP 1982). Each species exhibited a distinctive
pattern of distribution in space and time, inhabit-
ing some small portion(s) of the study area at higher
relative densities.
When comparing distributions of individual
species, there appear to be specific geographic areas
which consistently contained higher abundances of
several cetacean species. This phenomenon had been
noted during the CETAP study (CETAP 1982), but
had not been analyzed quantitatively. An individual
species approach to the analysis of such multispecies
phenomena has certain limitations. One cannot
simply combine the sighting distributions of several
species; the different cetacean species vary widely
'This report has been reviewed by the Minerals Management Ser-
vice and approved for publication. Approval does not signify that
the contents necessarily reflect the views and policies of the Ser-
vice, nor does mention of trade names or commercial products con-
stitute endorsement or recommendation for use
2Graduate School of Oceanography, University of Rhode Island,
Narragansett, RI 02882-1197.
Manuscript accepted July 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
in size and may have quite different ecological
requirements. An additional complication in a study
of habitat use, based on sighting data, is introduced
by the uneven allocation of sighting effort. One can-
not be certain whether a lack of sightings is due to
absence of whales or absence of observers, or, con-
versely, whether a concentration of sightings repre-
sents a real concentration of whales or simply a con-
centration of effort. Thus it is difficult to simply or
directly combine single-species sighting distributions
in any sort of multispecies habitat use analysis. In
this paper, we have attempted to synthesize, from
the CETAP individual species sighting data, a mea-
sure of the intensity of habitat use by the total ceta-
cean fauna in the study area which accounts for both
interspecific differences and differences in allocation
of effort. These results then serve to delineate those
specific habitat areas which are used at particularly
high levels by whales and dolphins off the north-
eastern United States.
An underlying assumption in this paper is that a
habitat which is occupied by whales or dolphins is
necessarily utilized by them. Previous results from
CETAP data have shown that the distribution of
sightings of a particular species where definite
feeding behavior was observed tended to closely mir-
ror the overall sighting distribution for that species.
Only feeding activity at or very near the surface can
be seen by observers on ships or airplanes, but much
feeding behavior likely occurs below the surface For
some species, observations of surface feeding are
very rare. In addition, cetaceans are large mammals
345
jyr-^?-
FISHERY BULLETIN: VOL. 84, NO. 2
with high metabolic rates and accordingly high feed-
ing rates. They are estimated to consume prey equi-
valent to 1.5-4% of their body weight daily (Sergeant
1969; Lockyer 1981), with some estimates for
smaller species as much as 10% of body weight per
day (eg. Smith and Gaskin 1974). The CETAP study
concluded that cetaceans "would be expected to feed
virtually every day while in the study area" and that
"each species of cetacean was likely feeding, either
at the surface or below, in any area in which it was
seen regularly" (CETAP 1982, p. 417). For the pur-
poses of the current study, we have also followed this
reasoning and assumed that a habitat which is be-
ing occupied by one or more cetacean species is
therefore being utilized by those species as a feed-
ing area.
METHODS
The CETAP study area was defined as the waters
of the U.S. continental shelf north of Cape Hatteras,
from the shoreline to 5 nmi (9.3 km) seaward of the
1,000 fathom (1,829 m) isobath. Surveys were con-
ducted from October 1978 through January 1982.
Data collected from two types of surveys have been
used in this analysis:
1) Dedicated aerial surveys: Random transect
aerial surveys were conducted in defined blocks
within the study area, including both regular surveys
throughout the year and special surveys targeted at
endangered species, particularly right whales. The
primary objective of these surveys was to estimate
the absolute abundance, e.g., the total number of in-
dividuals in the population, of each species in the
study area, using line transect census methods
(Burnham et al. 1980; Scott and Gilbert 1982). This
methodology requires consistent use of rigorously
standardized sampling, e.g., use of the same plat-
form, even allocation of sampling across the different
blocks, and random selection of transects within a
block.
The two aircraft used for these surveys were a
Beechcraft3 AT-11 and a Cessna 337-G Skymaster,
both twin-engine planes. The ATI 1 crew consisted
of a pilot, a navigator, and four observers; two
observers at a time were stationed in a clear acrylic
observation bubble in the nose of the plane The Sky-
master carried a pilot, a navigator, and two observ-
ers, who sat in the rear seats and watched out the
side windows. All surveys were conducted at an
'Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
altitude of 750 ft (229 m) and a groundspeed of 120
kn (222 km/h).
For any particular survey, a series of parallel track
lines was flown. For the regular surveys, the lines
sampled were randomly chosen from a pool of lines
running northwest-southeast (roughly perpendicular
to the bathymetry) and spaced at 2 nmi intervals
throughout the block to be sampled. For the en-
dangered species surveys, the lines were systema-
tically spaced at a predetermined interval, with the
first line placed at a randomly determined distance
from the edge of the block.
2) Platforms of opportunity (POP) surveys: Trained
observers were placed aboard various ships and air-
craft operating within the study area in order to col-
lect distributional data to supplement the dedicated
surveys. The platforms most often used included
Coast Guard cutters, U.S. and foreign oceanographic
and fisheries research vessels, and Coast Guard fish-
eries patrol and thermography aircraft. The track
of the ship or aircraft was wholly determined by its
primary mission. These data could not be used in
abundance estimation because effort was not al-
located randomly or evenly, and the platforms used
were not exactly comparable
Observers on both types of surveys recorded a
variety of information. The data collected included
date, time, latitude and longitude, platform heading,
beginning and end of periods when the observer(s)
were actively on watch, and environmental informa-
tion (air temperature, water temperature, depth,
weather, visibility, sea state, wind direction, and
cloud cover). The data were recorded at each sight-
ing, as well as at periodic intervals (typically 5 min
for aerial and 30 min for shipboard surveys) during
all on-watch periods. This allowed for subsequent
reconstruction of flight-cruise tracks. Additional
data recorded at sightings included species, reliabil-
ity of identification, number of animals, distance
from the platform, animal heading, and behaviors.
The data were transcribed from the field forms
to coding forms, keypunched, and input to a com-
puter data base A number of quality control steps
were included in the process, and all discovered er-
rors were corrected. In addition to the two types of
survey data described above, historical sighting data
collected prior to CETAP and opportunistic sight-
ing data provided by fisherman, mariners, whale-
watchers, fish-spotters, pilots, etc are included in the
CETAP data. None of these data have associated
track-line information, and are therefore not in-
cluded in this paper. After completion of the CETAP
346
KENNEY and WINN: CETACEAN HIGH-USE HABITATS
study, the entire data base was archived on magnetic
tape at the University of Rhode Island Academic
Computer Center. The data base is very large, com-
prising nearly 70,000 entries and 112 variables; it
includes almost 25,000 sightings of cetaceans, sea
turtles, or other large marine animals (eg., sharks,
ocean sunfish, swordfish, rays, etc.).
For this paper, the study area was partitioned in-
to blocks measuring 10 minutes of latitude by 10
minutes of longitude The area of the blocks ranges
from about 243 km2 at the northern extreme of the
study area to about 281 km2 at the southern end,
due to the curvature of the earth's surface and
resulting convergence of the meridians toward the
north pole The data were further grouped by calen-
dar seasons across all the years of sampling. All
dedicated aerial and POP data which met defined
criteria were included in the analysis. These criteria
included observer(s) formally on watch, clear
visibility of at least 2 miles, and sea states of Beau-
fort 3 or lower. Although the dedicated aerial and
POP data were not directly compatible for the pur-
pose of absolute abundance estimation, we are
justified in combining them for this analysis. An ex-
amination of sighting effort in the 1979 CETAP data
(Hain et al. 1981) demonstrated a significant corre-
lation between numbers of sightings and length of
line surveyed for both aerial and POP surveys. Re-
analysis of these same data shows that the average
number of sightings per mile of track line surveyed
was somewhat higher for the POP surveys, but that
the difference is not statistically significant at the
5% level (paired Student's £-test). Since we are in ef-
fect using the number of sightings per unit length
of track line as a measure of relative abundance in
this analysis, the two data types can be combined.
To remove any bias due to uneven allocation of
sighting effort among the blocks, the effort was first
quantified. A computer program was developed
which calculated the length of track line surveyed
each season within each of the 10-minute blocks, in-
cluding only line segments surveyed within the
criteria defined above Each line surveyed is recorded
in the data base as a sequence of latitude-longitude
positions. For any pair of successive positions, the
length of track line between the points (D, in km)
can be calculated by:
D = 111.12 arccos [sin (X:) sin (X2)
+ cos (X:) cos (X2) cos (Y2 - Yx)],
where Xj and X2 are the latitudes of the two posi-
tions, and Yj and Y2 are the corresponding longi-
tudes. This calculates great circle distance Flight
or cruise tracks would actually be rhumb lines rather
than great circles, but the algorithm required to
calculate rhumb line distance is much more complex.
Furthermore, for two points around 10 km apart,
typical of track line segments in the data, great cir-
cle and rhumb line distance differ by <L m, an error
of <0.01%.
For a pair of points within a single 10-minute
block, the length of the intervening line segment is
simply assigned to that block. The difficulty arises
for successive points located in separate blocks. It
is then necessary to find the point(s) of intersection
where the track line crosses any block boundary(ies).
The bulk of the computer program is concerned with
this procedure For a pair of points in separate
blocks, the equation describing the great circle
through the points is defined. The point where that
line crosses a boundary is then determined by insert-
ing the latitude or longitude value defining the
boundary into the great circle equation, and then
solving for the other coordinate The line segment
which originally spanned two or more blocks is there-
by partitioned into smaller segments, each wholly
contained in a single block, whose lengths are then
calculated as above The final step in the procedure
is to sum the lengths of all the line segments within
the block, which represents the amount of sighting
effort expended in the block.
All cetacean sightings made during track
segments meeting the defined criteria were also ex-
tracted from the data base These data were sum-
marized to produce, for each species, the total
number of individual animals sighted in each block
and season. (This is not to say that this number
represents all different individuals. An individual
may be sighted repeatedly by different surveys, but
this is taken into account by the correction for ef-
fort.) In order to combine different species, the num-
ber of animals of a particular species was multiplied
by the species' estimated average body weight to
calculate biomass sighted per block and season. The
biomass data for each species were then partitioned
into three feeding classes— piscivorous, teuthivorous,
and planktivorous— based upon the estimated per-
centages of each species' diet composed offish, squid,
and zooplankton, respectively. In an earlier analysis
of prey consumption by cetaceans in the CETAP
study area, Scott et al.4 classified each species into
a single category based on its principal prey type;
4Scott, G. P., R. D. Kenney, T. J. Thompson, and H. E. Winn.
1983. Functional roles and ecological impacts of the cetacean com-
munity in the waters of the northeastern U.S. continental shelf.
Paper presented at 1983 annual meeting, International Council for
the Exploration of the Sea, ICES CM. 1983/N:12.
347
FISHERY BULLETIN: VOL. 84, NO. 2
however, we felt that using the estimated proportion
of the diet comprised of the different prey types was
a more realistic representation of what was actually
occurring in the ecosystem. The body weight and
prey preference estimates were taken from Kenney
et al. (1985), who had based their estimates on an
extensive literature review. For three species not in-
cluded in that reference— beluga, false killer whale,
and rough-toothed dolphin— body weight and prey
preference estimates were based on Watson (1981)
and Nishiwaki (1972). For the categories of sightings
which were not completely identified, the body
weight and prey percentages were calculated as
averages for all species included in the category and
weighted by the number of sightings of each. (It
might be argued that the unidentified categories
should be excluded totally and that their inclusion
introduces too much uncertainty. However, we felt
that excluding them would eliminate many poten-
tially valuable observations and that including them
would provide a closer measure of habitat use Some
of the categories can be narrowed to only a couple
of species, and the number of sightings overall is a
valid basis for estimating the probability of an un-
identified sighting being a particular species.)
The biomass data were then summed for all
species in each block and season, as well as for the
piscivorous, teuthivorous, and planktivorous subsets.
Values for endangered species biomass were also
calculated by summing the data for right, humpback,
blue, fin, sei, and sperm whales, as well as for the
estimated proportion of the unidentified categories
made up of these species. The biomass data for each
block and season were then divided by the corre-
sponding effort data, resulting in values of biomass
per unit effort (BPUE) in units of kilograms of ceta-
cean sighted per kilometer of track line surveyed
(kg/km). The final data set therefore had, for each
block, BPUE values for all cetaceans, for en-
dangered species only, and for the piscivorous,
teuthivorous, and planktivorous components of the
cetacean fauna for each season and for the entire
year.
The simplest technique for looking at the pattern
of high-intensity habitat use by cetaceans is to plot
the blocks with the highest values of BPUE. Ob-
viously, the blocks with the highest BPUE values
within any of the individual data sets are those with
the highest intensity of habitat use The question
becomes one of defining the cutoff point in each
distribution for selecting the highest values. The fre-
quency distributions of each of the BPUE data sets
were examined for any patterns which might be
useful as an objective criterion to define a lower
bound for the high-use blocks (eg, bimodal distribu-
tions, or 2 standard deviations above the mean of
a normal distribution). Log-survivorship plots (plot-
ting BPUE vs. log of the number of blocks with
higher BPUE values; see Fagen and Young 1978)
were also tried to look for changes in slope which
could serve as a means of numerically defining this
boundary. When these techniques failed to select any
specific value for the cutoff point, we opted to use
simple percentile rankings to classify the blocks for
plotting the results.
The final step in the analysis was to develop an
index which would serve to define those areas which
are most important as cetacean habitat. By "impor-
tant" we include both the level of habitat use and
the management priority of the individual species.
Habitat requirements for an individual probably de-
pend heavily upon prey type, so each of the data sets
for the three feeding classes were included in this
process. Since management objectives concentrate
on the endangered species, the endangered species
data sets were also included. Since the endangered
species data are also part of the feeding type data,
the former are in effect being included twice This
gives the endangered species extra weight in the in-
dex, in accord with both their endangered status and
management focus. For each seasonal set of BPUE
data for the endangered species and the three feed-
ing classes, blocks were assigned points as follows:
5 if the BPUE was greater than the 99th percentile
value for that data set, 3 if it was between the 95th
and 99th percentiles, 1 if between the 90th and 95th
percentiles, and 0 otherwise The value of the index
for a block is then the sum of these point values for
all data sets. Since there were four seasons and four
BPUE variables used, the maximum possible value
for the index in any block would be 80 (4 x 4 x 5).
For lack of a more concise term, we shall refer to
this as Habitat Use Index, although it does have the
additional dimension of focus on endangered species.
Since this index is based on only the top 10% of each
of the 16 individual data sets, it provides a simple
way to point out those blocks which repeatedly stand
out as high-use habitat in more than one season
and/or for more than one prey type
RESULTS
During the CETAP study, observers on dedicated
aerial or POP surveys operating within the defined
survey criteria made 5,304 sightings of 26 different
species of whales and dolphins. These include sight-
ing of individuals in three genera— Globicephala,
Mesoplodon, and Kogia— which could only be iden-
348
KENNEY and WINN: CETACEAN HIGH-USE HABITATS
tified in the field to genus. In addition, there were
2,039 sightings of 30 more or less unidentified
categories of cetaceans, bringing the grand total to
7,343 sightings. Table 1 lists all the observed ceta-
cean species and unidentified categories, with num-
bers of sightings of each. It also shows, for each
species, the values used in this analysis for estimated
average body weight and percentage of diet com-
prised of the three major prey types.
Overall, 1,476 10-minute blocks were sampled by
CETAP dedicated and POP surveys, with a total of
over 373,000 km of track line surveyed within accept-
able criteria. Somewhat fewer blocks were sampled
during any one season. Sighting effort was most in-
Table 1.— List of cetacean species and unidentified categories sighted by CETAP dedicated aerial and POP surveys on the northeast
U.S. shelf, showing number of sightings, estimated body weight, and estimated percentage of the diet comprised of fish, squid, and
zooplankton. Endangered species are identified by *.
No. of
Body
Percent of diet
No. of
Body
Percent of diet
sight-
weight
Zoo-
sight-
weight
Zoo-
Species or category
ings
(kg)
Fish
Squid p
lankton
Species or category
ings
(kg)
Fish
Squid plankton
Right whale,
Spinner dolphin,
Balaena glacialis*
173
40,000
0
0
100
S. longirostris
3
50
20
80
0
Humpback whale,
Harbor porpoise,
Megaptera
Phocoena phocoena
584
45
95
5
0
novaeangliae'
409
25,000
95
0
5
Unidentified (unid.)
Sperm whale,
whale
263
25,000
71
12
17
Physeter catodon'
258
20,000
20
80
0
Unid. large whale
139
27,900
70
11
19
Blue whale,
Unid. large whale,
Balaenoptera
not B. glacialis
2
26,700
77
12
11
musculus*
2
70,000
0
0
100
Unid. large whale,
Fin whale,
not P. catodon
5
29,200
78
0
22
B. physalus*
946
30,000
90
0
10
Unid. rorqual
30
24,800
88
0
12
Sei whale,
Unid. rorqual,
B. borealis'
62
13,000
0
0
100
not B. acutorostrata
62
27,900
87
0
13
Minke whale,
Unid. rorqual,
B. acutorostrata
215
4,500
95
0
5
not M. novaeangliae
6
24,800
86
0
14
Beaked whale,
P. catodon or
Mesoplodon sp.
11
1,200
0
100
0
M. novaeangliae
2
23,100
66
31
3
Goosebeaked whale,
P. catodon,
Ziphius cavirostris
4
1,900
0
100
0
M. novaeangliae,
Northern bottlenose
or B. glacialis
6
26,600
52
25
23
whale, Hyperoodon
B. musculus, physalus,
ampullatus
4
4,700
5
95
0
or borealis
127
29,000
84
0
16
Beluga whale,
Unid. medium whale
68
4,080
81
15
4
Delphinapterus leucas
1
420
100
0
0
Unid. beaked whale
19
2,090
1
99
0
Pygmy/dwarf sperm
Unid. beaked whale or
whale, Kogia sp.
1
300
0
100
0
P. catodon
2
17,600
18
72
0
Pilot whale,
Mesoplodon sp. or
Globicephala sp.
537
850
0
100
0
Z. cavirostris
2
1,390
0
100
0
Killer whale.
Unid. blackfish
4
863
1
99
0
Crcinus orca
4
3,000
90
10
0
Unid. large blackfish
1
864
1
99
0
False killer whale,
Globicephala sp. or
Pseudorca crassidens
1
500
50
50
0
P. crassidens
6
849
0
100
0
Pygmy killer whale,
Unid. dolphin
785
133
74
26
0
Feresa attenuata
1
150
100
0
0
Unid. beaked dolphin
120
117
85
15
0
Gray grampus,
Unid. dolphin,
Grampus griseus
421
340
0
100
0
not G. griseus
161
96.7
90
10
0
Bottlenose dolphin,
Unid. long-beaked
Tursiops truncatus
828
150
100
0
0
dolphin
11
112
84
16
0
White-beaked dolphin
Lagenorhynchus sp.
10
121
89
11
0
Lagenorhynchus
Lagenorhynchus sp. or
albirostris
10
150
50
50
0
T. truncatus
2
141
96
4
0
Atlantic white-sided
L. acutus or D. delphis
23
93.8
88
12
0
dolphin, L. acutus
374
120
90
10
0
Stenella sp.
86
52.7
31
69
0
Rough-toothed dolphin,
Stenella sp., not
Sfeno bredanensis
1
100
50
50
0
S. longirostris
64
52.8
31
69
0
Saddleback dolphin,
Stenella sp. or
Delphinus delphis
340
65
85
15
0
T. truncatus
8
126
83
17
0
Striped dolphin,
S. coeruleoalba or
Stenella coeruleoalba
63
55
40
60
0
T. truncatus
1
136
91
9
0
Spotted dolphin,
S. attenuatal plagiodon
S. attenuata or
or T. truncatus
3
138
90
10
0
plagiodon
51
50
20
80
0
Stenella sp. or D. delphis
21
59.6
61
39
0
349
FISHERY BULLETIN: VOL. 84, NO. 2
tense during spring, followed in descending order
by summer, fall, and winter. Table 2 summarizes the
sighting effort by season and for the entire year.
The BPUE data are summarized in Table 3. The
distributions of BPUE values for all categories and
seasons were very similar. Each distribution was
highly skewed toward lower values. This can be seen
from the table; mean values ranged between 33 and
423 kg/km, but maximum values were as high as
33,747 kg/km. In 20 of the 25 cases, the median value
was 0, and in 9 of these the 75th percentile value
was also 0, indicating that no cetaceans of that par-
ticular category were seen in one-half or three-
quarters, respectively, of the blocks surveyed. In fact,
in two cases (endangered species and planktivores
sighted in winter) even the 90th percentile value was
0; no endangered or plankton-feeding cetaceans
were observed in 9 out of 10 blocks surveyed in the
winter.
The overall pattern of high habitat use by ceta-
ceans is depicted in Figure 1, which shows those
10-minute blocks with the top 10% of the whole-year
BPUE values (all species combined). The figure also
identifies locations to be used for geographic refer-
ence Three principle high-use areas can be de-
lineated: 1) the western margin of the Gulf of
Maine, from the Great South Channel northward to
Jeffreys Ledge, 2) the eastern portions of Georges
Bank, along with the Northeast Channel and rela-
tively deep basin north of the bank, and 3) the con-
tinental shelf edge There are also scattered high-
use blocks in other areas.
Table 2.— Summary of sighting effort in 10-minute blocks, expressed as kilometers
of track line surveyed within acceptable criteria, for CETAP dedicated and POP surveys.
Season
Winter
Spring
Summer
Fall
Total
Blocks sampled
1,179
1,344
1,395
1,169
1,476
Mean effort per block
40.3
108.0
80.7
58.2
252.9
Standard deviation
32.9
104.9
56.1
47.6
207.9
Maximum effort per block
372
1,137
596
546
2,389
Total effort
47,506
145,204
112,576
67,994
373,280
Table 3.— Mean, median, and maximum values of biomass sighted
per unit of sighting effort, by season and for the entire year, for all
cetacean species combined, endangered species only, and fish-,
squid-, and plankton-feeding cetaceans.
Biomass per unit effort
(kg/km)
Cetacean category Season Mean Median Maximum
All cetaceans All 368 67 15,170
All cetaceans Winter 234 10 23,049
All cetaceans Spring 423 2 20,928
All cetaceans Summer 386 0 28,447
All cetaceans Fall 270 0 33,747
Endangered species All 296 0 15,170
Endangered species Winter 198 120 22,048
Endangered species Spring 350 0 20,268
Endangered species Summer 323 10 27,478
Endangered species Fall 190 10 33,072
Piscivores All 205 21 6,920
Piscivores Winter 139 '0 16,266
Piscivores Spring 256 1 15,446
Piscivores Summer 235 0 22,483
Piscivores Fall 158 0 23,995
Teuthivores All 83 1 4,249
Teuthivores Winter 62 10 11,879
Teuthivores Spring 80 0 3,582
Teuthivores Summer 83 0 5,380
Teuthivores Fall 79 0 5,625
Planktivores All 80 0 12,323
Planktivores Winter 33 120 8,190
Planktivores Spring 87 0 5,874
Planktivores Summer 68 '0 12,910
Planktivores Fall 33 '0 5,805
175th percentile value was also 0.
290th percentile value was also 0.
Figure 2 shows the patterns of high habitat use,
again as the upper 10% of BPUE values, for the en-
tire cetacean community in each of the four seasons.
The seasonal patterns do not show any major dif-
ferences; however, a slight north-south shift in the
pattern is evident. The number of high-use blocks
is higher in the northern portion of the area and
lower in the southern portion during spring and sum-
mer than during fall and winter. It should be em-
phasized that the plots in Figure 2 do not indicate
differences in magnitude of utilization intensity
between seasons, but only pattern differences. Since
the blocks which are plotted are the upper 10% of
the BPUE values for each seasonal distribution, the
numbers of blocks plotted for each season are fair-
ly equivalent. For example, it appears from the plots
that the shelf edge may be more intensely used in
the winter than during the other seasons, but ac-
tually the reverse is true It is simply that the blocks
with highest winter utilization tend to be on the shelf
edge, but the intensity of use in these blocks is still
lower. Seasonal differences in intensity of habitat use
can be seen by referring back to Table 3. The inten-
sity of habitat use is highest in the spring and se-
cond highest in the summer for all categories except
the teuthivores, where the summer utilization is most
intense and spring and fall very close behind. There
350
KENNEY and WINN: CETACEAN HIGH-USE HABITATS
44° -
42° -
40° -
38'
36<
34c
Figure 1— Plot of 10-minute blocks with total cetacean biomass per unit effort values in the
top 10% of all blocks. GM = Gulf of Maine; GB = Georges Bank; NC = Northeast Channel;
JL = Jeffreys Ledge; SB = Stellwagen Bank; GS = Great South Channel.
is a general pattern of reduced utilization during the
fall and winter.
Figure 3 shows the whole-year patterns of high
habitat usage for the four subsets of the total ceta-
cean community. The pattern for endangered species
shows only slight differences from the total com-
munity pattern seen in Figure 1. Differences from
the total community pattern become somewhat
greater in the piscivorous component. The intensity
of utilization along the shelf edge is less, but there
appears an area or areas of high use at midshelf east
of the Chesapeake Bay region. The planktivorous
component shows a distinctive pattern. There are
only scattered high-use blocks in the southern half
of the area. In the northern half of the area, the pat-
tern is similar to those for the entire community, en-
dangered species, or piscivores, except that there are
more high-use blocks in the central portion of the
Gulf of Maine and on the southern part of Georges
Bank. The teuthivorous component shows the most
distinct pattern, with a dense concentration of high-
use blocks along the shelf edge in the southern half
of the area and a less dense concentration along the
more northern shelf edge and in the vicinity of the
Northeast Channel.
Finally, Figure 4 presents the overall composite
pattern of high-use areas, plotting those 10-minute
blocks with Habitat Use Index values in the upper
5%, 10%, and 20% of all blocks sampled. Of the total
of 1,476 blocks surveyed, 889 had index values of 0
and 587 were 1 or greater. The maximum index value
was 49 for a block located at the northern end of
Stellwagen Bank. Table 4 lists the blocks in the up-
per 1% of the distribution, showing their locations.
Of those 16 blocks, 13 are in the western Gulf of
Maine between the Great South Channel and Jef-
freys Ledge. This area shows the densest concentra-
tion of high-use blocks in Figure 4. The secondary
351
FISHERY BULLETIN: VOL. 84, NO. 2
Figure 2— Seasonal patterns of the top 10% of total cetacean biomass per unit effort values.
352
KENNED and WINN: CETACEAN HIGH-USE HABITATS
Figure 3— Blocks with top 10% of cetacean biomass per unit effort values for four subsets of the total cetaceans: endangered species
(right, humpback, sperm, blue, fin, and sei whales), fish-eating component, plankton-eating component, and squid-eating component.
353
FISHERY BULLETIN: VOL. 84, NO. 2
Figure 4— Plot of Habitat Use Index in 10-minute blocks, showing blocks with values
in the upper 5%, 10%, and 20% of the distribution.
Table 4.— List of the 10-minute blocks with Habitat Use Index values
in the upper 1% of all blocks sampled, in descending order, with
the latitude and longitude of the block center and the location of
the block.
Utilization
Central point
index
of block
General location
49
42°25'
70°25'
Northern end— Stellwagen Bank
41
41°25'
69° 15'
Great South Channel
36
41°25'
69°25'
Great South Channel
34
42° 15'
66°25'
Northeast Channel
33
41°35'
69°25'
Great South Channel
32
42°15'
70°25'
Stellwagen Bank
32
42° 15'
70°05'
Stellwagen Bank
32
40°35'
67°25'
Georges Banks— Powell Canyon
head
29
42° 15'
70° 15'
Stellwagen Bank
29
42°05'
70° 15'
Stellwagen Bank
28
41°25'
69°05'
Great South Channel
27
41°45'
69°45'
Great South Channel
27
41°25'
68°55'
Great South Channel
26
43° 15'
69°55'
Northern end— Jeffreys Ledge
26
42°55'
65°35'
Off Browns Bank
26
41°15'
69° 15'
Great South Channel
concentrations of high-use blocks tend to be around
the perimeter of Georges Bank and along the con-
tinental shelf edge
DISCUSSION
The CETAP sighting data for some individual
species showed a concentration of sightings along
the western margin of the Gulf of Maine This analy-
sis has demonstrated quantitatively that this area
is the most intensely used cetacean habitat on the
northeast U.S. continental shelf. It comprises a major
feeding ground for fin whales, humpback whales,
right whales, minke whales, and white-sided doi
phins. Humpbacks and fin whales are known to feed
heavily upon the American sand lance, Ammodytes
americanus, a small schooling fish (CETAP 1982;
Hain et al. 1982; Mayo 1982; Mitchell 1973, 1975c;
Overholtz and Nicolas 1979), and the minke whales
354
KENNEY and WINN: CETACEAN HIGH-USE HABITATS
and white-sided dolphins likely do so as well (CETAP
1982; Mayo 1982; Mitchell 1975b). The sand lance
populations of the western North Atlantic have in-
creased dramatically since the mid-1970's (Sherman
et al. 1981). Meyer et al. (1979) described the west-
ern Gulf of Maine, especially Stellwagen Bank and
east of Cape Cod, as an area of extremely dense sand
lance populations. Data from the National Marine
Fisheries Service 1979-1981 groundfish surveys (T.
R. Azarovitz5) also shows peak Ammodytes abun-
dance in the Stellwagen Bank-Jeffreys Ledge area.
A second area of high sand lance abundance shown
oy these data corresponds to the midshelf east of
the Chesapeake, which was identified above as a
region of high use by piscivorous cetaceans. It is
likely that sand lance distributions are a primary
controlling factor in the pattern of high-intensity
habitat use shown here for the western Gulf of
Maine.
Ammodytes is not the only cetacean prey species
which can be shown to have a strong effect on pat-
terns of cetacean habitat use within the western Gulf
of Maine, although it is the major one The right
whale feeds primarily upon copepods (Nemoto 1970;
Watkins and Schevill 1976). Right whales are a major
component of the cetaceans in the southeasternmost
portion of the high-use area in the western Gulf of
Maine, in the vicinity of the Great South Channel,
where they congregate in response to extremely
dense spring concentrations of Calanus finmar-
chicus (CETAP 1982).
The other high-use cetacean habitat we have iden-
tified is the edge of the continental shelf. The ceta-
cean assemblage of this region has been analyzed
in detail by Hain et al. (1985). The primary species
of the shelf edge are sperm whales, pilot whales, gray
grampus, saddleback dolphins, bottlenose dolphins,
and striped dolphins. Less common species include
the various beaked whales and other dolphin species.
This assemblage does not specialize on one or two
prey species as we have suggested for the Gulf of
Maine, but is highly diverse in prey taken, although
individual species may exhibit quite narrow dietary
specializations. Food items include a wide variety of
squids and fishes (Kenney et al. 1985). Furthermore,
the shelf edge assemblage on Georges Bank includes
sei whales, which feed primarily on copepods and
secondarily on euphausiids (Jonsgard and Darling
-;977; Mitchell 1975a, 1975b; Nemoto 1970). Sei
whales occur primarily on the southwest and eastern
portions of Georges Bank. The CETAP data also
show sightings of other baleen whales— primarily fin
whales, but also minke, humpback, and right whales
—near the southern edge of Georges Bank during
some times of the year. The shelf edge, although used
less intensely than the western Gulf of Maine, sup-
ports a cetacean fauna which is much more diverse
in terms of both cetacean species and variety of prey
taken.
We have interpreted our results in this study as
indicating control of cetacean distributions by the
distributions of the most important prey species.
This is almost certain to be the case on a microscale
level, but may or may not be true at the general level.
It is unknown how migratory cetaceans orient or
navigate to their feeding grounds, but it may be that
physical cues from the environment are used in this
process, in effect determining or influencing the
general pattern of distribution. Another alternative
could be that there is a significant traditional or
historical component of the return to the same
general vicinity each year, with microscale distribu-
tions within that region directly related to prey den-
sity. In each of these cases the ultimate controlling
factor is food, but the proximate factors are some-
thing different.
We have limited our discussion of individual species
mostly to the descriptive level. One factor, however,
should be noted. Because we are dealing with bio-
mass of cetaceans, these patterns are dominated by
the large whales for the most part. Because fin
whales are easily the most common whale in the
region, they are the dominant factor in patterns of
cetacean biomass distribution (Kenney et al. 1985;
Scott et al. fn. 4). The most common species num-
erically were white-sided and saddleback dolphins,
with estimated populations of each exceeding 30,000
individuals (CETAP 1982), but their contributions
to the patterns shown here are smaller because of
their relatively smaller sizes. One must refer to the
distribution plots in the 1982 CETAP report for the
details of individual species distribution patterns.
We have purposely avoided the use of the term
"critical habitat" in this analysis. Besides the legal
aspects of the term under the Endangered Species
Act and Marine Mammal Protection Act, Ray and
Miller6 have pointed out that there are many dimen-
sions to the concept of critical habitat. These include
the biological vulnerability of a species, the ecological
processes which support the species, and the poten-
BT. R. Azarovitz, Northeast Fisheries Center Woods Hole Labora-
tory, National Marine Fisheries Service, NOAA, Woods Hole, MA
02543, pers. commun. December 1982.
6Ray, G. C, and R. V. Miller. 1982. Critical habitats of marine
mammals. Paper presented at 1982 annual meeting, International
Council for the Exploration of the Seas, ICES CM. 1982/N:7.
355
FISHERY BULLETIN: VOL. 84, NO. 2
tial impacts of human activities. We have for the
most part addressed only the patterns of habitat use,
which contribute to the first two dimensions listed
above By giving extra weight to the endangered
species in the Habitat Use Index, however, we have
also further addressed the dimensions of biological
vulnerability and potential impacts. On the other
hand, the concept of critical habitat as strictly de-
fined should be limited to single species. We have
approached the problem from the viewpoint of the
entire cetacean fauna of the region. Our analysis has
defined those localities which appear to be impor-
tant cetacean habitats based on the intensity of
utilization with a special emphasis on the en-
dangered species. These results now can and should
be used as additional input for resource management
and decision-making purposes.
ACKNOWLEDGMENTS
The preparation of this paper was made possible
by funding from the Minerals Management Service,
U.S. Department of the Interior, contract number
14-12-0001-30090. The CETAP study, which was the
source of the data utilized, was funded by the Bur-
eau of Land Management, contract number AA551-
CT8-48. We would like to collectively acknowledge
the many individuals who contributed to CETAP's
success. G. B. Epstein developed the computer algo-
rithm to measure track line surveyed per block, R.
J. Medved provided statistical advice, and M. Nigrelli
typed the manuscript. We are also grateful to K.
Sherman, S. B. Saila, P. V. August, M. P. Sissenwine,
G. T. Waring, and several reviewers at Minerals
Management Service who provided helpful criticisms
of early drafts of the paper. The work reported
herein was part of a dissertation submitted by R. D.
Kenney to the Graduate School of Oceanography,
University of Rhode Island, in partial fulfillment of
the requirements for the degree of Ph.D.
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357
SOUNDS FROM BRYDE, BALAENOPTERA EDENI, AND
FINBACK, B. PHYSALUS, WHALES IN THE GULF OF CALIFORNIA
William C. Cummings,1 Paul 0. Thompson,2 and
Samuel J. Ha3
ABSTRACT
Low-frequency moaning sounds were recorded from Bryde whales, Balaenoptera edeni, off Loreto, Mex-
ico, in the Gulf of California. These utterances averaged 0.4 s in duration with most of the sound energy
at about 124 Hz. Elsewhere in the Gulf, we recorded about 1,300 low-frequency moans from at least 35
feeding finback whales, B. physalus. The finbacks' most outstanding sound was a long moan with a 1.9-s
component at 68 Hz and a 1.6-s component at 34 Hz. Overall sound source levels in the effective band-
widths ranged between 152 and 174 dB re 1 jiPa (1 m) for Bryde whales, and 159 to 183 dB for finback
whales. Short "20-Hz signals" that are typically associated with finback whales were not present in these
recordings, apparently because of seasonal or behavioral differences.
The main objective of this study was to describe
underwater sounds from two species of mysticete
whales— the Bryde whale, Balaenoptera edeni, and
the finback whale, B. physalus. We also wanted to
compare the presently described finback sounds with
those recorded elsewhere.
Contrasted with the typical whistles, squeals, and
clicks of odontocetes, we continue to find that
mysticetes utter mostly low-frequency sounds. How-
ever, exceptional and rare sounds of higher frequency
have been reported (Cummings and Thompson 1971;
Beamish and Mitchell 1971, 1973; Beamish 1978).
The combination of low frequencies (Hz), long wave-
lengths, and high source levels of mysticete whale
sounds enables their detection at distances up to 100
km or more, even with standard signal processing.
Low-frequency sounds (40-75 Hz, 1-s long, and
others) have been recorded from finbacks in the
North Atlantic (Schevill and Watkins 1962; Edds
1981). Short, powerful "20-Hz signals" have also been
recorded from this species (Schevill et al. 1964).
Watkins (1981) categorized underwater finback
sounds as 20-Hz pulses, ragged broadband low-fre-
quency pulses, low-frequency rumbles, higher fre-
quency sounds, and broadband impulses.
We have long been interested in "20-Hz signals",
having worked with many categories from wide-
spread areas of the world (Cummings and Thomp-
son 19664; Northrop et al. 1968, 1971), and the pros-
pects of recording them from the more accessible
^ceanographic Consultants, 5948 Eton Court, San Diego, CA
92122.
24256 Sierra Vista, San Diego, CA 92103.
3Millersville University, Millersville, PA 17551.
finbacks in the Gulf of California also was an impor-
tant objective.
We are unaware of any other descriptions (except
for 20-Hz pulses) of sounds from Pacific finbacks.
Underwater sounds from the Bryde whale were
unknown, this being the original description except
for a brief abstract of the present work in 1969
(Thompson and Cummings).
MATERIAL AND METHODS
An expedition took place in June 1969, aboard the
27 m yawl, Saluda. The ship left La Paz (southeast
Baja peninsula, Mexico) sailed northward to Mulege,
across the Gulf of California to Guaymas on the Mex-
ican mainland, northward past Isla San Esteban,
around Isla Angel de la Guarda, and southward to
Santa Rosalia— a distance of about 1,500 km (Fig.
1). Except for Contact 3, all of the sounds recorded
in the presence of unidentified large whales were
generally the same as those that we determined to
be from finbacks. However, we were not always cer-
tain which balaenopterid was being recorded,
especially at long distances. Consequently, if an iden-
tification of a balaenopterid whale was questionable,
the "contact" was noted simply as "Balaenoptera sp".
The water's surface varied from Sea State 0 to 2,
and currents usually were minimal. The ship's oper-
ating equipment was shut down during all record-
ings. The instrumentation included a hydrophone-
4Cummings, W. C, and P. O. Thompson. 1966. 20-Hz signals
in the northeast Pacific Unpubl. Rep., 17 p. Navy Electronics
Laboratory, San Diego, 92152.
Manuscript accepted July 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
2STf-$
>*
359
MSHfciKY BULLETIN: VOL. 84, NO. 2
Figure l.-Track of Saluda in the
Gulf of California (June 1969)
with numbered cetacean contacts.
360
CUMMINGS ET AL.: SOUND FROM BRYDE AND FINBACK WHALES
preamplifier (Wilcoxon,5 Type M-H90-A) suspended
at depths of 6 to 53 m below the surface Up to 800
m of floating cable carried the signals to the ship,
allowing the hydrophone to be stationary until the
ship drifted out to this distance The hydrophone was
suspended from an inflatable 8 m spar buoy which
provided effective acoustic isolation from low-fre-
quency acceleration caused by surface waves. The
hydrophone's response was attenuated at low fre-
quencies (beginning with 3 dB down at 12 Hz) to fur-
ther reduce low-frequency noise and to prevent most
of the preamplifier blockage from any drag motion
that remained. Without these or similar measures,
we have found that hydrophone and sea noise below
100 Hz, even in relatively smooth seas, usually
prevents satisfactory recordings of low-frequency
mysticete sounds with suspended systems.
One track of a magnetic tape recorder (Magnecord
1020), powered by a DC-AC converter, carried a run-
ning commentary and airborne whale sounds from
a radio microphone (Vega Telemike). The other track
recorded signals from the hydrophone. Continuous
visible records were made on station with a level
recorder (Briiel & Kjaer, Type 2301), also powered
by the converter which was acoustically isolated. A
sound analyzer (General Radio, Type 1558) was used
to monitor incoming signals and their absolute levels
and to provide power to the hydrophone-preamplifier.
Calibration was by means of a 1,000-Hz tone and
pink or white noise which were inserted through the
system and recorded at frequent intervals. Overall
response of the recording system was +5 dB from
25 Hz to 18 kHz.
Without a hydrophone array we could not precisely
localize sound sources. However, correlations be-
tween whale movements and changes in received
sound level provided evidence that those sounds
came from the whales observed.
At sea we find it difficult to distinguish the Bryde
BReference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
whale from other balaenopterids, especially the sei
whale, B. borealis. An exception was the circum-
stance noted here, involving long contacts and good
visibility above and below water, so that identifying
features of behavior and form were revealed. Most
useful of these field characteristics were 1) the pres-
ence of ridges on top of the head of Bryde whales,
2) the asymmetrical coloration of finbacks, usually
a yellowish white on the lower right jaw and baleen
that is contrasted with the darker appearance of the
left area, and 3) the peculiar surfacing of sei whales
whereby head and fin appear nearly simultaneous-
ly, without arching.
Received overall sound levels are reported in dB
re 1 jiPa, and source levels are referenced to 1 m.
Analysis was accomplished using graphic level
recorders, oscilloscopes, a sound spectrographic
recorder, and a RTA (real time analyzer).
RESULTS
Sightings and Recordings
The locations of whale sightings associated with
recordings of whale sounds are listed (Table 1). Un-
identified balaenopterid whales were sighted off La
Paz, where two low-level whale sounds were recorded
during Contact 1.
We spotted two Bryde whales, about 11 m long,
southeast of Loreto (Contact 2). The sea was calm
and the surface water temperature was 24 °C. The
two animals separated as the ship approached. One
swam away and remained mostly out of sight. The
other began passing back and forth under the ship's
keel. It dove about 10 m and surfaced every 1 to 6
min. W C. Cummings dove on the whale and photo-
graphed it underwater for identification.
We recorded 288 low-frequency moans in 50 min
from the Bryde whales during Contact 2. Some of
these sounds were of very low signal-noise ratio
(down into the ambient level of the sea noise) and
presumably originated from the more distant of the
Table 1.— Contacts with sound producing whales in the Gulf of California.
Contact Date Time
Location
Subjects (No.)
1
6-11
1000
24°43.
2
6-13
0700
25°57.
3
1930
26°50'
4
6-17
1815
28°18'
5
6-18
0530
28°25'
6
1330
28°58'
7
6-19
0900
29°35'
8
1430
29°41.
9
6-20
1430
29°14'
10
1530
29°15.
5'N, 110°36'W, 2 km S of Isla San Francisco
5'N, 110°19'W, 8 km SSE of Loreto
N, 111°42'W, 14.8 km SE of Pta. Concepcion
N,111°46'W, midway, Guaymas to Isla San Esteban
N, 112°9.5'W, 18.5 km ENE of San Pedro Martir Island
N, 112°53.5'W, 24.1 km ESE of Isla Angel de la Guarda
N, 113°31'W, 3.7 km ENE of Puerto Refugio
5'N, 113°27'W, 17.6 km NE of Puerto Refugio
N, 113°33'W, N. end of Ballenas Channel
5'N, 113°30'W, N. end of Ballenas Channel
Balaenoptera sp. (1)
B. edeni (2)
B. edeni (1)
Large whale (1)
Balaenoptera sp. (1)
B. physalus (3)
B. physalus (about 35)
B. physalus (2)
Balaenoptera sp. (1)
Balaenoptera sp. (1)
361
nonn.n.1 DUL.ijt.iiiM; »ul. 01, i\\j. i.
two whales. Coincidently we were recording low-
level, high-pitched whistles and squeals from a dis-
tant group of saddleback porpoises, Delphinus
delphis. It was obvious that changes in the loudness
of other low-frequency signals, as aurally monitored,
and in the level on the graphic recorder were cor-
related with the nearby Bryde whale's proximity to
the ship.
Later the same day, another whale was sighted off
Pta. Conception in the Mulege area and tentatively
identified as either a sei or Bryde whale of about
12 m (Contact 3). We recorded 407 sounds from this
whale The sounds were essentially the same as those
recorded earlier from the Bryde whales of Con-
tact 2. After analyzing the sounds, Contact 3 was
identified as a Bryde whale Sounds of these
characteristics were not encountered again during
the cruise, nor were any other Bryde whales
seen.
About 100 km northwest of Guaymas, a large
whale was sighted at a range of about 450 m (Con-
tact 4). A brisk wind and choppy seas prevented iden-
tification, but one distinctly whalelike moaning
sound appeared in the accompanying noisy record-
ing.
East of San Pedro Martir Island, we recorded 42
sounds from another whale (Contact 5) identified as
a finback, about 15 m in length. Three large finback
whales were sighted off the southern tip of Isla
Angel de la Guarda (Contact 6). All of the 376 moans
recorded from these whales occurred when the
animals were below the surface
On 19 June, we sighted about 35 finback whales
outside the entrance of Puerto Refugio (Contacts 7,
8). They surfaced in series of 2 to 7 times, usually
in pairs or in trios. Their blows were accompanied
by smooth resonant sounds similar to that expected
from air rushing through a confined space Climax-
ing the final appearance in a series of surfacings,
the whales strongly arched their backs and appeared
to dive at a steep angle Some of the finbacks' dor-
sal fins were distorted. Large concentrations of
whales, porpoises, and sea lions occurred over an
area of at least 6 km around the ship where they
0 1
TIME IN SECONDS
Figure 2.-Spectrograms of typical Bryde whale moans. The effective analyzing filter bandwidth was 3 Hz.
362
CUMMINGS ET AL.: SOUND FROM BRYDE AND FINBACK WHALES
were feeding on red crabs, Pleuroncodes planipes,
that swarmed at the surface during the early morn-
ing and evening. We distantly accompanied two of
the whales which were swimming at 18 km/h and
surfacing every 1 to 1.5 min. They rose high enough
above the surface for us to clearly identify them as
finbacks. Extensive sound recordings were made
among the large concentration of whales near shore
(Contact 7) and also much farther offshore (Contact
8), away from the main group.
Recordings of whale sounds from Contacts 9 and
10 were made in Ballenas Channel near finned
whales on the west side of Isla Angel de la Guar-
da.
Analysis of Whales Sounds
Most sounds attributed to Bryde and finback
whales, other than those from blows, were in a class
we called "moan'— emissions longer than 0.2 s and
<250 Hz in frequency. Many other sounds of
biological origin, including clicks, knocks, etc, were
recorded in the presence of the whales, but only
when other possible sources were present, such as
porpoises and sea lions.
Bryde Whales
As seen in Figures 2 and 3, upper, Bryde whale
IV RMS
LU
LU Q
< j 0
-«Ol
CO 5
IV R
MS
IPP^r
0
LU
70
LU
03
C/)
SEC
4
1
-jjA -?rW
0
HZ
100
Figure 3— Waveform and spectrum (/Hz) for Bryde whale (upper) and finback whale (lower).
Effective analyzing filter bandwidth was 0.75 Hz (Bryde whale sound), 0.375 Hz (finback whale).
363
FISHERY BULLETIN: VOL. 84, NO. 2
moans varied widely in duration and frequency (Hz).
Of the 93 miscellaneous moans analyzed (Table 2),
the principal sound energy occurred at a mean fre-
quency of 124 Hz; that of individual moans varied
from 70 to 245 Hz. Seventy-three percent of these
sounds exhibited frequency shifts (mean of 15.2 Hz)
that were downward or upward, or a combination
thereof. The mean duration of the moans was 0.42
s (range, 0.2 to 1.5). These sounds occurred at inter-
vals of 0.2 to 9 min.
The Bryde whale that apparently was attracted to
the ship (Contact 2) did not emit moans when very
closeby. The received overall sound level for a typical
moan, when this whale was estimated to be 300 m
away, was 102 dB. Assuming a spherical spreading
loss of 20 log10 1.094(R), R being distance in
Table 2.— Analysis of whale sounds.
68/34-Hz moans
Miscellaneous moans
Received
Source
Mean
Received
Source
Range
level
level
frequency I
Duration
Range
level
level
Contact
Identification
No.1
(m)
(dB)*
(dB)3
No.1
(Hz)
(s)
(m)
(dB)*
(dB)3
1
Balaenoptera sp.
2(2)
—
83
—
0
—
—
—
—
—
2
B. edeni
0
—
—
—
288(93)
123.9
0.42
300
102
152
3
B. edeni
0
—
—
—
407(35)
132.0
0.40
600
250
116
126
168
174
4
Large whale
0
—
—
—
1(1)
75.0
0.60
—
90
—
5
Balaenoptera sp.
30(10)
250
121
169
12(8)
49.6
0.55
200
121
166
No visual contact
44(16)
—
90
—
21(21)
50.7
0.63
—
92
—
6
Balaenoptera sp.
203(6)
2,000
115
183
173(14)
53.7
1.23
2,000
115
183
7
B. physalus
164(20)
—
108
—
468(131)
59.8
0.59
100
125
165
8
B. physalus
201(30)
—
99
—
550(42)
65.5
0.73
—
117
—
9
Balaenoptera sp.
3(3)
2,000
95
—
102(17)
63.3
0.70
2,000
118
181
10
Balaenoptera sp.
90(5)
800
108
166
12(8)
77.5
0.68
800
101
159
1Number of sounds encountered with number analyzed in parenthesis.
2dB re 1 iPa
3dB re
1 jiPa at 1
m.
AIR-BORNE
4-
4-
3-
3-
X
>
o
o
2
1
3-
2-
1
* * v - — •
0.5 1.0
K
WATER-BORNE
4-
3-
2-
Kfi
- » ^ . - --
-
a.
•'*" .
*r~
o
0.5 L0 1.5 0 0.5 1.0 1.5
TIME IN SECONDS
Figure 4— Spectrograms of two blows from a Bryde whale recorded in air (upper) and in water (lower). The effective analyzing filter
bandwidth was 20 Hz.
364
CUMMINGS ET AL.: SOUND FROM BRYDE AND FINBACK WHALES
meters, this received level would indicate an overall
source level of 152 dB in the effective bandwidth.
The whales were close enough and the frequencies
low enough that attenuation was probably minimal.
However, these particular moans could possibly have
been emitted by the other whale that was about 500
m away at the time In this case, the estimated overall
source level would have been 157 dB in the effective
bandwidth.
Weak exhalation sounds were recorded simultan-
eously from underwater and in the air from the near-
by surfaced Bryde whale. The exhalation sounds
received underwater were nearly obscured by splash-
ing sounds as the animal broke the surface (Fig. 4).
For the 35 moans analyzed from the Bryde whale
of Contact 3, the mean frequency of the strongest
component was 132 Hz and the mean duration was
0.40 s, both values close to those from Contact 2
(Table 2). However, the overall source level estimates
of 168 and 174 dB (in the effective band widths) were
greater.
The nearby Bryde whale (Contact 2) was totally
submerged as it produced all of its moaning sounds,
but no other apparent behavior was associated with
the moans.
Finback Whales
In addition to miscellaneous moans (Fig. 5) that
were similar to, but lower in frequency than those
recorded from Bryde whales, the sounds of identified
finback whales (Contacts 7, 8) included unique moans
characterized by a long 68-Hz component that was
usually followed by another component at 34 Hz
(Figs. 6, 3 (lower)). Of the miscellaneous moans
analyzed from recordings of the finback whales of
Contacts 7 and 8, the mean frequency of the strong-
est component was 59.8 and 65.5 Hz, and the mean
duration was 0.59 and 0.73 s, respectively (Table 2).
Typically, these moans showed some frequency
shift with <10% of the signals changing more than
20 Hz, generally downward. Overall source level
200
100 -
M
I
>
u
z
LU
o
Sf 200
100-
0 1
TIME IN SECONDS
Figure 5— Spectrograms of miscellaneous whale moans from finback whales off Isla Angel de la Guarda. The effective analyzing filter
bandwidth was 3 Hz.
365
FISHERY BULLETIN: VOL. 84, NO. 2
200 -
100 -
M
U
z
o
Sf 200 -
TIME IN SECONDS
Figure 6— Spectrograms of typical 68/34-Hz moans from finback whales recorded off Isla Angel de la Guarda. The first component of
the moans began at 65 Hz and increased to 68 Hz in the first sec It was accompanied by weaker modulation products at about 23-Hz
intervals, mostly above the main frequency. The 34-Hz component followed and sometimes overlapped the first component (lower spec-
trogram). The effective analyzing filter bandwidth was 3 Hz.
of the sounds was 165 dB in the effective band-
widths.
Of the 50 long moans from finbacks that were
analyzed, the mean frequency of the main, or first,
component was 68.2 Hz; the mean frequency at onset
being 66.1 Hz. The mean duration was 1.5 s. Thirty
moans exhibited additional lower frequency compo-
nents with a mean frequency of 33.5 Hz and a mean
duration of 1.3 s. The overall mean duration of these
two-part moans was 3.1 s. The 365 moans of this type
encountered in Contacts 7 and 8 occurred on the
average of 1.6 and 2.2 times/min, respectively.
In the case of unidentified balaenopterid whales,
the mean frequency of the strongest component of
the 68 miscellaneous moans analyzed was 58.5 Hz
(range from 15 to 95 Hz), and the mean duration was
0.8 s. Of these sounds <10% had any frequency shift
>10 Hz. Thirty-seven of the analyzed moans were the
same as the long two-part moans recorded in the
presence of finbacks. Their mean frequencies were
68.1 and 34 Hz, the mean component duration was
1.9 and 2.6 s, respectively, and the mean total dura-
tion was 3.4 s. The mean starting frequency of the
68-Hz component was 63.9 Hz. These two-part
moans occurred at a rate of 1.5 to 3.2/min. Overall
source levels ranged from 159 to 183 dB in the ef-
fective frequency bandwidth.
The blows of finback whales were as high as about
7 m above the water's surface, and often they were
clearly audible in air at distances out to 200 m. The
last blow in a series was followed by an inhalation
that sometimes involved a low-frequency whistlelike
sound just before a long dive (Fig. 7). The physical
characteristics of blow sounds varied slightly from
one whale to another, providing a certain degree of
uniqueness for an individual whale (Fig. 7). Wheez-
ing, shriek, and hornlike sounds produced by hump-
back whales in association with their blows have been
described by Watkins (1967) and Thompson et al.
(1977).
366
CUMMINGS ET AL.: SOUND FROM BRYDE AND FINBACK WHALES
WHALE I
q gggag <ge «r«i .a-»r..^»-
SSSSS=
<nfe,M trf-'tMiif
*«~
16
■ ~, T.O., » .-. t,. <*,!» ^ .. ^
31
flfe?
tr%sU«-
48
WHALES II & III
> o
a
t^Br
gSjStSg^f*-
9fe
iriTttrnrnWirra
14
21
«St»Tr ngKiiarr-iTinmi .awe
32
5 2
ui
as
Li.
H
■-£,--•- v -5-5
■J < i - V
M*
3tfc
--gr-Tis jjjgge '- 1- i ■ t - 4froa^ai^iBa5t*»ttia»agw4^ muk. 'jfrsasmiAe
•-Sfe
jte
41
51
64
71
84
TIME SCALE I 1
1 SECOND
Figure 7— Spectrograms of whale blow series recorded in air. Running time in seconds relative to the first blow is indicated on the abscissa.
Whales II and III (second series) can be distinguished throughout the first 105 min by the unique physical characteristics of their alter-
nating blows. Just before a long dive, the whales produced a low-frequency whistlelike sound at inhalation Oast spectrogram, first row;
last spectrogram, last row) which was not apparent during earlier blows of a series. In the second series, two low-level blow sounds at
110 and 132 min are not shown. The effective analyzing filter bandwidth was 20 Hz.
DISCUSSION
The moans recorded on this cruise from visually
unidentified or unseen whales were very similar to
those found to be from finbacks, except for Contact
3 involving Bryde whale sounds. Thus we believe the
former also were from finback whales.
Some of the moans recorded in this study only
slightly resembled short "20-Hz signals" described
by several investigators (Walker 1963; Patterson and
Hamilton 1964; Schevill et al. 1964; Weston and
Black 1965; Cummings and Thompson 1966 [fn. 4];
Northrop et al. 1968; Watkins 1981). However, none
of the presently described signals could be categ-
orized as short "20-Hz signals" noted in other
studies, because of differences in frequency (Hz) of
major sound energy, signal repetition, and inter-
vals between repetitions. Typical short "20-Hz
signals" are narrowband pulses with principal sound
energy near 20 Hz. They are repeated at remark-
ably constant intervals. Only about 3% of the
sounds reported here had components as low as 20
Hz.
The miscellaneous moans that were recorded from
finbacks mainly resemble the category that Watkins
(1981) called "higher frequency sounds". However,
most of his recordings of these sounds were down-
ward-sweeping pulses, eg., 75-40 Hz, with emphasis
around 40 Hz. We did not record sounds similar to
Watkins' low-frequency rumble or ragged pulse
367
FISHERY BULLETIN: VOL. 84, NO. 2
categories, nor did we record his nonvocal, sharp im-
pulsive category.
Our experience with finback and Bryde whales in
the Gulf of California showed that underwater-
generated sounds were not produced when visible
animals were at or very close to the surface. Excep-
tions were those sounds which, although principally
airborne (eg., blow and snort sounds), established
a physical coupling with the water medium allow-
ing detection by hydrophone The typical short
"20-Hz signals" noted from finback whales in other
locations (Northrop et al. 1968) appear in trains that
are interrupted after 3 to 22 min of pulsing (equi-
valent to expected dive times, Fig. 8). We believe that
these interruptions that last from 1 to 6 min
represented surface time. Blue whale sounds in
southeast Pacific waters had silent interruptions that
were associated with surfacing and ventilation (Cum-
mings and Thompson 1971). Winn et al. (1970) cor-
related certain "cries" and "ratchet" sounds with sur-
facing behavior of humpback whales. Data from the
present cruise, our recordings of typical short "20-Hz
signals", our recordings from blue whales, and from
work on humpback whales, apparently reveal sur-
face and dive times as learned through monitoring
underwater whale sounds.
Possible explanations for our lack of 20-Hz short
pulses in the presently described recordings and for
the absence of other classes of sounds that Watkins
(1981) has commonly recorded from finbacks are
seasonality and insufficient sampling. We now know
that seasonality is involved.
Watkins (1981) recorded the pulses in the North
Atlantic only from late October to early May. Cum-
mings and Thompson (fn. 4) recorded them in the
North Pacific from September to April, and Thomp-
20
40
60
TIME (sec)
100
00
(/>
LU
>
r-
<
-J
111
CC
20
40
60 80
TIME (min)
100
120
140
Figure 8— (a) Spectrogram of short "20-Hz signals" from finback whales; the effective analyzing filter bandwidth was 0.4 Hz. (b) Strip
chart showing 11 trains of short "20-Hz signals" with interruptions between; the filter passband was 12.5-25 Hz.
368
CUMMINGS ET AL.: SOUND FROM BRYDE AND FINBACK WHALES
son and Friedl (1982), working off Hawaii, recorded
them only from the end of August to late April. Nor-
throp et al. (1968), in the North Pacific, noted them
from October to March. Finally, in recordings from
finbacks in March 1985 (Gulf of California) typical
20-Hz short pulses were the predominant sound
(Thompson et al.6). Like the well-known songs of
humpback whales, these sounds are probably a
manifestation of social or other behavior which oc-
curs seasonally. According to Watkins (1981) they
"perhaps were a courtship or reproductive display".
Watkins and others apparently have not noted our
frequently recorded 68-34 Hz long moans.
There have been many technical advances in bio-
acoustic signal acquisition and processing. Long-
term recordings can be used for obtaining informa-
tion about certain behaviors, presence or absence of
animals, or perhaps distribution of a given species,
without the presence of an observer (Cummings et
al. 1983). Great gains are being made in the field of
sighal processing wherein computer- and optically
aided automatic acoustic pattern recognition is possi-
ble for a number of sounds with recognizable
physical criteria. However, regardless of technical ad-
vances, the use of such tools is severely limited
without first knowing the behavioral significance of
the animal sound production. In reality, the two are
mutually dependent. An analogous situation would
be the use of the most refined instrumentation
available for listening in on a conversation carried
out in a foreign language that is unfamiliar to the
observer. Although extremely difficult to fulfill, the
need for related behavioral information on finback
whales is paramount.
For these and other reasons, descriptions of sounds
from identified sources should be given in detail
along with adequate description of the recording in-
struments. Recording procedures and analyses can
greatly affect the apparent variability of sounds.
Moreover, one must be careful to consider the large
variety of sounds that is apparent in any species of
marine mammal (including the finback whale, as
shown in this report) and the relatively limited
number of recorded sounds of any species.
ACKNOWLEDGMENT
The authors thank R. S. Gales for assisting in the
field observations; D. R. Nelson for assisting in the
"Thompson, P. 0., L. T. Findley, and 0. Vidal. Finback whale
underwater sounds recorded near Guaymas, Mexico. Manuscr. in
prep. Paul 0. Thompson, 4256 Sierra Vista, San Diego, CA 92103.
diving and other field work; R. Ludwig and crew for
operating the ship; W. A. Watkins and W. E. Schevill
for comments on the research; and M. Richardson,
R. Hawley, and T Rydlinski for producing the
finished manuscript. This work was supported by
funds for Independent Research (Naval Ocean
Systems Center) and by the Office of Naval Research
(R. C. Tipper and B. Zahuranec) by means of con-
tracts with the San Diego Society of Natural History
and Scripps Institution of Oceanography.
LITERATURE CITED
Beamish, P.
1978. Evidence that a captive humpback whale (Megaptera
novaeangliae) does not use sonar. Deep-Sea Res. 25:469-
472.
Beamish, P., and E. Mitchell.
1971. Ultrasonic sounds recorded in the presence of a blue
whale, Balaenoptera musculus. Deep-Sea Res. 18:803-809.
1973. Short pulse length audio frequency sounds recorded in
the presence of a minke whale (Balaenoptera acutorostrata).
Deep-Sea Res. 20:375-386.
Cummings, W. C, D. V. Holliday, W. T Ellison, and B. J.
Graham.
1983. Technical feasibility of passive acoustic location of bow-
head whales in population studies off Pt. Barrow, Alaska.
Tracor, Inc., San Diego, Doc No. T-83-06-002, 169 p.
Cummings, W. C, and P. O. Thompson.
1971. Underwater sounds from the blue whale, Balaenoptera
musculus. J. Acoust. Soc Am. 50:1193-1198.
Edds, P. L.
1981. Variations in vocalizations of fin whales, Balaenoptera
physalus, in the St. Lawrence River. M.S. Thesis, Univ.
Maryland, College Park, 126 p.
Northrop, J., W. C. Cummings, and M. F. Morrison.
1971. Underwater 20-Hz signals recorded near Midway
Island. J. Acoust. Soc Am. 49:1909-1910.
Northrop, J., W. C. Cummings, and P. O. Thompson.
1968. 20-Hz signals observed in the central Pacific J. Acoust.
Soc. Am. 43:383-384.
Patterson, B., and G. R. Hamilton.
1964. Repetitive 20 cycle per second biological hydroacoustic
signals at Bermuda. In W. N. Tavolga (editor), Marine bio-
acoustics, p. 125-145. Pergamon Press, N.Y.
Schevill, W. E., and W. A. Watkins.
1962. Whale and porpoise voices. Woods Hole Oceanogr.
Inst, (with a phonograph record), 24 p.
Schevill, W. E., W A. Watkins, and R. H. Backus.
1964. The 20-cycle signals and Balaenoptera (fin whales). In
W N. Tavolga (editor), Marine bio-acoustics, p. 147-152. Per-
gamon Press, N.Y.
Thompson, P. O., and W C Cummings.
1969. Sound production of the finback whale, Balaenoptera
physalus, and Eden's whale, B. edeni, in the Gulf of Califor-
nia (A). In Proceedings of the Sixth Annual Conference on
Biological Sonar and Diving Mammals, p. 109. Stanford Res.
Inst., Menlo Park, CA.
Thompson, P. O., W C. Cummings, and S. J. Kennison.
1977. Sound production of humpback whales, Megaptera
novaeangliae, in Alaskan waters. [Abstr.] J. Acoust. Soc
Am. 62(Suppl. 1):S89.
369
FISHERY BULLETIN: VOL. 84, NO. 2
Thompson, P. 0., and W. A. Friedl.
1982. A long term study of low-frequency sounds from several
species of whales off Oahu, Hawaii. Cetology 45, 19 p.
Walker, R. A.
1963. Some intense, low-frequency underwater sounds of wide
geographical distribution, apparently of biological origin. J.
Acoust. Soc Am. 35:1816-1824.
Watkins, W. A.
1967. Air-borne sounds of the humpback whale, Megaptera
nwaeangliae. J. Mammal. 48:573-578.
1981. Activities and underwater sounds of fin whales. Rep.
Whales Res. Inst. 33:83-117.
Weston, D. E., and R. I. Black.
1965. Some unusual low- frequency biological noises under-
water. Deep Sea Res. 12:295-298.
Winn, H. E., P. J. Perkins, and T. C. Poulter.
1970. Sounds of the humpback whale In Proceedings of the
Seventh Conference on Biological Sonar and Diving Mam-
mals, p. 39-52. Stanford Res. Inst., Menlo Park, CA.
370
INCREASED FOOD AND ENERGY CONSUMPTION OF
LACTATING NORTHERN FUR SEALS,
CALLORHINUS URSINUS
Michael A. Perez and Elizabeth E. Mooney1
ABSTRACT
Data from pelagic northern fur seals, Callorhinus ursinus, taken during 1958-74 by the United States
and Canada in the eastern Bering Sea were analyzed to determine relative feeding rates of lactating
and nonlactating females. Estimates of the quantity of food and energy consumed by these seals during
July-September were evaluated. The average daily feeding rate (adjusted for percentage of time feeding
at sea) for lactating seals is 1.6 times that for nonlactating seals. During July-September, the total popula-
tion of lactating and nonlactating females were estimated to consume 146.5 x 103 1 (204.5 x 109 kcal)
and 43.1 x 103 1 (60.2 x 109 kcal) of food respectively. Fish accounted for 66.4% of food biomass (69.4%
of total energy consumption); squid, the remainder.
The energetics of reproduction, especially during
lactation, are poorly documented for free-ranging
animals. The various reproductive states of domestic
mammals, e.g., cattle, sheep, etc., have been exten-
sively studied; and there has also been considerable
research on rodents, e.g., mice, voles, etc., under
both laboratory and field conditions. As a result of
these studies it is widely accepted that most nursing
females require considerably more energy than do
nonnursing females of the same species, age, and
size. Brody (1945) also noted that the maintenance
requirements of lactating animals are elevated
relative to nonlactating animals.
In some mammalian species, food intake during
lactation may be up to 5 times greater than that
observed in nonpregnant, nonlactating adult
females, and lactating animals often convert con-
siderable body substance to support the lactation
process (Baldwin 1978). Previous studies on ter-
restrial mammals have specifically shown increased
energy consumption by lactating females relative
to nonlactating females. For example, captive deer
mice, Peromyscus maniculatus, have a 96% to a
194% increase (Stebbins 1977); and ewes have a
116% increase (Engels and Malan 1979). The bat,
Myotis thysanodes, which undergoes thermoregula-
tory physiological changes during reproductive
stages, also has higher energy requirements for lac-
tating females (Studier et al. 1973). Lactating
humans are recommended to increase food con-
sumption by at least 25% (Eagles and Randall 1980);
however, some lactating humans in Guatemala meet
their additional lactation energy costs by fat loss
(Schutz et al. 1980).
There are few studies on the energetics and con-
sumption of food during lactation by marine mam-
mals. Lactation appears to drain the energy reserves
of large baleen whales; the blubber of lactating
females (e.g., blue, Balaenoptera musculus, and fin,
Balaenoptera physalus, whales) is lean and
emaciated compared with nonlactating females
(Lockyer 1978, 1981a). Lockyer (1981b) estimated
that adult female sperm whales, Physeter macro-
cephalus, need to increase their food intake by about
32-63% during lactation, meaning that they would
need to feed 4 or 5 times daily to meet higher energy
requirements. Lockyer (1981b) also estimated that
minke, Balaenoptera acutorostrata, and fin whales
increase their food intake by 75 and 86%, respec-
tively. Spotte and Babus (1980) did not find a
significantly increased mean feeding rate for one
captive, pregnant bottlenosed dolphin, Tursiops
truncatus, but standard deviations were consistently
greater. In addition, during the first 3V2 mo of
lactation, a captive mother bottlenosed dolphin con-
sumed 170% more food than she did while not lac-
tating the following year (Mooney2). Costa and Gen-
try (in press) derived metabolic rates for lactating
female northern fur seals from measurements of
water flux and discussed the components of the
'Northwest and Alaska Fisheries Center National Marine Mam-
mal Laboratory, National Marine Fisheries Service, NOAA, 7600
Sand Point Way, N.E., Seattle, WA 98115.
2Mooney, E.E. 1981. Unpubl. data. Northwest and Alaska
Fish. Cent. Natl. Mar. Mammal Lab., Natl. Mar. Fish. Serv.,
NOAA, 7600 Sand Point Way NE, Seattle, WA 98115.
Manuscript accepted August 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
371
FISHERY BULLETIN: VOL. 84, NO. 2
energy budget for females and pups during the first
two months of the reproductive cycle.
Although most mammals ingest more food while
they are lactating than they would in a nonlactating
state, many species of phocid seals fast during the
lactation period (Harrison 1969). These seals (e.g.,
gray seal, Halichoerus grypus, and northern ele-
phant seal, Mirounga angustirostris) do not feed
from parturition to weaning of the young, and all
of their energy needs during lactation must be met
by metabolism of in situ energy such as fat reserves.
This behavior has been well documented for the gray
seal (e.g., Amoroso and Matthews 1951, 1952; Fedak
and Anderson 1982) and also for the harp seal, Phoca
groenlandica, (Lavigne et al. 1982). However,
metabolism of fat reserves does not reduce the
energetic costs of producing offspring; it merely
shifts the time that energy must be acquired, at
some energy cost for storage (Millar 1978).
The objectives of this study were to show, using
both stomach content and body mass data, that lac-
tating female fur seals ingest more food than nonlac-
tating females in order to meet their increased
energy requirements for maintenance and milk pro-
duction, and to make estimates of the magnitude of
this difference in food ingestion. For this study, we
utilized data from postpartum and nonpregnant
adult, female northern fur seals, Callorhinus ur-
sinus, taken pelagically during 1958-74.
METHODS
Data on the contents of stomachs from the female
northern fur seals taken pelagically (Fig. 1) in the
eastern Bering Sea during 1958-74 by the United
States and Canada were analyzed to determine the
relation between lactation and food consumption
during the summer breeding season. Only data from
female fur seals (age >4 yr) which had information
on both body mass and stomach content mass were
included. Age was determined from longitudinal
half-sections of the upper canine teeth by counting
the annual growth layers in the dentine, a method
widely accepted by researchers during recent
decades to determine the age of many species of
mammals (Klevezal' and Kleinenberg 1967).
Methods used during 1958-74 to determine age,
reproductive status, and the different items in the
stomachs were discussed by Lander (1980).
The data used in this study represented stomach
contents under different stages of digestion; how-
ever, it was not possible to make comparisons be-
tween stages because no data on stages of diges-
tion were recorded. Rates of digestion of all prey
were assumed to be similar for all females during
the same time interval. In our study, all postpartum
females were considered lactating, and all non-
pregnant (not postpartum) females were considered
nonlactating.
Statistical Methods
The cumulative frequency distributions of data on
mass of total stomach contents for both lactating
and nonlactating females were compared using the
one-tail Kolmogorov-Smirnov two-sample test
(Siegel 1956).
Data from seals with empty stomachs or stomachs
with only a trace of contents (i.e., <10 cc) were con-
sidered as zero mass and pooled with data from seals
with food in their stomachs. Data for different ages
and months were pooled to provide sufficient sam-
ple size for analysis because the normal approxima-
tion to compute confidence limits is only valid if sam-
ple sizes are adequate (Cochran 1977). In order to
use parametric statistics, and yet not seriously
violate basic assumptions of normality, data were
transformed by the modified arcsine transformation
discussed by Zar (1974):
X = \/ M + 0.5 arcsin \/ (S + 0.375)/(M + 0.75)
where M is the net body mass (excluding mass of
stomach contents, S) and X is the transformed value.
This equation was used because of its utility where
a large number of the data were from stomachs con-
taining only a trace or less.
The transformed values on the mass of total
stomach contents (expressed as a percentage of net
body mass) obtained from the above equation were
transformed back to percentages to obtain means.
We calculated an index of the relative intake of food
by lactating females compared with that of non-
lactating females by multiplying the ratio of their
respective mean mass of stomach contents by 100.
The £-test for two independent samples, with the
assumption of unequal variance (Snedecor and
Cochran 1980), was used on the transformed data
to determine if any significant difference in total
food consumption and body mass existed between
females of different reproductive status.
The relative importance of individual prey in the
total diet was assessed using the modified volume
percentage method (Bigg and Perez 1985). Only
foods with fleshy remains were used as evidence of
diet in this method, and the procedure combined the
traditional methods of volume and frequency of oc-
currence. The proportion of total fish and total squid
372
PEREZ and MOONEY: LACTATING NORTHERN FUR SEALS
+
+
+
&
-*&=-
Unimak Pass
61° N
59°
57°
55°
53°
51'
177°W
167°
157c
Figure 1.— Locations where 3,494 adult female northern fur seals (ages >4 yr), whose data were analyzed in this study, were taken
by the United States and Canada in the eastern Bering Sea during July-September 1958-74.
in the diet was determined by frequency, while the
ration of each species within only fish and squid was
determined by volume. Statistical comparison of the
diets of lactating and nonlactating females included
1) the Spearman rank correlation coefficient (Siegel
1956; Fritz 1974), 2) percentage similarity (Goodall
1973), and 3) 2 x 2 contingency table analysis (Zar
1974) on the number of stomachs with fish or squid.
Feeding Time at Sea
The largest breeding population of northern fur
seals (currently estimated at 8.7 x 105 for a declin-
ing population; North Pacific Fur Seal Commission
1984) resides on the Pribilof Islands during the sum-
mer months. Pups first appear in late June (Bar-
tholomew and Hoel 1953) and the mean date of pup
birth based on recent data is 5 July (Gentry and Holt
in press); a date median between values cited by Bar-
tholomew and Hoel (1953) and Peterson (1968).
After this time, adult females spend a number of
days on shore in several visits to the islands during
June-November, and the intervening days between
these visits at sea foraging for food (Bartholomew
and Hoel 1953; Peterson 1968). They do not feed
daily.
373
FISHERY BULLETIN: VOL. 84, NO. 2
Once arriving at the rookery, a parturient female
gives birth to one pup, initiates lactation, comes into
estrus, and copulates with a male, but does not feed.
Gentry and Holt (in press) provided data showing
that the average adult female is on shore about 1
d before and 7.4 d after parturition. Each subse-
quent shore visit lasts about 2.2 d (Peterson 1968;
Gentry and Holt in press). The duration of the first
sea trip is the shortest (4.8 d), with the duration of
the subsequent sea trips increasing at a rate of an
additional 1.2 d/30 d postpartum (Gentry and Holt
in press).
Recent data collected on the Pribilof Islands by
Gentry and Holt (in press) suggests that nonpreg-
nant (= nonlactating) adult females arrive later
(about 8 d) on the rookeries and that they may show
a somewhat different behavioral pattern than preg-
nant females. Their first foraging trip at sea is
longer (8.9 d), but each of their subsequent shore
visits is of constant duration (2.5 d). From these data
we derived values for total percent of time spent
at sea during July- September (92 d) for the average
adult female. Assuming birth of pups on 5 July, this
was 69.3 and 75.9% for lactating and nonlactating
females, respectively. However, it should be noted
that individual females vary from these averages
because the period during which adult females first
arrive on the rookeries extends over 30 d (Bartholo-
mew and Hoel 1953; Peterson 1968; Gentry and Holt
in press).
Feeding Rate Calculations
Bigg et al. (1978) provided data on feeding rates
for three captive adult female northern fur seals.
Their data for these seals were 5,977 kcal/d (3.0
kg; 6.7% of body mass), 6,118 kcal/d (3.1 kg; 7.6%
of body mass), and 5,055 kcal/d (2.5 kg; 8.5% of body
mass). These captive northern fur seals were main-
tained with a diet of Pacific herring (2.01 kcal/g dur-
Table 1 .—Body mass (minus stomach contents mass) of lactating
(postpartum) and nonlactating female northern fur seals (ages >4
yr pooled) taken pelagically in the eastern Bering Sea and western
Alaska, 1958-74.
Lactating
Nonlactating
x and 95% C.I.
x and 95% C.I.
Month
n
(kg)
n
(kg)
June
M99
41.10 + 0.54
128
29.77 + 1.41
July
743
34.04 + 0.42
376
31.49 ± 0.70
Aug.
1,481
35.62 + 0.30
551
31.05 + 0.57
Sept.
305
36.46 ± 0.34
118
30.19 ± 1.36
July-Sept.
2,529
35.26 ± 0.23
1,045
31.11 ± 0.42
ing winter), and it was necessary to consider the
energetic concentration of the seal's diet in the
wild with respect to the data in Bigg et al. (1978).
We derived the following relationship from these
data:
Daily energy consumption (kcal/d) = 375.47 M° 75
by averaging the results given for the three captive
seals. We calculated average daily feeding rates
using this relationship and data on seal body mass.
RESULTS
Body Mass
Table 1 gives the mean values of body mass of
adult female northern fur seals (age >A yr) taken
during June-September in the eastern Bering Sea
and western Alaska. During July-September, the
average lactating female (mean 35.3 kg, median age
10 yr) had a body mass 1.13 times that of the
average adult nonlactating female (mean 31.1 kg,
median age 5 yr; seals age ^4 yr only). However,
as Figure 2 shows, lactating and nonlactating
females of the same age were similar in body mass.
The differences shown in Table 1 are primarily due
to the higher proportions of lactating females at
older ages (Lander 1981).
Lactating females exhibited a significant (P <
0.001) loss of 7.1 kg of body mass between June and
July following parturition (Table 1). This is based
60 r-
50 -
_ 40 -
en
■o,
CD
E 30
20
10
10
Age
15
> 18
'Pregnant (prepartum) females. Body mass does not include fetal mass.
Figure 2.— Mean body mass (minus stomach contents mass) of lac-
tating and nonlactating female northern fur seals by age taken
pelagically in the eastern Bering Sea and western Alaska during
July-September 1958-74.
374
PEREZ and MOONEY: LACTATING NORTHERN FUR SEALS
on data for pregnant females, after excluding fetal
mass, which we used to represent body mass of lac-
tating females prior to parturition. Figure 3 shows
that this loss in body mass occurred for all ages.
60
50 -
40
E 30
20
10
■ Pregnant
▲ Lactating
10
Age
15
> 18
Figure 3.— Mean body mass (minus stomach contents and fetal
mass) of pregnant (prepartum) and lactating (postpartum) female
northern fur seals by age taken pelagically in the eastern Bering
Sea and western Alaska during June and July respectively
(1958-74).
Relative Food Intake
We found a significant difference (P < 0.05) in the
relative magnitude of food consumption between lac-
tating and nonlactating female northern fur seals
during July-September, but not October, and Figure
4 shows the relative percentage frequency of the
number of lactating and nonlactating adult females
showing different masses of stomach contents dur-
ing July-September (pooled data). It is apparent that
a greater proportion of lactating females contained
food in their stomachs. Lactating females signifi-
cantly (P < 0.001) ingested more food because they
had lower cumulative percentages of empty stom-
achs and stomachs with smaller quantities of food
than did nonlactating females.
Table 2 presents the results of analyses between
lactating and nonlactating females for the July-
September period by time of collection during the
day. Our calculated values of the index of relative
food intake after sunrise were 162% during 0-3 h,
166% during 4-7 h, 537% during 8-11 h, and 585%
during 12-15 h (P < 0.05). The calculated index
values during 8-15 h after sunrise are excessive,
presumably an artifact of food digestion in the
stomach.
c
01
u
c
01
a.
>■
u
c
01
3
or
01
>
45
40 -
35
30 -
25
£ 20 -
75 15-
10
■ Lactating (N=981)
"J Nonlactating (N=2513)
rirl J
rl •* J LM
hi [■ tH- ■" "■» i" ' " i " — ' '" "
Empty
Trace
<0.2
CM
CM
CN
CN
T
o
CM
I
O
m
I
o
o
T—
CM
CO
Tf
o
A
Total mass of stomach contents (kg)
Figure 4.— The relative percentage frequency of lactating and nonlactating female northern
fur seals (age >4 yr) by total mass of stomach contents during July-September.
375
FISHERY BULLETIN: VOL. 84, NO. 2
Table 2.— Body mass and arcsine transformed mass of stomach contents (expressed as a percent-
age of body mass) for lactating (LACT) and nonlactating (NON) female northern fur seals (age >4
yr) by hour of collection after sunrise during July-September 1958-74. The relative consumption index
(percentage expression of the ratio of the proportion of body mass which was stomach contents for
lactating females relative to that for nonlactating females) is also given.
Hours
after
sunrise
Repro-
ductive
condition
n
Body mass
(kg)
x and 95% C.I.
Mass of stomach
percentage of t
Arcsine units
x SE
contents as
>ody mass
Percentage
units
Relative
consumption
index
(0/0)
X
Pi
0-3
LACT
NON
312
108
35.7 + 0.7
31.4 ± 1.5
1,355.81
997.74
57.24
83.33
1.558
0.964
161.6
<0.05
4-7
LACT
NON
1,070
381
35.5 ± 0.4
31.1 ± 0.7
623.22
453.29
25.86
35.42
0.333
0.201
165.7
<0.05
8-11
LACT
NON
906
365
35.0 ± 0.4
31.4 + 0.7
408.80
167.27
24.46
20.22
0.145
0.027
537.0
<0.05
12-15
LACT
NON
225
127
34.6 + 0.7
30.5 ± 1.2
415.60
161.66
47.64
36.38
0.152
0.026
584.6
<0.05
'Significance levels for comparisons between the mean proportions of body mass which was stomach contents
(arcsine units) for lactating and nonlactating females were determined by t tests.
To derive a single index value for relative food
consumption between lactating and nonlactating
females, we performed alternative calculations. In
this case we did not simply pool data because that
would not adequately account for digestion trends.
Northern fur seals feed primarily at night or in the
early morning hours (Fiscus et al. 1964; Gentry et
al. in press); therefore, we considered the value at
0-3 h after sunrise (0.96; Table 2) as the relative daily
quantity of stomach contents for nonlactating seals.
Feeding more than once a day to satisfy only energy
needs of maintenance and routine activity should be
done by all fur seals, and would already be included
in these results (Table 2) when the inherent relative
rate of digestion is examined. However, lactating
females require additional food intake for milk pro-
duction, and we added an increment (0.12) to the
value observed at 0-3 h after sunrise (1.56; Table
2) to calculate an adjusted index of 1.68% of body
mass. This incremental value was derived first by
calculating the rate of decrease between data values
for partially digested stomach contents at the dif-
ferent hourly time intervals. We assumed the rate
of digestion throughout the day was the same for
lactating females as that observed for nonlactating
females. Next, keeping the value for lactating
females at 0-3 h after sunrise (1.56) as constant, we
summed the absolute value of the differences be-
tween the expected values for remaining stomach
contents and the observed values in Table 2 to ob-
tain a value of 0.12. We then calculated a value of
174% as our index of relative food intake (i.e., the
ratio of 1.68 for lactating females relative to 0.96
for nonlactating females) for a typical foraging day.
However, because females do not feed every day
during the breeding season (Bartholomew and Hoel
1953; Peterson 1968; Gentry and Holt in press), the
average daily feeding rate (adjusted for percent-
age of time feeding at sea) for lactating seals is 1.6
times that for nonlactating seals during July-
September, i.e, the increased cost of lactation is
+ 59.8%.
Estimated Energy and Food Requirements
Lactating and nonlactating female northern fur
seals consumed the same species of prey in relatively
similar proportions within their diet, when feeding
in the same general area at the same time during
1958-74. Ranks of importance of prey to the diet
were significantly correlated (P < 0.05); the percent
similarity of relative prey importance by percent
modified volume was 80%; and there was no signifi-
cant difference in the frequency of food stomachs
containing fish or squid. Being culled from the same
region and for the same season, data for all adult
females were pooled.
We derived a gross energy estimate of 1.40 kcal/g
as the average energetic density of northern fur seal
prey during July-September based on their relative
dietary importance and information in the literature
on their energy content (Table 3). Using the data
on seal body mass (Table 1) and increased cost of
lactation ( + 59.8%), we calculated average daily
feeding rates of 18.2% (6.42 kg) and 11.4% (3.55 kg)
of total body mass, respectively, for the average lac-
tating and nonlactating adult female. This repre-
sents daily energy consumption requirements of
376
PEREZ and MOONEY: LACTATING NORTHERN FUR SEALS
Table 3.— Relative dietary importance, energy value and average daily consumption of prey by individual
lactating and nonlactating female northern fur seals (age >4 yr) in the eastern Bering Sea during
July-September.
Relative
Relative
dietary
importance
Energy
energy
value in
diet
Estimated average consum
ption
Biomass (kg/d)
Energy (kcal/d)
Prey
(o/o)1
(kcal/g)2
(%)3
Lactating
Nonlactating
Lactating
Nonlactating
Pacific herring
7.67
"2.17
11.95
0.49
0.27
1,070
590
Salmonids
1.87
52.01
2.69
0.12
0.06
240
130
Capelin
14.85
61.31
14.00
0.95
0.53
1,250
690
Deepsea smelt
3.30
70.76
1.81
0.21
0.12
160
90
Walleye pollock
36.11
61.41
36.51
2.32
1.28
3,270
1,800
Atka mackerel
1.05
81.58
1.19
0.07
0.04
110
60
Pacific sand lance
0.43
51.22
0.38
0.03
0.02
40
20
Flounders
1.10
51.20
0.94
0.07
0.04
80
50
Subtotal (fish)
66.38
91.46
69.47
4.26
2.36
6,220
3,430
Gonatid squid
33.62
101.27
30.53
2.16
1.19
2,740
1,510
Total
100.0
91.40
100.00
6.42
3.55
8,960
4,940
'Percent modified volume of stomach contents data collected during 1958-74.
2For some species, data were derived from results of proximate analyses on muscle tissue composition using energetic
density factors of 9.50, 5.65 and 4.00 kcal/g (gross energy), respectively for fat, protein, and carbohydrate (Watt and Merrill
1963). Data for other species were based on bomb calorimetry analyses of whole specimens.
3Derived by multiplying columns 1 and 2, and summing to 100%.
4Based on proximate analysis data for Pacific herring, Clupea harengus pallasi, in Bigg et al. (1978).
5Based on proximate analysis data for salmonids (Salmonidae); Pacific sand lance, Ammodytes hexapterus; and flounders
(Pleuronectidae) in Sidwell (1981).
6Based on data from heat of combustion in analyses of whole fish specimens of capelin, Mallotus villosus, and walleye
pollock, Theragra chalcogramma [Miller, L K. 1978. Energetics of the northern fur seal in relation to climate and food resources
of the Bering Sea. U.S. Mar. Mammal Comm. Rep. MMC-75/08, 27 p.]
'Based on proximate analysis data for deepsea smelt (Bathylagidae) in Childress and Nygaard (1973).
8Based on proximate analysis data for Atka mackerel, Pleurogrammus monopterygius, in Kizevetter (1971).
9Average value of prey species in diet adjusted by their relative dietary importance.
10Perez, M. A. 1984. Unpubl. data. Northwest and Alaska Fish. Cent. Natl. Mar. Mammal Lab., Natl. Mar. Fish. Serv.,
NOAA, 7600 Sand Point Way NE., Seattle, WA 98115.
8,960 kcal and 4,940 kcal for the average, individual
lactating and nonlactating adult female northern fur
seal during July-September (Table 3). Average
postpartum females not in a lactating state would
have a daily energy consumption requirement of
5,430 kcal or feeding rate of 11.0% (3.89 kg) of total
body mass.
Table 3 also provides estimates for each food item
of the total energy and biomass consumed daily by
the average individual adult female. Lactating
females each consume about 6,220 kcal/d gross
energy (4.3 kg/d) of fish and 2,740 kcal/d gross
energy (2.2 kg/d) of squid, and each nonlactating in-
dividual consumes about 3,430 kcal/d gross energy
(2.4 kg/d) offish and 1,510 kcal/d gross energy (1.2
kg/d) of squid. Female northern fur seals are not
able to feed every day, and thus estimated consump-
tion for the average foraging day is 8,980 kcal/d
gross energy (6.1 kg/d) of fish and 3,950 kcal/d gross
energy (3.1 kg/d) of squid by lactating seals, and
4,530 kcal/d gross energy (3.1 kg/d) of fish and 1,990
kcal/d gross energy (1.6 kg/d) of squid by nonlac-
tating females.
We also calculated estimates of the total energy
in biomass consumed by all adult females during
July-September in the eastern Bering Sea (Table 4).
Because the northern fur seal population has been
declining in recent years (North Pacific Fur Seal
Commission 1984) we used 80% of the estimated
population values given by Lander (1981): 2.61 x
105 pregnant/postpartum and 1.19 x 105 nonpreg-
nant adult females (age ^4 yr). We assumed all of
these seals are present in the eastern Bering Sea
during this period. Because 5% of the pups born on
St. Paul Island, Pribilof Islands, between 1975 and
1982 died on the rookeries during July and August
(Kozloff 1985), we modified our calculations to
reflect the number of postpartum females which are
nonlactating. We thus estimated a total of 2.48 x
105 lactating and 1.32 x 105 nonlactating adult
females (age >A yr). Multiplying individual estimates
by these population totals, lactating females con-
sume an estimated collective total of 204.5 x 109
kcal gross energy (146.5 x 103 1) and nonlactating
females consume an estimated collective total of
60.2 x 109 kcal gross energy (43.1 x 103 1) of food.
Therefore, all adult female northern fur seals con-
sume an estimated collective biomass of 189.6 x
103 1 with a gross energy value of 264.7 x 109 kcal
during July-September, of which 69.4% of this
energy (183.7 x 109 kcal; 125.9 x 103 t) are fish
and 30.6% (81.0 x 109 kcal; 63.7 x 103 1) are squid.
377
FISHERY BULLETIN: VOL. 84, NO. 2
Table 4.— Estimated energy value and consumption of fish and squid by the total population of lactating
and nonlactating female northern fur seals (age >4 yr) during July-September (92 days).
Prey
Lactating females
Nonlactating females
Individual
average
Energy consumption
(kcal/g)1 (kg/d)1
Total seasonal
consumption by
population (2.48 x 105)
Biomass Energy
(x 103 t) (x 109 kcal)
Individual
average
consumption
(kg/d)'
Total seasonal
consumption by
population (1.32 x 105)2
Biomass Energy
(x 103t) (x 109 kcal)
Fish
1.46
4.26
97.2
141.9
2.36
28.7
41.8
Squid
1.27
2.16
49.3
62.6
1.19
14.4
18.4
Total
1.40
6.42
146.5
204.5
3.55
43.1
60.2
'From Table 3.
includes postpartum females that fail to lactate.
DISCUSSION
The food consumption data presented in Table 2
were based on partially digested stomach contents,
and thus underestimate the actual feeding rates of
adult female northern fur seals. It is apparent from
these data that lactating seals obtain most of their
energy needs by filling their stomachs slightly more
than the nonlactating seals early in the day and by
eating additional food later in the day. Any female,
whether lactating or not, may eat more than once
during the day, as captive northern fur seals often
do (Spotte 1980). Females must feed more than once
during the 24-h period (on those days when they are
able to feed) to meet their daily food requirements
because the maximum observed stomach contents
by percentage of body mass during July-September
1958-74 were 13.8 and 8.2%, respectively, for lac-
tating and nonlactating females (Perez3), which are
less than their predicted feeding rates. In addition,
digestion does vary among individual seals and with
the type and amount of prey eaten (Bigg and Faw-
cett 1985). However, the data in Table 2 should be
typical of the relative relationship between lactating
and nonlactating females if actual feeding rates
could be measured for free-ranging seals.
Lactating northern fur seals were estimated to
consume 8,960 kcal/d (gross energy), of which 3,520
kcal/d (gross energy) represent the additional intake
of food related to lactation. Energy expenditures for
maintenance and routine activity not directly at-
tributable to lactation were estimated to be 5,440
kcal/d (gross energy). This estimate is about 5.4
times the amount predicted (1,010 kcal/d metaboliz-
able energy or 49.0 WO for basal metabolism by the
relationship between metabolic rate (MR) in watts
3Perez, M. A. 1981. Unpubl. data. Northwest and Alaska
Fish. Cent. Natl. Mar. Mammal Lab., Natl. Mar. Fish. Serv.,
NOAA, 7600 Sand Point Way NE, Seattle, WA 98115.
(W) and body mass (M) shown by Kleiber (1961) (MR
(W) = 3.39 M° 75).
These estimates are not typical of energy expen-
diture during the first week (7.4 d average) post-
partum, a period during which the parturient female
does not feed. Lactating seals must metabolize their
energy from fat reserves during this period (in-
cluding the day before parturition when they usually
do not feed, although we considered only the post-
parturition period). The loss in body mass (Table 1)
in postpartum females following parturition ac-
counts for some of this metabolism of energy from
fat reserves. This loss includes about 0.6 kg (12%
of pup mass as in harp seals, Lavigne and Stewart
1979) of placental matter and 3.3 kg (7% prepar-
turient female mass) of amniotic and other fluids
during parturition (Costa and Gentry in press).
There is a calculated net mass loss of 3.2 kg. Loss
of body water, as has been reported for some mam-
mals, e.g., cattle (Degen and Young 1980) is also
probably part of this loss. In addition, this loss in-
cludes the utilization of fat reserves to satisfy energy
requirements for lactation (Sadleir 1969) during the
first few days of the pup's life, a period when par-
turient females remain on shore and do not feed
(Bartholomew and Hoel 1953; Peterson 1968; Gen-
try and Holt in press).
Our estimate of net mass loss, presumably through
fat metabolism, is an underestimate because it was
derived from mean body mass data from seals taken
at sea, and, therefore, includes lactating animals
which probably regained some body mass after their
first foraging trip at sea. Costa and Gentry (in press)
measured an average of 8.75 kg of mass loss,
presumably by tissue metabolism and water loss,
prior to the female's initial departure to sea, after
which they gained additional body mass. This situa-
tion is analogous to that in gray seals. The gray seal
does not feed during its entire 18-d lactation period
from parturition to weaning (Amoroso and Mat-
378
PEREZ and MOONEY: LACTATING NORTHERN FUR SEALS
thews 1951, 1952) and over 80% of the female's
stored energy reserves are used to feed their pup
(Fedak and Anderson 1982).
We conducted similar analyses of data comparing
pregnant and nonpregnant adult females (age >4
yr) during June-July, but we did not find any sig-
nificant difference in relative feeding rates. We,
therefore, conclude that the onset of the lactation
process, and not pregnancy, initiates increased
feeding behavior in parturient fur seals. Pregnant
northern fur seals presumably consume more food
than required by nonpregnant females (i.e., more
than that simply required as a function of body
mass). This would be necessary for growth of the
fetus, especially during winter and spring months
when they are in the North Pacific. This conclusion
was based on a preliminary examination of the
pelagic fur seal data, although the results were not
statistically conclusive. Female northern fur seals
probably also store energy in fat reserves for the
stresses of birth and the first week of lactation.
Nevertheless, any additional food intake required
by pregnant females is substantially less than that
of lactating seals.
We believe lactating females may reduce their
need for additional food intake during the last month
prior to weaning of pups because we did not find
a significant difference in food consumption between
lactating and nonlactating females during October;
however, data were few. Weaning does not occur
until late October or early November when females
abandon their pups; the mean date of weaning is
about 2 November (Peterson 1968). It should be
noted that births occur over at least a 30-d period
(Peterson 1968), and weaning of individual pups will
likewise occur over a similar time frame. It is thus
possible that pups born earlier will quit nursing
earlier than those born later in the season. The total
lactation period is about 3-5 mo. Therefore, the
feeding rate relationships and energy estimates
presented in this paper should typify those during
the first three months of lactation only, and not
necessarily during July-September.
We assumed that all postpartum females taken
during 1958-74 were lactating. We believe that this
assumption does not significantly affect our results
because only a small percentage of the postpartum
females fail to lactate or terminate lactation for one
reason or another (such as still birth or death of the
pup). Therefore, our estimate of the difference in
consumption between lactating and nonlactating
females is a conservative indicator of the magnitude
of this ratio. This is because inclusion of postpartum
females that did not lactate would have decreased
the mean value of stomach contents for the lactating
group.
Individual northern fur seals show variations in
their feeding locations. Differences may occur over
location and time. For example, lactating females
may travel great distances, e.g., at least 160 km
from the Pribilof Islands (Perez4), during their sea
trips in search of food, and they may dive up to 200
m (Gentry et al. in press) to catch prey. There are,
of course, differences in availability (e.g., walleye
pollock, Theragra chalcogramma, Smith and Bak-
kala 1982) and energetic density (e.g., Pacific
herring, Clupea harengus pallasi, Bigg et al. 1978;
deepsea smelt, Bathylagidae, Childress and Nygaard
1973) of prey by season, region, and depth. The 95%
C.I. for the importance of fish biomass in the fur
seal diet in the Bering Sea is 64.0-68.6% (Perez and
Bigg5). Therefore, the estimated quantity of fish and
squid consumed, and their relative energy contribu-
tion, may vary ±5%.
It should also be stressed that the estimates pre-
sented in this paper also depend heavily on metabolic
rate information for adult females which we ob-
tained from the literature. Individual variations
among seals will cause differences in results ob-
tained from several experiments, and future
research may provide somewhat different metabolic
rates. Should feeding rates be revised substantial-
ly, then the magnitude of energetic estimates from
these data will be affected in a corresponding direc-
tion. However, the relative ratio of food consump-
tion between lactating and nonlactating females dur-
ing the breeding season will be unaffected, and
remain about 1.6. We suggest the need for further
studies on feeding behavior and energetics of lac-
tating females and pups prior to weaning.
ACKNOWLEDGMENTS
We thank Michael Bigg and Peter Olesiuk of the
Pacific Biological Station, Nanaimo, B.C.; Daniel
Costa of the University of California at Santa Cruz,
and Roger Gentry and the late Mark Keyes of the
National Marine Mammal Laboratory, Seattle, WA,
for valuable information on the biology and behavior
of fur seals. We also thank Charles Fowler and
"Perez, M. A., Northwest and Alaska Fisheries Center National
Marine Mammal Laboratory, National Marine Fisheries Service,
NOAA, 7600 Sand Point Way NE, Seattle WA 98115, pers.
observ., 1984.
6Perez, M. A., and M. A. Bigg. 1984. Food habits of northern
fur seals (Callorhinus ursinus) off western North America. Un-
publ. rep., 67 p. Northwest and Alaska Fish. Cent. Natl. Mar.
Mammal Lab., Natl. Mar. Fish. Serv., NOAA, 7600 Sand Point
Way NE, Seattle, WA 98115.
379
FISHERY BULLETIN: VOL. 84, NO. 2
Thomas Loughlin for constructive criticism of the
draft manuscript. We are grateful to Teresa
Clocksin, Carol Hastings, Sherry Pearson, James
Kenagy, and George Antonelis, Jr., for comments,
suggestions, and technical assistance.
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381
ARRIVAL OF NORTHERN FUR SEALS, CALLORHINUS URSINUS,
ON ST. PAUL ISLAND, ALASKA
Michael A. Bigg1
ABSTRACT
The age-specific arrival times and relative numbers of northern fur seals, Callorhinus ursinus, on St.
Paul Island, Alaska, were determined from an analysis of kill data collected during 1956-82, and a review
of the fur seal literature. Arrival times differed by sex, age, and reproductive state. Arrival took place
progressively earlier with age in young males and females. Most males age >6 arrived by late June,
while most males age 5 arrived by late June to early July, those age 4 by mid-July, those age 3 by late
July, those age 2 by mid- to late August, and those age 1 by late September to early October. Females
tended to arrive later than males of the same age. Nonpregnant females age >3 arrived by mid-August,
while those age 2 arrived by mid- to late September, and females age 1 by October to early November.
Pregnant females age >4 arrived mainly by mid-July, about 1 month before nonpregnant females of the
same age. For both sexes, the number of seals returning increased between age 1 and age 3. Both sexes
appeared to stop arriving earlier and in larger numbers at about the age of sexual maturity. The process
of gradual maturation may play a role in inducing a cohort to undertake the return migration at earlier
times with age, and to cause a greater proportion to return.
The northern fur seal, Callorhinus ursinus, inhabits
the North Pacific Ocean mainly between lat. 32 °N
and 60°N (Fiscus 1978; King 1983). The species is
migratory, being pelagic and widely dispersed in
winter, and gathering on rookeries to give birth,
mate, nurse, and rest in summer. Rookeries occur
along the Asian coast on Robben, Kurile, and Com-
mander Islands, and along the North American
coast mainly on the Pribilof Islands and on San
Miguel Island. The presence of large numbers of
animals on Robben Island, Commander Islands, and
the Pribilof Islands has allowed an annual commer-
cial kill for pelts over many years.
The Pribilof Islands, in particular St. Paul Island
and St. George Island has the largest stock of seals,
numbering currently about 0.9 million (North Pacific
Fur Seal Commission 1984a). The species has been
harvested there almost every year since discovery
in 1786 (Roppel and Davey 1965; Roppel 1984). Over
the years, fishery managers learned to adjust the
kill quite specifically for seals of a particular age and
sex by making use of the arrival sequence of
migrants and their preferences for haul-out sites.
For example, Russians in the early 1800's took
juvenile males on hauling grounds, and left the
breeding adults and pups undisturbed on nearby
rookeries. Americans in the late 1800's knew that
the largest, and thus oldest, juvenile males arrived
before small males (Jordan and Clark 1898). Follow-
^epartment of Fisheries and Oceans, Pacific Biological Station,
Nanaimo, British Columbia, Canada V9R 5K6.
ing the discovery in 1950 that teeth could be used
for aging, the kill was refined further to focus on
3- and 4-yr-old males. Although the kill has been
directed primarily at young males since the early
1900's, females were taken during a herd reduction
program from 1956 to 1968.
Behavioral studies on the Pribilof Islands have
documented the arrival times for broad population
categories, such as adult and juvenile males, and
pregnant females (Jordan and Clark 1898; Barthol-
omew and Hoel 1953; Peterson 1965, 1968; Gentry
1981). However, these studies could not determine
the age-specific arrival times because no method was
available to distinguish the age of the live animals
being observed. The widely accepted arrival se-
quence was for bulls to arrive on land first, followed
by progressively younger males, progressively
younger pregnant females, and later by mostly
young nonpregnant cows (Kenyon and Wilke 1953;
Fiscus 1978). This arrival sequence was deduced
from preliminary examinations of the age and sex
composition of commercial kills and from the arrival
times of tagged individuals and to some extent from
differences in body size, at least for the 1- and 2-yr-
olds. There are no published analyses that describe
age-specific arrival times, although some unpub-
lished reports give information on arrival times.
In this study, I determine the arrival times for
seals of each age, sex, and reproductive condition
on hauling grounds and rookeries of St. Paul Island,
the largest of the Pribilof Islands. The study is based
Manuscript accepted July 1985.
FISHERY BULLETIN: VOL. 84, No. 2, 1986.
383
FISHERY BULLETIN: VOL. 84, NO. 2
mainly on an analysis of seasonal changes in the
number of animals killed of each age during
harvests. I examine the evidence for arrival times
by order of decreasing age within each sex, and com-
pare the relative numbers returning for each age
of young seals. The published and unpublished
literature on northern fur seals is reviewed for in-
formation on arrival times and abundance. The rela-
tionship between arrival schedules, relative number
returning, and onset of sexual maturity is discussed.
METHODS
The kill data from St. Paul Island used in this
study were collected during 1956-82 by the National
Marine Mammal Laboratory, National Marine Fish-
eries Service, Seattle. Most data up to 1979 were
listed by Lander (1980), who noted the method of
data collection and the number killed by age, sex,
date, and location. Kozloff (19812, 1982, 1983) listed
the data collected during 1980-82. Abegglen et al.
(1956, 1957, 1958, 1959) determined the age-specific
pregnancy rates of females killed during 1956-59.
These authors considered a female to be pregnant
when parous (carrying a term fetus), or recently
postpartum (lactating or uterus involuting). They did
not separate females into these two categories, or
determine whether postpartum females were carry-
ing a new conceptus.
Almost all males and females were killed on haul-
ing grounds rather than on rookeries. No commer-
cial kills for males took place on rookeries, and only
a few took place for females. Typically, the kill of
both sexes on hauling grounds was made between
late June and mid- August. It consisted of a series
of consecutive 5-d circuits, or rounds, of all hauling
ground sites. During each round, a crew undertook
one killing operation at each site, and killed all seals
present of a particular sex and length. The body
length limits for harvesting were set in inches (in)
from nose to tip of tail, or from nose to base of tail.
I converted all lengths to cm and standard length,
using 1 in for tail length. Lander (1980) and the
North Pacific Fur Seal Commission (1984b) noted
the annual changes in management practices on St.
Paul Island. The changes included variations in body
length limits, kill dates, quotas, kill locations, and
special kills for sex and age. I used only data that
were collected under comparable management
restrictions.
2P. Kozloff (editor). 1981. Fur seal investigations, 1980.
NWAFC Processed Rep., 96 p. National Marine Mammal Lab-
oratory, National Marine Fisheries Service, NOAA, Seattle.
Probit plots of age-specific cumulative length fre-
quencies were used to determine the percentage of
males and females of each age present in the kill for
each set of length limits. Sufficient age-length data
were not available for the plots from kills made on
St. Paul Island, but were available from samples col-
lected pelagically for research purposes by the
United States and Canada under the terms of the
North Pacific Fur Seal Commission. These data are
on file at the Pacific Biological Station, Nanaimo,
and at the National Marine Mammal Laboratory,
Seattle. The age-length data used were from seals
collected near St. Paul Island during June-August
1958-74. The lengths of females used were those of
postpartum and nonpregnant seals, the main cat-
egories of females killed on land.
I assumed that seals were arriving on St. Paul
Island when the number killed increased in suc-
cessive rounds and that arrival was completed when
the number killed reached an asymptote. These
assumptions were valid only under certain circum-
stances. One was that all seals encountered of a
designated sex and length were killed, which was
the case. Another was that the number of seals
hauled out, and thus available for killing, was a con-
stant proportion of the number alive through the
harvest season. The assumption seems reasonable
in that Gentry (1981) estimated an average of about
19% of marked juvenile males were ashore at any
one time on St. George Island. Finally, the propor-
tion of a particular age and sex killed during each
year must have been sufficiently small so as not to
have substantially reduced cohort size, and thus
altered the trend in numbers killed by round. This
qualification was probably true for all ages, except
perhaps for 4-yr-old males. Lander (1981) estimated
the harvest utilization rate of males on St. Paul
Island to be only 2.8% for age 2, 40.3% for age 3,
14.7% for age 5, but 57.3% for age 4. Escapement
rates of females from the commercial harvest were
not calculated, but were probably high. The females
killed were mainly of ages 3 and 4 with the largest
annual take for age 3 in the years studied being
9,700, and for age 4 being 6,300. These figures com-
pared with about 55,000 and 48,000, respectively,
for females present in the whole population, based
on Lander's (1981) life table for the species.
The number killed of each age up to the last day
of each round for each year was plotted to describe
the seasonal change in numbers killed. For males,
the most common last-day dates for each round were
in the series of 5-d rounds ending between 1 July
and 5 August. For years in which the dates for last-
day rounds differed from this series, the number of
384
BIGG: ARRIVAL OF NORTHERN FUR SEALS
males killed was interpolated from the annual plots,
so as to standardize the number killed by date. The
mean number of males killed, and standard error
of the mean, were determined for each date of the
last-day of rounds. During 1965-72, a kill of males
sometimes took place twice at a haul-out site in one
round, but was missed at this site in the preceding
or following round. In these cases, one of the two
kills was selected randomly and transposed to the
other round. Occasionally, sites were visited extra
times without being missed in the adjacent round.
These data were omitted.
The kill data used for females on hauling grounds
were from years in which the kills on rookeries and
hauling grounds were recorded separately, and in
which the pregnancy rates were noted. Such kills
took place only during 1956-59. These kills were
made during the 5-d rounds with the last-day dates
between 1 July and 20 August. The only kills on
rookeries for which pregnancy data could be used
were in 1956 and 1957. On 1-6 July 1956, a kill was
made on Polivina rookery. All kills made in the
region of this rookery on 1-21 July 1957 were in fact
made only on the rookery (A. Roppel3). The number
of females killed on rookeries was set by quota,
rather than by all available animals being taken, as
on hauling grounds. No body length limits were im-
posed on the kill of females on rookeries in 1956 and
1957.
To determine the relative number of each age that
returned to St. Paul Island, I reviewed the largely
subjective comments on abundance given in the
literature, and also compared the number killed
when arrival was believed to have been completed.
For the latter, the only data used were from years
when body length limits included at least 50% of the
individuals of the relevant age and when the total
number of living animals of a particular age did not
change substantially between years. The main
change in herd size was between 1956 and 1959,
when pup production on St. Paul Island decreased
by about 27% due to the killing of adult females dur-
ing the herd reduction program (York and Hartley
1981; Fowler 1982). Pup production changed little
between 1960 and 1980, although declined slightly
in 1981-82. The cumulative effect of harvesting a
cohort over several years was considered when com-
paring the relative number of each age killed. The
relative numbers of females of each age killed be-
tween 1956 and 1959 were biased slightly downward
with time by the herd reduction program during the
3A. Roppel, Northwest and Alaska Fisheries Center, National
Marine Fisheries Service, NOAA, 7600 Sand Point Way N.E.,
Seattle, WA 98115, pers. commun. July 1983.
intervening years. The bias was only slight because
of the years and ages selected for analysis, the lack
of time for the herd reduction program to have
potentially changed age distribution, and the fact
that most seals ages 1 and 2 remained at sea.
RESULTS
Effect of Body Length Limits
The lower length limit of 107 cm for males in-
cluded essentially no individuals age 1, few age 2,
but most of those >2> yr (Table 1). The upper length
limit varied by year, with the smallest upper limit
including a few ^4 yr, and the largest, a few >6 yr.
I used kill data collected from the years 1969-82 to
describe arrival times and relative numbers of males
ages 1 and 2. Data from the years 1962-82 were used
to describe the arrival time and relative number of
3-yr-olds. For males >4 yr, the relative numbers
returning by age could not be compared with one
another, or with younger males, because of the
cumulative reduction in the size of a cohort by the
harvest, and the exclusion of seals by upper length
limits. I used data from the years 1963-72 and
1980-82 to describe the arrival schedule for age 4,
and 1964-71 for ages 5, 6, and >7.
The lower length limit of 104 cm for females in-
cluded most individuals >4 yr, while the upper
length limit of 116-117 cm included mostly <5 yr.
Data collected in 1956 were used to describe the ar-
rival schedules for females >A yr, and 1958-59 for
those <5 yr. The number of females killed at age
3 during 1959 was not used due to an unusually low
pup survival in 1956 (Abegglen et al. 1959; Lander
1979).
Arrival of Males on Hauling Grounds
1 -Year-Olds
No yearling males were taken in the kill by 5
August, and thus none were likely to have been on
hauling grounds up to this time. However, few year-
ling males apparently go to hauling grounds. Osgood
et al. (1915) and Roppel et al. (1965a) indicated that
yearlings of both sexes preferred rookery edges,
near cows and pups, and only occasionally went to
hauling grounds (see section on Arrival of Males on
Rookeries).
2-Year-Olds
Very few 2-yr-old males arrived by 1 July (Fig.
385
FISHERY BULLETIN: VOL. 84, NO. 2
Table 1 .—Percent of each age included in standard length restrictions for kills of male
and female northern fur seals on hauling grounds. Percentages determined from Probit
plots of age-length cumulative length frequencies of seals collected at sea near St.
Paul Island by the United States and Canada. Sample sizes are in parentheses.
Length
limit
(cm)
Age (yr)
Years
1
2
3
4
5
6
>7
Males
(24)
(166)
(251)
(117)
(48)
(20)
(43)
107-119
1956-58, 1960
1.6
27.7
71.0
44.2
5.0
3.0
0.0
107-121
1959
1.6
27.9
76.5
55.7
8.3
4.0
0.0
107-124
1961-63
1.6
28.0
79.5
71.2
15.5
6.5
0.0
107-1135
1964-68
1.6
28.0
82.0
96.8
64.0
28.0
<1.2
1<135
1969-71
100.0
100.0
100.0
98.6
64.0
28.0
<1.2
<124
1972, 1980-82
100.0
100.0
97.5
73.0
15.5
6.5
0.0
<117
1973-75
100.0
99.2
82.0
35.0
3.0
1.5
0.0
<119
1976-79
100.0
99.5
86.0
40.0
-emales
4.0
2.0
0.0
(18)
(69)
(297)
(465)
(301)
(136)
(530)
>104
1956
0.0
16.0
48.0
89.0
97.0
99.4
3>99.9
<116
1958
100.0
99.8
98.4
80.0
54.0
31.5
<12.0
<117
1959
100.0
99.9
99.0
84.0
63.0
40.0
<16.0
1 Upper body size was the presence of a mane. A. Roppel (National Marine Mammal Laboratory,
National Marine Fisheries Service, NOAA, Seattle, WA 981 15, pers. comm. July 1983) felt that the
mane developed at a body length of about 135 cm.
1). Numbers began to increase in early July and con-
tinued to increase up to 5 August. This age group
began to arrive earlier than the yearlings. Osgood
et al. (1915) observed the first branded 2-yr-old in-
dividuals on 12 June, about IV2 mo before the first
branded yearling males on rookeries. As found in
the current study, Kenyon and Wilke (1953) noted
that 2-yr-olds were quite common by the end of July,
and after 1 August became increasingly abundant.
5000-
4000
3000
2000-
1000
21 14
^4
a 2yr
• 3yr
O 4yr
1 ,9,o/a '* ? n
Figure 1.— Mean number, and standard error, of northern fur seal
males killed of age 2-4 on hauling grounds of St. Paul Island, by
date. Data from Lander (1980) and annual reports of the National
Marine Mammal Laboratory, Seattle. Number of years of data for
each date indicated above means.
The date of peak numbers, and thus the date when
most arrived, was probably after early August. The
date when most would have arrived may be deter-
mined by assuming that the interval between the
time when seals clearly began to increase in number
and the time when essentially all seals had arrived
was the same for 2-yr-olds as for bulls and cows.
Observations by Peterson (1968) suggested that this
interval was about 1-1 V2 mo for bulls and pregnant
females. Because the number of 2-yr-old males
began to increase in early July, the arrival time for
most was probably mid- to late August. A similar
arrival time was also indicated by subtracting I-IV2
mo, the interval separating the first sightings of
tagged yearlings and 2-yr-olds, from the arrival time
of late September to early October for yearling
males on rookeries.
The number of 2-yr-olds returning appeared to be
greater than that for yearlings, but less than that
for 3-yr-olds. Roppel (fn. 3) felt that more 2-yr-old
males returned than yearling males, and Kenyon et
al. (1954) noted that many 2-yr-olds remained at
sea.
3-Year-Olds
The 3-yr-olds were already quite abundant by 1
July and reached a peak in numbers by late July
(Fig. 1), suggesting that arrival was completed by
late July. Kenyon and Wilke (1953) similarly noted
the maximum number of 3-yr-olds on hauling
grounds was after mid-July. This age group
386
BIGG: ARRIVAL OF NORTHERN FUR SEALS
appeared to have the largest number of males
returning.
4-Year-Olds
The number of males killed of age 4 remained
essentially constant during July, except for a
decrease in late July (Fig. 1). Although no distinc-
tive peak in numbers was evident, several factors
suggest the main arrival was probably completed
by mid-July. First, the number killed in the first
round (i.e., up to 1 July) was likely to have been too
large relative to later rounds because of an accum-
ulation of males that arrived before the kill began.
This situation was most obvious for kills of males
ages 5 and 6 (Fig. 2), but also could have existed
to some extent for the kill of males ages 2 and 3.
For ages 2 and 3, the accumulation would not have
been as obvious because the main arrival time was
after kills began. Secondly, the true peak in number
killed of 4-yr-olds was probably flattened by the high
harvest utilization rate of this age. Finally, an ex-
amination of the trend in numbers killed by round
for individual years indicated the seasonal pattern
was quite variable, ranging between that noted for
males age 3, and that for males age 5. For exam-
ple, the arrival time for 4-yr-olds in 1971 was similar
to that seen for the typical 3-yr-olds; it was similar
for the typical 5-yr-olds in 1968; and in 1980 it was
intermediate, with a distinctive peak in mid-July.
Such variations tended to dampen the peak. Kenyon
and Wilke (1953) remarked that the maximum
number of males older than 3 yr arrived before mid-
July. Fewer age-4 males returned than age-3 males,
probably due to the large kill at age 3.
5-Year-Olds
Most 5-yr-olds appeared to have already arrived
400-
S-
a 5yr
300-
200-
e s
B
7
7
4-
4
♦ 6yr
100-
6
e a
8
7
6
4
0-
-£=*=
=f M=
=4=
=+=
=*=
=t
r ■ i ■ ■ i
6 II 16 21 26 31
JULY
5 10 15 20
AUGUST
Figure 2.— Mean number, and standard error, of northern fur seal
males killed of age 5-6 on hauling grounds of St. Paul Island, by
date. Data from Lander (1980) and annual reports of the National
Marine Mammal Laboratory, Seattle. Number of years of data for
each date indicated above means.
by early July (Fig. 2). However, as noted for 4-yr-
olds, the kill by 1 July was probably large relative
to the number killed in later rounds. Most males
probably arrived by late June to early July, assum-
ing the time in peak numbers of 5-yr-olds was earlier
than mid-July, but not earlier than for territorial
bulls (>7 yr) on rookeries. Fewer 5-yr-olds returned
than 4-yr-olds because of the large kill of males at
age 4.
6-Year-Olds
As with 4- and 5-yr-olds, the first kill was likely
too large. Most 6-yr-olds probably arrived by late
June. Gentry (1981) tagged juvenile males on haul-
ing grounds of St. George Island in 1977 and count-
ed them during late May to mid- August 1980. Al-
though the ages were not known with certainty, the
most common age in 1977 was likely 3 yr, with a
range of 2-5 yr (R. Gentry4), and thus most males in
1980 were probably 6 yr of age. His counts indicated
numbers began to increase in late May, reached a
peak on 19-28 June 1980, and declined thereafter.
^7-Year-Olds
No males older than 6 yr of age were taken in the
annual kills on hauling grounds. This was because
the upper length limits excluded these ages from
kills, and because many males of these ages go to
rookeries for breeding rather than to hauling
grounds.
Arrival of Males on Rookeries
1 -Year-Olds
Behavioral studies suggest most yearling males
probably arrived on rookeries by late September to
early October, and the number returning was the
smallest of any age group of males. Osgood et al.
(1915) reported that branded male yearlings were
rarely seen between late July and mid- August but
became more numerous later, although they always
remained small in number. Kenyon and Wilke (1953)
mentioned yearlings of unspecified sex returned
principally in September to November, and that only
a few individuals were involved. Using counts of
tagged yearlings seen on rookeries between 17
September and 17 October, Roppel et al. (1965a)
4R. Gentry, Northwest and Alaska Fisheries Center, National
Marine Fisheries Service, NOAA, 7600 Sand Point Way N.E.,
Seattle, WA 98115, pers. commun. February 1984.
387
FISHERY BULLETIN: VOL. 84, NO. 2
suggested that the largest number of yearlings of
unspecified sex was present on 27 September to 11
October. These animals were predominantly males,
as indicated by the recorded sex ratio of 84% males
in a sample of 356 yearlings seen during 1961-65
(Roppel et al. 1965a, 1965b, 1966). Osgood et al.
(1915) noted all yearlings examined during his study
were males. Surveys by Abegglen et al. (1961) in-
dicated very few yearlings of either sex were pres-
ent on rookeries after early November.
^7-Year-Olds
Essentially all males present on rookeries during
the pupping season were bulls (Jordan and Clark
1898). According to Johnson (1968), the age of such
bulls would have been >1 yr. Peterson (1965, 1968)
noted that bulls began to arrive on rookeries in mid-
May, reached peak numbers by late June, and
declined in numbers after mid-July. No data exist
on whether old bulls arrived before young bulls.
(Lander 1981). Pregnant females age ^4 were rarely
taken on hauling grounds during July, but were in-
creasingly common during 1-15 August (Fig. 3).
Using the trend in the number of 4- and 5-yr-olds
killed after 15 August, most pregnant females prob-
ably arrived by mid-August. Because essentially all
pregnant females gave birth in July, the pregnant
females killed on hauling grounds during August
would have been postpartum. An examination of the
median dates for collection of pregnant females sug-
gested that arrival times on hauling grounds of age
^4 did not differ among ages (Table 2).
Nonpregnant
1-YEAR-OLDS.— As with yearling males, year-
ling females apparently preferred rookeries to haul-
ing grounds (Jordan and Clark 1898; Roppel et al.
1965a). No yearling females were taken on hauling
grounds during the commercial kill for females up
to 20 August.
Arrival of Females on Hauling Grounds
Pregnant, >4 Years
Very few females younger than 4 yr give birth
2000
1000
II 16 21 26 31
JULY
5 10 15 20
AUGUST
Figure 3.— Mean number, and range, of pregnant females of
northern fur seal killed of age >4 on hauling grounds of St. Paul
Island, by date. Data from Lander (1980) and annual reports of
the National Marine Mammal Laboratory, Seattle.
2-YEAR-OLDS.-Jordon and Clark (1898) and
Osgood et al. (1915) suggested 2-yr-old females also
preferred rookeries to hauling grounds. However,
a few were taken on the hauling grounds during the
harvest for females. Numbers began to increase in
mid- August (Fig. 4), and thus increases began about
1 mo later than males of the same age. Assuming
a 1-1 V2 mo interval for essentially all animals to ar-
rive, as assumed for 2-yr-old males, then 2-yr-old
females probably arrived by mid- to late Septem-
ber.
^3-YEAR-0LDS.-Very few nonpregnant fe-
males >3 yr were taken on hauling grounds in July,
but many were present by 15 August (Figs. 4, 5).
Based on the trend in the number of females killed
at 3-5 yr, the arrival of ages >S yr was essentially
completed by mid-August. Support for this conclu-
sion comes from Peterson (1965, 1968), who counted
Table 2.— Median dates of collection of pregnant and nonpregnant females of north-
ern fur seals taken during 1956, 1958, and 1959 on hauling grounds of St. Paul Island.
All dates are in August. Data from annual reports of the National Marine Mammal
Laborabory, National Marine Fisheries Service, NOAA, Seattle.
State
Age (yr)
Year
3
4
5
6
7
8
9
>10
1956
Pregnant
11
11
9
11
10
10
9
Nonpregnant
12
11
11
10
11
10
10
9
1958
Pregnant
—
9
9
9
8
10
15
10
Nonpregnant
13
11
10
10
8
10
10
8
1959
Pregnant
—
13
12
12
12
12
12
13
Nonpregnant
14
13
13
12
12
13
11
12
388
BIGG: ARRIVAL OF NORTHERN FUR SEALS
"nonbreeders" on hauling grounds and the inland
edges of rookeries. "Nonbreeders" were thought to
consist of idle females and young males. He ob-
served a sharp increase in numbers in early August
and that most arrived by mid- August. The current
study indicated the female component of Peterson's
"nonbreeders" were mainly nonpregnant females,
plus a few postpartum females. Abegglen et al.
(1956) noted an increase in the number of seals on
hauling grounds and rookery edges between 15
August and 4 September. While this increase may
have resulted from a continued influx of nonpreg-
nant females at >S yr, it may also have been due,
at least in part, to the arrival of some 2-yr-old males
and females.
The increase in number of nonpregnant females
during August consisted primarily of 3- and 4-yr-
olds. A comparison of the median dates for collec-
tion of nonpregnant females at ^3 yr on hauling
grounds suggests that arrival times were similar for
each age (Table 2).
3000-
2000-
* 2yr
• 3yr
O 4yr
/ <
N
1000-
/
/
>
0-
-i 1 9-
-9-
^
-r— + — t==t — i '
Arrival of Females on Rookeries
Pregnant, >4 Years
Females gave birth on St. Paul Island during 15
June to 10 August, with about 90% of all births com-
pleted by 20 July (Bartholomew and Hoel 1953;
Peterson 1965, 1968). The general belief that preg-
nant females arrived by order of decreasing age ap-
parently originated from Wilke (1953). He collected
571 females on rookeries from 15 June to 4 Septem-
ber and showed the median date of collection for
each age became progressively earlier with age. For
example, the median collection date for females at
MO yr was 7 July, while that for females at 3 yr
was 23 August. However, Wilke did not separate
pregnant and nonpregnant females in his calcula-
tions. The large shift in median dates probably
resulted mainly from an influx of young nonpreg-
nant females on rookeries during August, as took
place on hauling grounds.
An analysis of arrival times for pregnant females
of each age should not include seals that are non-
pregnant. Such an analysis can be made using data
collected by Wilke between 15 July and 22 July 1953
(Table 3). Although Wilke did not record pregnancy
2000
1000
16 21
JULY
26 31
5 10 15
AUGUST
20
II 16 21 26 31
JULY
5 10 15 20
AUGUST
Figure 4.— Mean number, and range, of nonpregnant females of
northern fur seal killed of ages 2-4 on hauling grounds of St. Paul
Island, by date. Data from Lander (1980) and annual reports of
the National Marine Mammal Laboratory, Seattle.
Figure 5.— Mean number, and range, of nonpregnant females of
northern fur seal killed at age >5 on hauling grounds of St. Paul
Island, by date. Data from Lander (1980) and annual reports of
the National Marine Mammal Laboratory, Seattle.
Table 3. — Median dates of collection of northern fur seal females on rookeries of St.
Paul Island during 17 June to 22 July 1953. Data from Wilke (1953) and the current
study.
Age (yrs)
Number collected by age
Date
4
5
6
7
8
9
>10
n
17 June
0
2
2
1
0
0
20
25
22 June
1
0
7
3
2
2
22
37
27 June
0
2
3
1
1
3
26
36
2 July
0
4
5
7
5
5
23
49
7 July
0
2
6
3
3
6
20
40
12 July
1
3
5
1
1
0
2
13
17 July
2
2
5
3
5
5
21
43
22 July
3
9
8
7
6
1
16
50
Median date
16 Jul
10 Jul
6 Jul
4 Jul
9 Jul
3 Jul
29 Jun
389
FISHERY BULLETIN: VOL. 84, NO. 2
rates for this sampling period, the rates were prob-
ably 90-100%, as will be shown later on rookeries
for the period 1-21 July. A comparison of median
collection dates suggests arrival may have taken
place slightly earlier with increasing age, but no
clear shift in arrival times was evident, as previously
believed. Unfortunately, the true age-specific arrival
times of parous females cannot be determined
readily from these data. The main difficulty is that
the pregnant females used in the analysis included
not just parous seals, but postpartum seals as well.
Postpartum seals usually remain on land for 2 d,
then go to sea to forage for 8 or 9 d, and repeat this
pattern about 10 times throughout the nursing
period (Peterson 1958; Gentry and Holt in press).
The potentially complex effect that returning post-
partum females could have on the trend in the num-
ber of parous females arriving of a particular age
must be considered. Other difficulties were the small
sample sizes, and the fact that the sample sizes taken
on each date did not reflect the increase in numbers
on rookeries. At this time, while a slight shift in ar-
rival times of parous females may exist with age,
more research is needed for confirmation.
Nonpregnant
l-YEAR-OLD.-Jordan and Clark (1898) felt year-
ling females did not arrive on rookeries before
September. As noted earlier for yearling males,
Kenyon and Wilke (1953) felt yearlings returned to
the Pribilof Islands mainly during September to
November, and only a few individuals were involved.
The date of arrival for most yearling females is
unclear, although it is probably after yearling males,
during October to early November. Only a small
number of yearling females had arrived by late
September to early October compared to males.
However, they arrived presumably no later than
early November, because few yearlings were pres-
ent on the rookeries after that time.
2-YEAR-OLDS. -The arrival of 2-yr-old females
on rookeries began in August, a similar time to that
seen on hauling grounds. Branding studies by
Osgood et al. (1915) suggested a few individuals
began to arrive about one month after males. The
first branded 2-yr-old female was seen on 19 July
compared to 12 June for males age 2. Thus, arrival
was probably completed also a month later than
males, by mid- to late September. Jordan and Clark
(1898) reported that 2-yr-old females began to in-
crease in numbers by about 1 August, while Ken-
yon and Wilke (1953) noted they did not begin until
late August, and the current study suggested arrival
on hauling grounds began in mid- August. Kenyon
and Wilke (1953) believed the largest number were
present in October, slightly later than suggested by
the current study. Based on the comments by Ken-
yon and Wilke (1953) and Kenyon et al. (1954), fewer
2-yr-olds returned than 3-yr-olds, but more 2-yr-olds
returned than yearlings.
>4-YEAR-OLDS.-A total of 1,533 females were
collected on rookeries during 1-6 July 1956 and 1-21
July 1957, a period covering the main pupping
season. All females were >4 yr of age. Of these, only
2% were nonpregnant, a low rate compared to 31%
nonpregnancy for the population as a whole, based
on the life table derived by Lander (1981). The low
rate likely resulted from the small number of non-
pregnant females on the rookeries, as was found on
Table 4.— Summary of the times of arrival and relative numbers for males and
females of northern fur seal rookeries and hauling grounds of St. Paul Island,
based on the current study and a review of the literature.
Age
Sex
Site1
State2
(yr)
Arrival time3
Abundance
Male
R
1
late Sept. to early Oct.
few
HG
2
mid- to late Aug.
2 yr > 1 yr
HG
3
late July
3 yr > 2 yr
HG
4
mid-July
—
HG
5
late June to early July
—
HG
6
late June
—
R
>7
late June
—
Female
R
NP
1
Oct. to early Nov.
few
HG,R
NP
2
mid- to late Sept.
2 yr > 1 yr
HG
NP
>3
mid-Aug.
3 yr > 2 yr
HG
P
>A
mid-Aug.
—
R
P
>4
mid-July
—
1R = rookery; HG = hauling grounds.
2NP = nonpregnant; P = pregnant.
3 Date when essentially all seals would have arrived.
390
BIGG: ARRIVAL OF NORTHERN FUR SEALS
the hauling grounds at this time (Figs. 4, 5). The rate
was probably biased downward by the fact that non-
pregnant females stayed on land for a slightly
shorter period of time than nursing females. Using
data given by Gentry and Holt (in press), nonnursing
females appeared to stay on shore for only about
64% as long as nursing females. Nonnursing females
make about half as many visits to land as nursing
females, but stay about one-third longer for each
visit.
A gradual increase in the nonpregnancy rate took
place on Polivina rookery during early to mid-July:
1 July - 0% (n = 280), 6 July = 2% (734), 11 July
= 1% (198), 16 July = 3% (148), and 21 July = 6%
(173). When weighted for the shorter period of stay
on land by nonpregnant females, the rates increased
from 0% by 1 July to 10% by 21 July. Presumably,
the increasing rate during July resulted from the
arrival of more nonpregnant females age >A.
Numbers of nonpregnant females began to increase
particularly by mid-July.
DISCUSSION
Northern fur seals arriving on St. Paul Island can
go first to rookeries located on beaches just above
high tide, or to hauling grounds more inland. The
typical arrival sequence (Jordan and Clark 1898;
Kenyon and Wilke 1953; Peterson 1965, 1968) is for
the bulls to establish territories for breeding on
rookeries in May-June. Pregnant females arrive
next on rookeries to pup, mate, and nurse in harems
within the territories. Subadult males arrive main-
ly during the pupping season and go to hauling
grounds rather than rookeries. Although young
males of different sizes (i.e., ages) tend to arrive in
successive waves with time, studies of marked seals
(Gentry et al. 1979) indicate that arrival times of in-
dividual subadult males can be quite variable be-
tween years. In early August, harem bulls abandon
their territories, and the social structure of the
rookery disintegrates. Nursing cows then tend to
disperse more widely on land, and nonterritorial
bulls and some subadult males move on rookeries
from hauling grounds. The mixing of seals between
rookeries and hauling grounds after July results in
less site distinction. The literature is unclear as to
the arrival times of subadult and nonpregnant adult
females after July, and whether these seals go first
to rookeries or to hauling grounds, or go to both
simultaneously. Age 2 females arrive later in the
season, and go to rookeries and hauling grounds,
while yearlings of both sexes arrive last, and go
mainly to rookeries. Seals begin leaving St. Paul
Island for the southern migration in October to
November (Roppel et al. 1965a; Kenyon and Wilke
1953). Few remain on the hauling grounds after mid-
October, and few on rookeries after early
November.
Table 4 summarizes the age-specific arrival times
and relative numbers of seals seen on rookeries and
hauling grounds, based on information given in the
Results. Two arrival times existed for pregnant
females, one by mid-July on rookeries and the other
by mid- August on hauling grounds. The second date
no doubt resulted from the movement of some post-
partum females from the rookeries to the hauling
grounds after the harems disintegrated. Thus, the
arrival time on St. Paul Island was by mid-July,
rather than mid-August.
The arrival times for nonpregnant females at >2>
yr on to St. Paul Island was less certain than for
pregnant females because age-specific data on ar-
rival times existed from hauling grounds up to mid-
August, but not from rookeries after mid-July. Also
it was not known whether nonpregnant females
went first to rookeries or to hauling grounds. The
main arrival time was probably by mid- August, a's
was found on hauling grounds. This was likely
because nonpregnant females began to increase in
numbers on rookeries in early to mid-July, and an
interval of 1-1 V2 mo was probably needed for essen-
tially all arrivals to be completed. Also, Abegglen
et al. (1956) felt that most females on the hauling
grounds during August came directly from the sea,
although some came from rookeries. From the cur-
rent study, some postpartum females go from
rookeries to hauling grounds. Perhaps most non-
pregnant females go first to the hauling grounds.
Nonpregnant females >3 yr arrived about 1 mo
later than pregnant females. According to R. Gen-
try (fn. 4), marked adult females on St. George
Island also arrived later when nonpregnant, al-
though only about 10 d later. The reason for the dif-
ferences in length of delay caused by nonpregnan-
cy found in the two studies is unclear at this time.
The answer may come when details of the study by
Gentry are reported, or perhaps when more is
known about movement patterns of adult females
between rookeries and hauling grounds.
The finding that nonpregnant females arrived
after pupping suggests nonpregnancy delayed the
date of mating. A delay in mating has been reported
previously for maturing females, but not for non-
pregnant cows. Because parous females pup about
1 d after arrival, and mate 5-6 d after pupping
(Peterson 1968; Gentry and Holt in press), essen-
tially all females that pup will have mated by mid-
391
FISHERY BULLETIN: VOL. 84, NO. 2
to late July. Assuming a similar interval between
arrival and mating for nonpregnant females, most
nonpregnant females would be mated by mid- to late
August. Jordan and Clark (1898) stated that young
females were impregnated in early August, after old
females, and Abegglen et al. (1958) observed that
females ages 3 and 4 bred after the harems dis-
banded. Also, Craig (1964) reported females
ovulated for the first time in late August or Septem-
ber. The only evidence that I could find of late
mating in a nonpregnant cow was by Osgood et al.
(1915), who observed a harem bull mating a female
that was "not very young" on 21 August.
A comparison of the age-specific arrival times for
each sex on St. Paul Island (Table 4) largely con-
firms the comments by Kenyon and Wilke (1953) and
Fiscus (1978) that arrival began progressively earlier
with increasing age. However, the current study in-
dicated that this phenomenon was obvious only for
young ages. It was seen in nonpregnant females
ages 1-3 and in males ages 1-6. Although no dif-
ferences in arrival times were shown for older males
and nonpregnant females, differences could exist,
but would be small. The differences in arrival times
became progressively less with age for males be-
tween 1 and 6 yr and apparently for females
between 1 and 3 yr.
A comparison of the relative numbers returning
to St. Paul Island (Table 4) suggests that progres-
sively more males and females returned between
ages 1 and 3. The cumulative effect of the kill on
males of 2 and 3 yr prevented comparisons of abun-
dance with males >4 yr. For females, the number
of 4-yr-olds returning was probably not greater than
3-yr-olds, as suggested by the similarity in the
number of 3- and 4-yr-olds killed on hauling grounds
by mid-August (Figs. 3, 4). However, pregnancies
complicate comparisons of abundance on hauling
grounds between females 3 yr and older. Between
ages 4 and 10, an increasing proportion of females
become pregnant (Lander 1981) and thus go to
rookeries rather than hauling grounds.
The data collected in this study suggest that, with
age, young seals of both sexes arrive progressively
earlier, and in progressively larger numbers. The
reason for these changes in arrival schedules lies in
an understanding of the mechanism that controls
the migration schedule. However, little is known
about this mechamism in the northern fur seal. The
mechanism, if it is like that of other vertebrates (see
Gauthreaux 1980; Baker 1978), is probably complex.
It could involve selective factors, such as food supply
and climate, and numerous environmental and
physiological factors, such as photoperiod, reproduc-
tive hormones, and endogenous rhythms. For north-
ern fur seals, learned and innate components are
likely to be involved. There are several examples of
where learning has been suggested to be involved
in migration. When the species leaves the Pribilof
Islands for the southern migration, juveniles tend
to disperse widely in the North Pacific Ocean, preg-
nant females tend to travel to the coastal waters off
California, and adult males generally remain in the
northern Gulf of Alaska (Baker et al. 1970; Fiscus
1978). Baker (1978) has suggested that the juvenile
northern fur seals may explore the habitat, and, with
age, eventually learn the best wintering areas. Also,
an increasing proportion of immature seals return
to their natal sites on Pribilof Islands with age (Ken-
yon and Wilke 1953), although sometimes the natal
site is abandoned and a new colony is established,
such as at San Miguel Island, CA (Peterson et al.
1968). Baker (1978) has proposed that site recog-
nition may be learned shortly after birth, and with
time, the site is usually relocated. However, other
components of migration may be innate. For exam-
ple, the annual timing of arrival for pregnant
females on St. Paul Island is remarkably precise.
Peterson (1968) calculated the mean arrival date to
be 30 June for each of 3 years. Such precision seems
unlikely to be the result of only learning. Keyes et
al. (1971) examined the pineal gland of this species
for seasonal variations in hydroxy-indole levels for
various ages of males and females, and postulated
photoperiodic regulation of the reproductive cycle.
A physiological event in the lives of young males
and females which coincides with the cessation of
arriving earlier and returning in greater numbers
is the attainment of sexual maturity. Baker (1978)
pointed out that sexual maturation controls the ini-
tiation of migration in many vertebrates. While a
few male northern fur seals begin to produce sperm
at 3 yr, most do not do so until about 5 yr (Kenyon
et al. 1954; Murphy 1969, 1970). The average female
conceives for the first time on her 5th birthday,
although typically ovulates for the first time on her
4th (Craig 1964; York 1983). Thus, it was during the
years of immaturity that young seals gradually syn-
chronized their arrival schedules with that of the
adults. Perhaps the gradual process of gonad
maturation in both sexes over several years plays
a role in inducing a cohort to migrate progressively
earlier in the year and in causing a greater propor-
tion to return to breeding sites.
A relationship between sexual maturity and
changes in arrival times on St. Paul Island could ex-
plain two other arrival phenomena noted in this
study. In the first case, considerable annual varia-
392
BIGG: ARRIVAL OF NORTHERN FUR SEALS
tion was noted in the seasonal pattern of arrival for
4-yr-old males, ranging from the typical pattern seen
in 3-yr-olds to that seen in 5-yr-olds. Such dif-
ferences in the arrival pattern may indicate that the
age at which males reach sexual maturity differs
between cohorts, a possibility worth further investi-
gation. Variations in the age at sexual maturity
could result from annual variations in body growth
rate caused in turn by fluctuations in food supply.
In the second case, pregnant females at >A yr may
have arrived slightly earlier with increasing age.
This would take place if the first conception resulted
in a later date of parturition than in subsequent
years. This is a possibility because, according to
Craig (1964), the first ovulation appears to be later
than subsequent ovulations. The age of primiparous
females spans mainly between 4 and 10 yr (York
1983), and thus the age at first ovulations presum-
ably also spans a similar number of years. Arrival
times would tend to be slightly earlier with age from
the increased proportion of mature females.
An alternate explanation for seals arriving in pro-
gressively larger numbers, may lie in the energetic
costs of the return migration from the North Pacific
Ocean to the Bering Sea. For yearlings, the
energetic costs may be too large for all but a few
individuals to return. With age, the relative costs
may be more favorable and permit an increased pro-
portion to return.
For each age, males tended to arrive before
females. This situation could result if, through selec-
tion or learning, the time of the return migration
was ultimately established for each sex by the adults.
The mechanism controlling the timing of migration
in young seals would gradually shift arrival times
with age to eventually synchronize with those of the
adults. However, because the arrival times of adult
males was earlier than that of cows, the arrival times
of immature males would also be before those of im-
mature females. The fact that nonpregnant adult
females arrived after parous females could be the
result of nonpregnant females gaining some advan-
tage in the energetic costs of migration. Since pre-
sumably competition exists for food around the
Pribilof Islands during the summer, perhaps survival
of nonpregnant adult females is enhanced by feed-
ing elsewhere, thus delaying the return migration
by 1 mo.
ACKNOWLEDGMENTS
I am grateful to P. Olesiuk for preparing the
Probit plots, and I. Fawcett for collating much of
the data on kills and pregnancy rates. I thank P.
Olesiuk, T. Quinn, and two journal reviewers for
useful comments on the manuscript.
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394
MODELING LIFE-STAGE-SPECIFIC INSTANTANEOUS
MORTALITY RATES, AN APPLICATION TO
NORTHERN ANCHOVY, ENGRAULIS MORDAX, EGGS AND LARVAE
Nancy C. H. Lo1
ABSTRACT
Life-stage-specific instantaneous mortality rates (IMRs) are often estimated individually for each life
stage of an organism using regression analysis. A single estimation procedure for all life stages may
be preferable because it would increase the overall precision of the IMRs and also provide a more realistic
mortality model. Two such procedures were developed in this paper. One is single-equation model where
regression estimates of all IMRs are obtained by fitting a single survivorship function to the entire data
set. The other is the maximum likelihood estimator. These models were compared using northern an-
chovy egg and larval data. The survivorship functions of each were, respectively, exponential and Pareto
functions.
The mortality of marine fish can be described by its
survival probability S(t) = P(T > t) - exp [- f
•Jo
X(u)du], where T is the age of the fish and X(t) is the
instantaneous mortality rate (IMR) at age t. Dur-
ing their early life history, pelagic marine fishes pass
through a series of life stages: eggs, yolk-sac lar-
val, feeding pelagic larval, juvenile and adult stages.
The IMR X(t) could be different for some life stages.
Therefore, for / life stages, there may be G distinc-
tive IMRs where G<I. The IMR X(t) is then a piece-
wise function (Gross and Clark 1975, p. 20-21;
Johnson and Kotz 1976, p. 272-273)
' kjit) 0 < t < ux
X2(t) ux < t < u2
and the survival probability S(t) = (P T>t) will be
m -
Kit)
ug-l <
t < un
MO UG-1 < t < UG
where ug is the maximum age of mortality stanza
g. Xg(t) # Xg(t) for g ± g. For example, Xx(t) may be
the IMR for egg and yolk-sac larval stages, even
though each is a different life stage, and X2(t) the
IMR for feeding larvae. As a result, the conditional
survival probability, Sg(t) = P (T > t\T > ug_x) cor-
responding to Xg(t), will also be different from Sg(t)
'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038.
Sl(ul)S2(t)
ux < t < u2
S(t) =
G-l
n Sd(ud)SG(t) Uq.^Kug
<f=l
The common method for estimating Xg(t)'s for
marine fishes has been to fit Sg(t) to sample age
data separately for each life stage or to assume one
common A(£) for all life stages and to fit one S(t) to
sample data of all life stages (Hewitt and Brewer
1983). For northern anchovy, Engraulis mordax,
eggs and larvae <20 d old, the IMR k(t) for eggs and
yolk-sac larvae is different from that of the feeding
larvae (Lo 1985):
m =
Xx(t) = a 0 < t < Mi
hit) = -f ^i < t < 20
6
(1)
Manuscript accepted August 1985.
FISHERY BULLETIN: VOL. 84, No. 2, 1986.
where ux is either the hatching time (th ~ 3 d) or
the age of yolk-sac larvae (tys ~ 4.5 d) with the first
feeding as the critical period after which mortality
decreased. Either th or tys has been used in various
models under different assumptions. If mor-
phological differences cause the changes in mortality
rates, th is a reasonable separation point between
395
FISHERY BULLETIN: VOL. 84, NO. 2
egg and larval stages. However, predation, the ma-
jor cause of mortality in the embryonic period, may
be similar for eggs and yolk-sac larvae (Hunter2).
If this is true, then the end of the yolk-sac stage is
a reasonable separation point for the mortality
stanza.
The conditional survival probability corresponding
to IMR in Equation (1) is
Stf) = e
— a- at
t < Ux
(2a)
and
S2(t) = l — \ u1< t< 20 (2b)
To assess Sg(t) for g = 1,2 in Equation (2), anchovy
egg and larval data were first divided into K age
groups. The mortality curves (Equation (3)) were fit-
ted to the sample mean counts (^) and mean age
E(yd =
0O SJfa xm t{ < ux
0„ SJt£ hit)] m, < tr < 20
(3)
where 0t is the expected number of fish at age t.
Using separate equations like Equation (3) is un-
satisfactory for some applications because separate
mortality curves may produce discontinuities at
transitions between mortality stanzas (or life
stages). The purpose of this paper is to obtain a
regression estimator and a maximum likelihood
estimator (MLE) of the IMRs (\{t)). The regression
estimator was based upon a single mortality curve
for all early life stages of anchovy, and the MLE
was based upon a truncated exponential (Equation
(2a)) and Pareto (Equation (2b)) likelihood function
of time to death (Lo 1985).
In section on Data, I describe the method of an-
chovy egg and larval data collection and standard-
ization procedures. The standardization procedures
are necessary because the gear and sample sizes
used to collect eggs differ from those used to col-
lect larvae. In section on Multi-Equation Model, the
current estimation procedures for constructing mor-
tality functions for different life stages are pre-
sented. In these procedures separate mortality func-
tions are fitted to the data set for each life stage.
In the next two sections, I develop two estimation
procedures for the IMRs of different life stages from
a single analysis: a single mortality function is con-
2 J. R. Hunter, Fishery Biologist, Southwest Fisheries Center La
Jolla Laboratory, National Marine Fisheries Service, NOAA, P.O.
Box 271, La Jolla, CA 92038, pers. commun. July 1983.
structed which is based on the IMRs of different life
stages, and the maximum likelihood estimators of
life-stage specific IMRs are described. The MLEs
of anchovy eggs and larvae (<20 d) are obtained. The
results and the comparisons of various models based
on anchovy egg and larval data are given in the last
two sections.
DATA
The standardized abundance of anchovy eggs and
larvae taken in routine biomass surveys was used
to elevate different estimation procedures for mor-
tality rates (Smith 1972; Parker 1980). The variables
used in the standardization procedures were extru-
sion through the net, avoidance of the net mouth,
and the variation of the water volume filtered per
unit depth (Zweifel and Smith 1981).
The northern anchovy spawning area lies off cen-
tral and southern California and Baja California. The
sampling area was divided into 23 regions covering
17.566 x 1011 m2 (Fig. 1). The central anchovy
stock is enclosed by 8 regions (4, 5, 7, 8, 9, 11, 13,
and 14) with a total of 5.703 x 1011 m2 (Duke3). In
this paper, I study the mortality of egg and larva
of central anchovy stock. Anchovy eggs and larvae
are sampled by net tows and each tow is a sampling
unit. Every year, m1 egg tows, vertical tows of
0.333 mm mesh with 25 cm diameter mouth open-
ing, and m2 larval tows using an oblique plankton
net of 0.505 mm mesh with 60 cm diameter mouth
opening are made. Ages were assigned to life stages
using stage specific growth curves (Methot and
Hewitt 19804; Lo 1983). The standardized number
of larvae in each group was divided by the time that
larvae remained at a particular length to yield the
sample mean daily larval production per unit area
(0.05 m2). A weighted mean per unit area for the
entire survey area (8 regions) was calculated: yi =
2. wr yir where wr was the weight for region r and
r
Z.wr = 1 (Table 1) (Lo 1985) and yir was the sam-
r
pie mean count for ith age group in region r. I con-
sidered only larvae smaller than 10 mm (20 d old)
because for anchovy larvae larger than 10 mm, the
3Duke, S. 1976. CalCOFI station and region specification.
Southwest Fish. Cent. Admin. Rep. No. LJ-76-3, 37 p. National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038.
4Methot, R. D., and R. P. Hewitt. 1980. A generalized growth
curve for young anchovy larvae; derivation and tubular example.
Southwest Fish. Cent. Admin. Rep. No. LJ-80-17. National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038.
396
LO: MORTALITY RATES OF NORTHERN ANCHOVY
135°
~1
35'
30'
25°
20c
15°
NORTHERN CALIFORNIA
1 INSHORE
2 NEARSHORE
3 OFFSHORE
CFNTRA1 CALIFORNIA
4 INSHORE
5 NEARSHORE
6 OFFSHORE
SOUTHERN CALIFORNIA
7 INSHORE
8 NEARSHORE
9 OFFSHORE
IO EXTENDED
BAJA CALIFORNIA
11 INSHORE
1 2 BAY
13 NEARSHORE
14 OFFSHORE
15 EXTENDED
SOUTH BAJA
16 INSHORE
17 NEARSHORE
18 OFFSHORE
19 EXTENDED
CAPE
20 INSHORE
21 NEARSHORE
22 OFFSHORE
23 EXTENDED
35°
30°
120°
115°
1 10c
Figure 1.— Sampling area for estimating mortality of northern anchovy eggs and larvae (<20 d) with sampling sta-
tions denoted by the open circles, and regions denoted by numbers.
397
FISHERY BULLETIN: VOL. 84, NO. 2
Table 1.— Group data of anchovy eggs and larvae: Sample mean daily production (yt) at age f,, days for regression esti-
mators and sample mean daily death (n,) for maximum likelihood estimators (MLEs) of egg and larval mortality.
1980
1981
Regression estimators
' t, y,
1 0.41666 1.57
MLE
Regression estimators
' ', Vi
MLE
Vi
0.91666 1.21
3
4
5
6
7
8
9
10
11
12
1.41666
1.91666
2.41666
3.05
5.6
9.06
11.40
13.98
16.00
18.63
1.07
0.64
0.88
0.74
0.37
0.21
0.16
0.10
0.086
0.012
1 0.41666 1.57
0.91666 1.21 0.36
1.41666 1.07 0.14
1 0.41666 1.33
0.91666 2.00
1 0.6666 1 .665
1 .6666
4
5
6
7
8
9
10
11
2.1666
3.05
5.6
9.06
11.40
13.98
16.00
18.63
0.76 0.31
0.74 0.02
0.31
0.21
0.16
0.10
0.086
0.072
0.37
0.16
0.05
0.06
0.014
0.014
3
4
5
6
7
8
9
10
11
12
13 18.56
1.41666
1.91666
2.41666
22.91666
3.10
5.98
9.45
11.97
14.37
16.53
1.19
1.47
1.11
0.60
1.23
0.44
0.25
0.16
0.10
0.10
2.41666 1.11
5
6
7
8
9
3.008
5.98
9.45
11.97
14.37
16.53
0.44
0.25
0.16
0.10
0.10
0.08 10 18.56
n,
1.33 0.335
0.22
0.915 0.195
0.475
0.19
0.09
0.06
0
0.08 0.02
1982
1983
Req
ression estimators
t, Vi
MLE
Rec
i
iression estimators
h v,
MLE
/
/
h
y,
"/
/
*,
Vi
"/
1
0.41666
0.84
1
0.6666
1.21
1
0.41666
1.78
1
0.41666
1.78
2
0.91666
1.57
2
0.91666
1.02
2
1.1666
1.67
0.11
3
1.41666
0.76
2
1 .6666
0.93
0.28
3
1.41666
2.31
4
1.91666
1.10
4
1.91666
0.99
3
1.91666
0.99
0.68
5
2.41666
0.61
3
3.42
0.64
0.29
5
2.41666
0.92
4
2.41666
0.92
0.07
6
4.42
0.67
6
3.82
0.68
5
3.82
0.68
0.24
7
8.00
0.23
4
8.00
0.23
0.41
7
7.03
0.16
6
7.03
0.16
0.52
8
11.07
0.14
5
11.07
0.14
0.09
8
9.97
0.11
7
9.97
0.11
0.05
9
13.62
0.08
6
13.62
0.08
0.06
9
12.34
0.08
8
12.34
0.08
0.03
10
15.74
0.06
7
15.74
0.06
0.02
10
14.60
0.05
9
14.60
0.05
0.03
11
18.13
0.05
8
18.13
0.05
0.01
11
16.73
0.0405
10
16.73
0.0405
0.01
12
18.88
0.0375
11
18.88
0.0375
0.003
Vi-,
2Used in MLE only.
avoidance of the net becomes a serious bias.
legion
nm2 x 10 s
n2 x 10~10
wr
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
0.054
13
21
7.122
0.125
14
29
9.866
0.174
Total
167
57.031
1.00
The sample mean daily production of eggs and lar-
vae per 0.05 m2 (^) with its age (^) constituted the
data base for regression estimates of IMRs of eggs
and larvae in MEM and SEM. Mean daily produc-
tion represent eggs for 0.17 d (4 h) < t{ < 3d, and
larvae for 3 d < t{ < 20 d; i = 1, . . .K, where K is
the total number of age groups. The sample age
structure (y^ tj) reflects that of a single cohort
under the assumption of steady production over the
survey period (Seber 1980). The same data set was
also used to generate the sample mean number of
eggs or larvae lost per day between two adjacent
age groups (n^ = yi_1 - y%). The statistics n/s were
used directly in the MLE. Normally, sample totals
were used instead of sample means in MLE. I used
n/s because anchovy eggs and larvae were sampled
with different nets and because the number of egg
tows was different from that of larvae.
MULTI-EQUATION MODEL (MEM)
In the current estimation procedures, separate
mortality curves are constructed (Equation (3)) for
398
LO: MORTALITY RATES OF NORTHERN ANCHOVY
the IMRs (X(t)) of anchovy eggs and larvae. If the
life-stage-specific IMR is the main objective, the
MEM is an easy method for obtaining the estimates
of IMRs. The mortality curves (Equation (3)) are
nonlinear functions of age (t). The IMRs can be
estimated by either nonlinear regression (NR) or
linear regression (LR) after the data set (yi7 t$ is
transformed. The NR is based upon the assumption
that the errors are additive. The observed mean
daily production (y^ relates to the conditional sur-
vival probability as
Vi = % Sife; h(t)] + «ii
= y0e-at, + eu
k < Mi
(4a)
Vi = K siik; hit)] + e2l
Vu,\
+ e2l
ux < ti < 20 (4b)
where % = th ~ 3 d old. Nonlinear regression
estimation procedures provided by standard statis-
tical packages such as BMDP statistical software
(Dixon et al. 1983) are then used to estimate the
parameters of IMRs, i.e., a and /?.
The LR assumes that the errors are multiplicative.
The observed daily production (y{) relates to the
conditional survival probability in the form of
Vi = eu , SJU; Ut)) egi for g = 1,2.
i-i
The logarithm of both sides of the equation yields
two linear functions
ln(&) = A - ati + £u
t
k < Wi
(5a)
Info) = B - /Jin -t + E2i Ul<U< 20. (5b)
u
Equation (5a) is then fitted to data set (lnfo)> k f°r
k < ux), and Equation (5b) is fitted to data set
(Info), \n(klux) for ux < k < 20 d) to estimate a and
SINGLE-EQUATION MODEL (SEM)
The SEM consolidates all the conditional survival
probabilities (Sg(t)) from each mortality stanza into
a single equation. It not only eliminates discontin-
uities at transitions between life stages, but also im-
proves the precision of overall mortality estimates
because of the large sample size Moreover, the SEM
makes it possible to estimate the IMR for life stages
where data are scarce.
Based upon Equation (2), S(k) of anchovy eggs
and larvae is
m =
or
S(k) =
Sife) k < u,
S^u^iti) Ui < ^ < 20
s^tdSM k < ux
Sx(ux)S2(k) ux<k< 20
where Sx(ux) = P (T > ux\T > 0) = e~M\ S2(ux) =
P(T> ux\T > ux) = 1, and ux = tys = 4.5 d. Thus
by creating two new independent variables xxi and
x2i such that
Xli -
and
x2i -
k k < ux
ux ux < ti < 20
ux k < ux
k % < t{ < 20
it follows that S(k) = Sx(xxi)S2(x2i) and the mortal-
ity curve can be written as
E(yd = e^x(xXl)S2(x2l) = e,e-°*i>
<x
2i
-p
u.
(6)
The data set for fitting Equation (6) looks like
age group
age
(i)
(ti)
Yi
xii
x2i
1
h
Vi
h
ux
2
h
Vi
k
ux
i
k
Vi
ux
k
k
k
Vk
ux
k
ux = 4.5 d
In order to use Equation (6) to estimate the IMRs
of eggs and larvae in Equation (1), a combined data
399
FISHERY BULLETIN: VOL. 84, NO. 2
set (2/1; xlit x2i), which includes all the data from
each life stage and the maximum ages of mortality
stanzas (ug's), is important to ensure the accuracy
of the estimates of the IMRs. The determination of
u's depends primarily on the changes of the mor-
tality rates, which may be related to the changes in
morphology or behavior that affects mortality rates.
In the best fit of the SEM, however, the end points
of morphological patterns may not correspond to the
maximum ages. Three life stages were identified for
anchovy eggs and larvae, with the end point of mor-
tality stanza 1 being the average age of yolk-sac lar-
vae («! = 4.5 d). In the MEM, the hatching time (th)
was used, but, the best fit of the SEM occurred when
ux = 4.5 d. Two mortality stanzas were assigned to
three life stages of anchovy (<20 d) because from
the existing data, no evidence for a change in the
IMRs within a life stage existed although the data
may not have been adequate to detect such changes.
The regression estimates of the IMRs for the SEM
can be obtained by either NR or LR as described in
the previous section. If NR is used, Equation (6) is
fitted to the data set Qjit xlif and x2i) directly to
obtain estimates of parameters of X^t) and X2(t).
Because the variance of egg data is larger than that
of larvae, a weighted NR (WNR) would be prefer-
able If errors are assumed to be multiplicative,
taking the logarithm of both sides of the Equation (6)
yields
\n(yt) = A - axu - pin
' x2i
+ &.
(7)
The data set (ln(2/i)> Xj*, and \n(x2ilu{}) is then used
to estimate a and (1 through linear least squares
regression.
MAXIMUM LIKELIHOOD ESTIMATOR
(MLE)
The MLE is presented here as an alternative
method of estimating IMRs. Because the data used
for mortality estimators are grouped by age, I fol-
lowed the procedures described by Kulldorff (1961)
and McDonald and Ransom (1979) for grouped data.
Here, N{ = Y{_x - Y{ (number of deaths between
ages ti_i and t£ of a single cohort are multinomial
variables, each with probability
Pi = Sfo-i) - SiU).
L{N%,Pt{z');i = 1, ...,/) ex n p&y,
1=1
(8)
where z is the parameter vector in X(t). The
derivatives of the logarithm of likelihood function
with respect to the parameters z's are set equal to
zero. Solutions to the simultaneous equations
31nL
dZs
= 0
are MLEs of z, if certain conditions are satisfied
(Kulldorff 1961). In marine fish only the IMRs of
a few life stages are considered because of the lack
of data. It is then necessary to compute the condi-
tional probability
Px = %1<r<ii|TGDJ
= [S&_i) - S(tJ\/P(T 6 D)
where D is the domain of ages of life stages con-
sidered.
Because I considered only the IMRs of anchovy
eggs and larvae of ages >4 h (0.17 d) and <20 d, the
conditional probabilities are computed from a
truncated exponential and Pareto survival proba-
bility (Equation (2)) (Gross and Clark 1975, p.
128-132):
P% = P(ti_1<T< ti\ *i<r<20)
= (S(«,_i) - SitiWWd - S(20))
e-<-i _ e~ot'
e~at^ - e~
'20 \-"
u.
Pi =
Vi
Mi
g-ati _ e~aux
(9)
ux < t{ < 20.
The likelihood function of N{'s for the whole life
cycle (i = 1, ...,/, and Yj = 0) is
Then the likelihood function of iV/s for anchovy
eggs and larvae of ages <20 d is
400
LO: MORTALITY RATES OF NORTHERN ANCHOVY
l « n p^ =
i = 2
k
n (SKAc-i) - £W
i = 2
S(«i) - 5(20)
k
I TV,
i-2
and
ln(L)= I [JVi ln(P,)] = I [JV,- ln(P?)] + I [Nt ln(Pt)]
i = 2
i = 2
i = c + l
(10)
where A/", = m(yi_1 - yt) = ra-r^ and c is max(i) for ^ < 3 d (u^. Substituting Equation
(9) for P, in Equation (10) yields
ln(L) = 1 ty ln(e-"f.-i - e~at) + S Nl{-au1 + p In Mj) + ty ln(^ - ^-P)
1 NAn
i = 2
g-<"l _ g-«™,
'20W
Mi
(11)
Solving simultaneous equations = 0 and for a and /? gives their
MLEs.
da
8<
The asymptotic variance-co variance (ASVAR-COV) of MLEs of a and ft was computed
according to Kulldorff (1961, p. 86-87):
As var(a)
As cov(a,(i) As var(/J)
= (UN)
3,P
a
li
3-21 a22
= (UN) As3
s,P
1
T paMnP,
i o 2
N
4 „88lnP, 4 p^lnP;
t^2 * 3a3/J tl i a/32
«,p
(12)
For detailed derivation of the MLEs, see the Appendix.
Conceptually, abundance declines monotonically with increasing age, but this may not
occur in the sample. Although its absence does not complicate regression analysis, cor-
rections are required when the MLEs are used. The MLEs are functions of sample totals
fy = (Hi-i - y~i)m, Ni > 0, and can also be expressed as function of sample proportions
NJN (Equations (Al) and (A2)), which are equal to the ratios of differences of sam-
ple mean daily productions (^_j - y^K^i - Vk)-n^n (see Appendix). The quantity n^ =
NJm is the sample mean daily death between two adjacent groups. The MLEs require
N{ > 0. Due to sampling error, it is possible to observe more individuals in the older
group than the adjacent younger group, i.e., yi_x < y{. If so, some adjacent groups
401
FISHERY BULLETIN: VOL. 84, NO. 2
(i/i, ti) have to be combined so that y{ > y{- for t{
< tf. The ratio n{ln can be used in place ofNJN to
compute the MLEs. This correction is inappropriate
if the reason for y{ > y{; for t{ < t? is that in-
dividuals were evicted from the sampling area or
immigrated into it, as such movements violate the
assumption of a stationary population.
Although %s are sufficient for computing point
estimates of the MLE, the total number of deaths
between ages tx and tk (N = m(yl - yk) is required
for computation of the ASVAR-COV of the
MLEs. N can then be used to determine minimum
number of tows (mx) for the youngest stage
through m1yl = N for a given precision of the
MLE. Although the sample size for eggs may dif-
fer from that of larvae, an equal number of sample
sizes is assumed to compute the ASVAR-COV. The
minimum number of egg tows can be determined
by m, = Nlyv
RESULTS
Both the MEM and the SEM were fitted to the
basic data (yi7 t(, 0.17 d < t{ < 20 d) collected from
1980 to 1983, using NR and LR (Table 1, Fig. 2).
The point estimates and their asymptotic standard
errors are listed in Table 2 and Figure 3. NR and
LR produced similar estimates of the IMRs for the
MEM. When the SEM was applied to the combined
egg and larval data, the WNR was also used to com-
pute the IMRs in addition to NR and LR because
of the inequality of the variances among life stages.
The variance of egg counts was higher than that of
larvae because eggs were more patchily distributed
than larvae. Because of this, the inverse of the
variances of sample means of eggs and larvae was
used as the weights for the WNR. The estimates
from the WNR were similar to those from LR and
the standard errors from both methods were lower
than those from NR.
The WNR estimates of egg IMRs from the SEM
were more precise than estimates from the MEM,
whereas the most precise estimates of larval IMRs
were provided by the MEM using NR. The SEM was
more precise than the MEM for eggs but not for the
larvae, because the variance of eggs was larger than
that of larvae. Thus, when eggs and larvae were
combined in an SEM, the variance around the single
equation was smaller for the eggs and larger for the
larvae. Nevertheless, the SEM produced larval
IMRs with reasonable precision when the WNR was
used. Therefore, the SEM WNR is suitable for ap-
UNWEIGHTED SEM
2.0 r
1983
10 15 20 25 0 5
AGE IN DAYS
10 15 20 25
10 15 20 25
Figure 2.— Observed daily anchovy egg and larval production/0.05 mz (O = eggs, • = larvae), and the mortality curves from the MEM
(two short curves) and the SEM (one single curve) using unweighted and weighted nonlinear regression for 1980-83 field collected data.
402
LO: MORTALITY RATES OF NORTHERN ANCHOVY
Table 2.— Estimates from multi-equation model (MEM), single-equation model
(SEM), and maximum likelihood estimator (MLE) for anchovy egg and larval mor-
tality {a and /?), and their standard error (SE) based upon 1980-83 field data where
K is number of age groups and m is number of tows used in each model. For both
MEM and SEM, nonlinear regression (NR), linear regression (LR) and weighted
nonlinear regression (WNR) estimates are given.
Egg mortality
Larval mortality
a
SE
Km
P
SE
Km
1980
MEM
NR
0.39
0.103
5(961)
1.22
0.0314
7(199)
LR
0.35
0.13
1.32
0.06
SEM
NR
0.32
0.05
12(1,160)
1.06
0.41
12(1,160)
WNR
0.25
0.02
1.33
0.06
LR
0.24
0.05
1.36
0.13
MLE
0.36
0.012
11(961)
1.28
0.09
11(961)
0.016
(500)
0.12
(500)
0.02
(300)
0.16
(300)
0.03
(199)
0.27
(199)
1981
MEM
NR
0.13
0.16
5(1,134)
1.53
0.032
7(403)
LR
0.13
0.15
1.54
0.06
SEM
NR
0.13
0.07
12(1,537)
2.19
0.96
12(1,537)
WNR
0.33
0.06
1.70
0.18
LR
0.20
0.05
1.64
0.15
MLE
0.24
0.008
10(1,134)
0.96
0.06
10(961)
0.01
(500)
0.08
(500)
0.02
(300)
0.11
(300)
0.01
(403)
0.10
(403)
1982
MEM
NR
0.17
0.26
5(992)
1.81
0.036
6(96)
LR
0.19
0.24
1.87
0.065
SEM
NR
0.14
0.10
11(1,088)
1.77
1.46
11(1,088)
WNR
0.13
0.04
1.83
0.36
LR
0.12
0.07
1.85
0.20
MLE
0.24
0.008
8(992)
1.20
0.08
8(992)
0.01
(500)
0.11
(500)
0.015
(300)
0.14
(300)
0.03
(100)
0.25
(100)
1983
MEM
NR
0.23
0.29
5(850)
2.05
0.11
7(78)
LR
0.27
0.25
1.80
0.10
SEM
NR
0.26
0.19
12(928)
2.45
2.71
12(928)
WNR
0.30
0.05
2.23
0.28
LR
0.33
0.08
1.84
0.22
MLE
0.32
0.007
11(850)
2.48
0.10
11(850)
0.01
(500)
0.14
(500)
0.013
(300)
0.18
(300)
0.02
(80)
0.35
(80)
plications where it is preferable to estimate IMRs
for egg and larvae simultaneously (e.g., simulation
studies of mortality at all life stages). The SEM is
preferable for modeling the mortality curves
through all life stages because it eliminates the
multiple estimates that occur at the endpoint of each
life stage (Fig. 2). In addition, the SEM allows
estimation of the IMRs for all life stages even when
data for some life stages are inadequate for indepen-
dent estimation of a life-stage-specific IMR. In com-
paring NR and LR, the estimates of IMRs from
these two procedures were similar, despite the dif-
ferent assumptions about the error term. One com-
plication of using LR is that the abundance for any
403
FISHERY BULLETIN: VOL. 84, NO. 2
0.5
0.4
>
~ 0.3
o
S 0.2 -
en
o>
Ui
0.1 h
0.0
1979
0.5 r
2. 0.4 H
1980
x MEM-NR
• MEM-LR
o SEM-NR
A SEM-WNR
A SEM-LR
+ MLE
1981
1982
1983
1983
^ 3.0
oa
c 2.5
^ 20
O
o
> 1.5
r i.o
o
« 0.5
(0
0.0
x MEM-NR
• MEM-LR
o SEM-NR
A SEM-WNR
▲ SEM-LR
+ MLE
1980
1981
1982
1983
1983
Figure 3.— Estimated anchovy egg mortality (a), larval mortality coefficient (/3), and their standard error (SE) using multi-equation
model (MEM), single-equation model (SEM), and maximum likelihood estimator (MLE) for 1980-83.
specific age needs to be transformed back to the
original unit. Direct inverse transformation may
bias the estimates. Thus, the LR may not be ap-
propriate for biomass estimation or other applica-
tions where a transformation back to original units
is required.
In addition to the above regression models, the
MLEs of egg and larval IMRs were also computed
based on the data set n{ = y^\ - yit i = 1, . . .k
(Equations (Al) and (A2), Table 1). The ASCOV-
VAR for anchovy egg and larval mortality rates re-
quires the total number of eggs and larvae that died
between ages 4 h and 20 d from the sample (N). It
is not possible to obtain N directly from my^ (i.e.
N = myx) because eggs and larvae are sampled
with different nets and in different regions. Anchovy
eggs have a more concentrated and patchy distri-
bution than larvae which are less numerous and
distributed more uniformly throughout the entire
survey area because of the diffusion of larvae after
hatching (Hewitt 1982). Zero density of eggs was
assumed for the offshore regions where eggs were
not sampled to compute the weighted average egg
production y% = Z. wr yir. I then divided m^ by
r
the proportion of area sampled (q = Z. wr where
wr's are summed over the regions where egg tows
were taken) to obtain sample daily death N in [tlt
tk). Thus, N = mtfjjq; q ranges from 0.53 to 0.82
for 1980-83. Four sets of sample sizes were con-
sidered: m = m1, 500, 300, m2 where mx is the ac-
tual number of egg tows and m2, actual number of
larval tows (Table 2). For any given N, one obtains
the ASVAR-COV of a and p by dividing a{j by N
where a^'s are the elements in matrix A of Equa-
tion (12).
The MLE point estimates a and /?, were between
the estimates yielded by the SEM and the MEM in
most cases. The precision of the MLE for egg IMR
was higher than that of the regression estimates.
The standard error of the MLE of the larval IMR
was between those of the MEM and SEM regres-
sion estimates (Table 2, Fig. 3).
404
LO: MORTALITY RATES OF NORTHERN ANCHOVY
DISCUSSION
All the estimates of instantaneous mortality rates
(IMR) discussed in this paper were computed from
age (stage) frequency data. To ensure the unbiased-
ness of the estimates, three assumptions have to be
met: a stationary population, reliable growth curves,
and accurate samplers. Any violation of these
assumptions will cause biases in the mortality
estimates. Nets usually do not retain fish of all sizes
because some small fish extrude through the net and
some large fish avoid the net. Thus the estimates
of size-specific retention rates are essential correc-
tion factors for the catch. If fish migrate at a signifi-
cant rate, either the migration rate should be
estimated or the sampling area should be expanded
to eliminate migration problems, for migration
violates the assumption of a stationary population
and thus biases the mortality. Because growth
curves are normally used to assign age to stage of
eggs and larvae, biased growth curves would lead
to inaccurate age assignments which definitely
would bias the mortality estimates.
Although modeling the mortality rates of the early
life stages of anchovy is the focus of this paper, I
have shown that the SEM (Fig. 2) can be applied
to any continuous process whose parameters are life-
stage specific and generally estimated separately.
For example, many allometric relations such as the
growth curves may have different instantaneous
growth rates for different life stages. A single con-
tinuous growth curve for the whole life cycle is possi-
ble using the SEM which allows greater latitude of
modeling life-stage-specific growth rates than
modeling the instantaneous growth rate for the
whole life cycle as proposed by Schnute (1981). How-
ever, the SEM does require knowledge of the forms
of instantaneous rates and the endpoint of each mor-
tality stanza (or life stage).
In this study, the determination of a cutoff point
between life stages was based upon examination of
the empirical data and biological implications. It is
conceivable to include the cutoff point (%) as one
of the parameters in both SEM and MLE (Matthews
and Farewell 1982). The cutoff point can then be
estimated directly through the models. Matthews
and Farewell considered the exponential mortality
curve with one cutoff point and obtained MLE of
the cutoff point (change point). For anchovy egg and
larvae, the cuttoff point for the eggs and larvae up
to 20 d old was easily determined from the IMR and
age data (Lo 1985). Estimation of the cutoff point
through SEM or MLE would be laborious and any
improvement may be minimal. However, the
estimates through the models would eliminate the
problem of whether ux should be hatching time or
the age of yolk-sac larvae.
Comparison of these two regression models with
the MLEs based on anchovy egg and larval data in-
dicated that the point estimates of the IMRs were
similar. The SEM using WNR provided the most
precise egg IMR which was nearly the same as the
MLE. The MEM, using NR, provided the most
precise estimates of larval IMR's. The regression
estimators of the IMR's are easier to compute than
the MLEs, yet they require larger sample sizes than
the MLEs. If money is not a constraint, the SEM
is preferred to the MLE. Otherwise, the MLE
should be used. Based upon 1980 anchovy egg and
larval data, 300 tows for eggs and larvae each (a
total of 600 tows) could guarantee MLEs of a and
(i with cv = 0.10. The current sampling design (egg
tows ~ 1,000) seems to use an excessive number of
egg tows for the MLEs of egg and larval IMRs. If
the larval IMR is the only parameter to be
estimated, the MEM is recommended.
ACKNOWLEDGMENTS
I thank J. Hunter of Southwest Fisheries Center,
National Marine Fisheries Service, and C. J. Park
of San Diego State University for valuable discus-
sions through the writing of the manuscript, the
referee for constructive comments, and Mary Ragan
and Larraine Prescott for typing the manuscript.
LITERATURE CITED
Dixon, W. J., M. B. Brown, L. Engleman, J. W. Frane, M. A.
Hill, R. J. Jennrich, and J. D. Toporek.
1983. BMDP statistical software. Univ. Calif. Press,
Berkeley.
Gross, A. J., and V. A. Clark.
1975. Survival distributions: reliability applications in the
biomedical sciences. John Wiley and Sons, N.Y., 331
P-
Hewitt, R. P.
1982. Spatial pattern and survival of anchovy larvae: implica-
tions of adult reproductive strategy. Ph.D. Thesis, Univ.
California, San Diego, 207 p.
Hewitt, R. P., and G. D. Brewer.
1983. Nearshore production of young anchovy. CalCOFI
(Calif. Coop. Oceanic Fish. Invest.), Rep. 24, 235-244.
Johnson, N. L., and S. Kotz.
1976. Distributions in statistics: continuous univariate
distributions - 2. John Wiley and Sons, N.Y., 306 p.
KULLDORFF, G.
1961. Contributions to the theory of estimation from grouped
and partially grouped samples. John Wiley & Sons, Inc.,
N.Y., 144 p.
Lo, N. C. H.
1983. Re-estimation of three parameters associated with an-
405
FISHERY BULLETIN: VOL. 84, NO. 2
chovy egg and larval abundance: Temperature dependent
hatching time, yolk-sac growth rate and egg and larval reten-
tion in mesh nets. U.S. Dep. Commer., NOAA NMFS
SWFC-31, 33 p.
1985. Egg production of the central stock of northern an-
chovy 1951-83. Fish. Bull., U.S. 83:137-150.
Matthews, D. E., and V. T. Farewell.
1982. On testing for a constant hazard against a change-point
alternative. Biometrics 38:463-468.
McDonald, J. B., and M. R. Ransom.
1979. Alternative parameter estimators based upon grouped
data. Commun. Stat.-Theory, Method A8(9)899-917.
Parker, K.
1980. A direct method for estimating northern anchovy,
Engraulis mordax, spawning biomass. Fish. Bull., U.S.
78:541-544.
Schnute, J.
1981. A versatile growth model with statistically stable
parameters. Can. J. Fish. Aquat. Sci. 38:1128-1140.
Seber, G. A. F.
1980. Some recent advances in the estimation of animal abun-
dance. Tech. Rep. WSG 80-1, 101 p.
Smith, P. E.
1972. The increase in spawning biomass of northern anchovy,
Engraulis mordax. Fish. Bull., U.S. 80:849-974.
ZWEIFEL, J. R., AND P. E. SMITH.
1981. Estimates of abundance and mortality of larval an-
chovies (1951-75). Rapp. P.-v. Reun Cons. int. Explor. Mer.
178:248-259.
APPENDIX
The two partial deviations of In L (Equation (11)) are
a InL
N
-N I
da i=2 N
-U-i- k«-aLi
1 - e
-oA.
Ni
% Z -z + tx - (% - h)
I— I -
= 0 (Al)
d InL
dp
-N I
N
i=c+i N
In ux +
\-j~\ ln li
1 -
/ u W
k-i
- In
'201
Wi
i— r
= 0 (A2)
where A^ = t{ - ti_1 and ux ~ 3.
Both Equations (Al) and (A2) depend on the proportion NJN rather than the absolute counts (iV/s). In
order to have a unique solution of a and (1, it is necessary to have
a2 In L „ - , 32 InL ^
— n o < 0 and — nn9 < 0.
da2 dft2
Moreover, the conditions
(A3)
and
hm — > 0, hm — < 0
o — o da o— oo da
.. d InL .. d InL
hm — — — > 0, hm — — -— < 0
is— o dp p~oo dp
(A4)
guarantee a positive solution of a and p. Equation (A3) leads to the following constraints
406
1 <
g^-t,) |20r _ ±
| — I
.2 JV 1- e-^i-^-i)
(A5)
and
1 <
I — I
/ u \-p
In
'20^
MT
W
e°(ui-fi)
i=c+i N
ti-it
In
ti
t-
i-l
Mi
«
i-l,
(A6)
After algebraic manipulation, it was easy to see that Equation (A4) was true for this truncated exponential
and the Pareto MLE. We used an iterative procedure to select the MLE of a and /J, which satisfies not
only Equation (A3) but also the constraints of Equations (A5) and (A6).
The partial derivations in each entry of matrix A (Equation (12)) are
'201"
32lnP,
da2
e«(«i-*i)
-5— - e**i + (Ml _ tf-
u.
e.<.,-.,. g ' . i
32 In ^
dp2
In
'201
Wi
201"
Ui
e"(»i-(i)
g-d^-y j^j'3 _ i
and
d2\nP, V J v\uJ \ux
dadp
e-dH-t,) I?0-]" _ i
407
METHODOLOGICAL PROBLEMS IN
SAMPLING COMMERCIAL ROCKFISH LANDINGS
A. R. Sen1
ABSTRACT
The present sample survey plan, for the estimation of age and species composition of California rockfish
landings, which is stratified two-stage with port-month group as a stratum, poses serious operational
problems in data collection. A revised plan is suggested which is workable. Formulas have been developed
for estimating total catch and its error by species-sex-age groups; optimum sampling and subsampling
fractions have been obtained for a given cost function and the precision of the estimator is compared
with two other estimators. The method developed has been extended to cover situations other than rockfish.
The paper also deals with double-sampling for specified cost for the estimation of age composition
of a species, which is important to predict the status of a stock in future years, the inherent problems
in data collection in commercial fisheries, and the measurement errors involved in the survey.
Estimates of the total catch (in terms of number)
by species-sex-age and by area of landing and dur-
ing a given time for commercial rockfish caught in
California north of point Arguello are currently
based on a probability sample of landings. The com-
mercially important species of rockfish taken by
California's fishery with mixed species are widow
rockfish, Sebastes entomelas; bocaccio, Sebastes
paucispinis; and chilipepper, Sebastes goodei.
A study was undertaken during 1983 under agree-
ment between the present author, the Humboldt
State University Foundation, and the Tiburon
Laboratory of the National Marine Fisheries Ser-
vice, NOAA, to determine if the present sampling
plan for the estimation of species and age-composi-
tion of California rockfish landings is workable. The
study revealed that the current plan is not opera-
tionally feasible. A revised plan is proposed which
is workable and would provide efficient estimates
of the parameters based on existing catch data
within the usual limitations of budget and person-
nel and under the assumptions made in the plan.
Formulas have been developed for the ratio
estimators of mean and total catch and their errors.
Optimum sampling and subsampling fractions have
been obtained for a given cost function and the preci-
sion of the estimator is compared with two other
estimators.
For most theoretical population work and for
management purposes, the knowledge of the age
'Department of Mathematics and Statistics, Queen's University,
Kingston, Ontario, Canada K7L 3N6; present address: 67 Ranch-
Ridge Way N.W., Calgary, Alberta, Canada T3G 1Z8.
composition is important to predict the status of the
stock in future years. Fridricksson (1934) developed
the age-length key method for determing age com-
position from a large number of length measure-
ments. Fridricksson's approach was improved by
Ketchen (1950) who provided more accurate results
for age groups at the extremities of the distribution.
Kutkuhn (1963) mentioned the limitations of the age-
length key approach except in situations where price
differentials may demand sorting of landings by size
criterion. Westrheim and Ricker (1978) pointed out
that the age-length key approach will almost always
give biased estimates. Clark (1981) and more recent-
ly Bartoo and Parker (1983) dealt with methods for
control or elimination of bias. Following the method
of Tanaka (1953) in which stratification occurs after
subsampling for age, Kutkuhn (1963) estimated
absolute age composition of California salmon land-
ings by port-month groups. He showed that the sam-
pling procedure is not effective unless the age sam-
ple is at least five times costlier than the length
sample.
Mackett (1963) found double sampling more effi-
cient than simple random sampling with fixed sam-
pling costs for estimating relative age composition
of Pacific albacore landings.
Southward (1976) found that a sample of otoliths
proportional to the length frequency of sampled fish
from each port was preferable to fixed sample size
procedure for estimating age composition of Pacific
halibut. Kimura (1977) arrived at the same conclu-
sion as Southward by following a somewhat dif-
ferent approach.
We will present some of the important considera-
Manuscript accepted August 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
409
MSttfcKX JBULL^IIJN: VUL. 84, INU. Z
tions in sampling for estimating age composition of
rockfish landings based on recent widow rockfish
data from the California coast. Finally, we will
describe some of the measurement errors, which
would normally occur in simple random sample of
individual fish and which are taken care of in cluster
sampling adopted in our approach.
The sampling plan arrived at may produce usable
results under the assumptions stated, though some
of the assumptions have been under attack during
recent years.
DESIGN OF THE SURVEY
Rockfish are being landed at 14 points on the
California coast. Of these, three cater only to com-
mercial fishing, four to sport fishing, and seven to
both sport and commercial fishing. The 10 commer-
cial ports are grouped into 6 port groups with a sam-
pler (six in all) assigned to each of the 6 ports—
Eureka, Fort Bragg, Bodega Bay, San Francisco,
Monterey, and Morro Bay.
The commercial trawlers make trips varying in
length from 1 to 8 d. These vessels maintain log
books to keep records of area fished and appropriate
catch for each tow. Sampling by tow is generally not
feasible because it is not possible for the sampler
to be on board during haul time. For the same
reasons no estimates of fish being rejected and
returned to the sea are obtained because this would
involve collection of discarded fish from randomly
selected tows within sampled trips.
Selection Procedure
A two-stage stratified random sampling plan was
adopted with port-month group as a stratum and
boat trips within a stratum as first-stage sampling
units. Fish are sorted at sea into market categories.
The first stage sampling units are poststratified into
categories and at least one cluster of a given weight
is subsampled within each sort-type from a first-
stage sampling unit. Categories are based upon
species composition, size, and quality, but in other
contexts they could be strictly size or species
categories. Cluster (box) of 25 lb is taken when
sampling small fish, or any time small rockfish are
landed such that there would be more than 20 fish
in the 50-lb cluster. In all other cases 50-lb standard
cluster size is selected. A cluster is next separated
by number of each species and its weight, which are
recorded along with sex, total length, and otolith
of each member of a species in the cluster.
The instructions are to "sample all market
categories (sorts) from a boat, and from as many
boats as possible and select:
"(i) 1 cluster per 20,000 lb of widow rockfish
landed by each boat, up to 4 clusters,
"(ii) 1 cluster for all other species, if less than
5,000 lb landed, and
"(iii) 2 clusters for all species if more than 5,000
lb are landed.
"The second cluster should not be taken if this
precludes sampling another boat."
Estimation with Poststratification of
Sample Trips by Categories
Consider the problem of estimation of total catch
of a given species for a port-month stratum. Equa-
tions for estimation of other characteristics for
fisheries with mixed species are straightforward and
can be obtained by substituting the value of the
characteristic for the catch of the species. Totals
across strata are formed by simple additon.
Notation
For a given species, let
N = total number of trips,
n = number of randomly sampled trips,
W = total weight of fish caught from all trips,
W{ = weight of fish caught on trip i,
Wy = weight of fish for sort j caught in trip
i,
my = number of clusters sampled from sort j on
trip i,
mi = number of clusters sampled on trip i,
m = number of clusters sampled over n trips,
Wi = Z. Wy where L{ is the number of sorts
3 in trip i,
yv-k = number of fish of the species in cluster k
from sort j of trip i,
Yy- = total number of the species caught from
sort j of trip i,
Y = total number of species caught from all
trips,
Y = mean catch per cluster for the species,
yv- = 2. yyklrriy = unbiased estimate of Yv-,
wijk = weight of the A;th cluster from the jt\\ sort
of the ith trip,
Wi
Mi = -5=-^ where w,- = 2. 2. Wi^lZ. m^ =
w{ j k l3k j y
410
dEjri. osxmr LiLlvkj ov^iuiYiii*n.v^in.u r 1011 um^iyiiiuo
average weight of sampled clusters
in the ith trip.
If Wx is a constant, its estimate w will be given by
w = 2 X 5! wilkIZ. 2. mvj. In practice, N and Mt
i j k J i j J
will not be known and will be estimated by N =
wW - - W
= WIW; M{ = -zr respectively, if Wl is a
" w
constant = w (say).
Ratio Estimates of Mean and Total
The ratio estimate of mean catch (Y) per cluster
is
n n
I mm I wt
y,
YP =
(1)
I Mi I Wi
where yx = 1 M^-/Z My = I W^/I ^
California Fish and Game. The reasons for failure
to collect the data are discussed in the section on
Collection of Representative Data-Measurement Er-
rors. The above estimators are, however, recom-
mended for use in situations where the problem does
not exist and, in particular, for single species where
the categories are based on size. The estimates of
error are given in Equations (4) and (5).
Estimation Ignoring Category
Variation Within Sampled Trips
Assume that a cluster is selected at random from
all possible clusters in a sampled trip. In other
words, we ignore categories altogether both in sam-
ple selection as well as in estimation. Valid ratio
estimates Y^ of Y and Y^ of Y are respectively
given by
Y,„ =
1 Wi
LR
I Wi
Vi „ w =
W
(3)
The ratio estimate of total catch Y is
W -
Y« - i Y°-
(2)
The above estimators recommended for use are not
workable in rockfish sampling because the sampler
failed in almost all cases to subsample from more
than one category in a sampled trip as would be seen
from a sample of basic data for 1982 (Table 1)
available for Eureka from the Department of
Table 1 .—Distribution of landing weights (lb) from all categories
and from the sampled category for Eureka for 1982.
Number of
Weight of
Weight of all
clusters
Market
all fish
fish for the
Sample no.
sampled
category
(IV,-) in a
category in
(boat trip)
(m,)
sampled1
given trip
a given trip
1528
1
269
26,550
24,176
1529
1
250
4,133
445
1530
2
269
59,218
58,239
1531
1
269
20,511
15,987
1533
1
269
35,022
14,661
1534
1
269
20,757
20,705
1535
1
269
15,812
8,436
1536
1
250
1,975
1,010
1537
1
250
16,055
1,075
1541
3
269
65,837
65,837
'Shows the code number of categories which are based on species, size,
and quality.
Note: In all cases, only one of the categories could be sampled from a given
trip. In boat 1541 there was only one category (269) of fish.
Note these equations are essentially the same as
Equations (1) and (2) except that we now assume
that a cluster is randomly selected from all possible
clusters in a sampled trip where W{ is the total
landing weight from all categories for the ith boat
trip in the sample (W = X W{). In practice, the
X
sampler would tend to subsample from a category
which is accessible and is preponderant. This may
lead to some bias in the estimate though its contribu-
tion to the total error will be negligible, since this
would occur at the second stage of sampling.
The estimates of variance of estimated total and
mean are approximately given by
HYW) =
JL (1 . /l)8f + MLzJ^i
n nm
v(Ym) ± (^)2 v{Ym)
(4)
(5)
where s2h = Z.
K\2®i- Ym)2.
W
n - 1
n —
m
i n
w,
2 „2
s2i
m,-
(6)
411
nSHfcKY BULLETIN: VUL. 84, NU. Z
and si = Z (ylk - ^/(m, - 1); W = I W^n;
/! - Z W,IW;f2 =
W,-
w
(7)
We will consider an operationally feasible plan in
which sample trips at a port during a month are
poststratified into categories and clusters are sub-
sampled from each category; where one or more
categories are missed due to inadequate field staff
and/or management problems, clusters should be
selected from other boat trips containing the missed
categories.
Assuming that the cluster weight of the unequal
cluster size varies over trips, i.e., w^ = Z Z wijlc/
J k
Z m„ estimates of mean and total are
j 3
n n
£ Z wA Z wA
(8)
Z Wilwt Z Wi
where Rt = -=?- ; viY^) and viY^) can be obtained
similar to Equations (4) and (5).
Yj =
Vj
5
W
v(Y3R) =
Z
3
+
17?
y W^
(11)
j <k W* v^'
and
v(Y3R) ± v(Y3) + 2 Z Z cov(fy, f,). (13)
Both v(^) and v(F3^) are of standard forms and can
be obtained as in Equation (4). Similarly, v(Y3) and
v(YSR) can be obtained. The covariance terms in
Equations (12) and (13) are ignored when the sub-
samples from different categories are from different
boat trips and are, therefore, independent. In rock-
fish sampling this was found true, because the sam-
pler failed in almost all cases to subsample from
more than one category. In general, for all fish
where sampling from more than one category per
boat trip is feasible, e.g., with few species-size-
qualities, Equation (13) should be used.
Assume that the clusters vary in size over trips.
For any sort (say j )
Yk-
Z w13r13iL wi3
WJ = RJWJ (14)
Estimation Based on
Categories as Domains of Study
This method is almost as precise as proportional
stratified sampling if within each port-month
stratum (a) a minimum of four landings or boat trips
(n3 > 4) is selected for each category and (b) the
landing weights are available by categories after the
season to serve as weights at the estimation stage.
The minimum number in (a) is mainly based on
limitations of field staff and budget restrictions. The
ratio estimates of mean catch per cluster, total
catch, and their errors, assuming clusters of equal
size and using categories as domains of study are
given by
Y3R = Z W^y/Z Wfi Y3R = Z Yj (9)
where y3 = Z W^lJ. Wl} (10)
and
y,
= Z wdtdl. WJw.
ir"iy-r xy^i)
where iL = !*; A = Z iL-WyZ Wu.
y w..' J y lJ i lJ
(15)
(16)
If yij is small compared to N3 and if the same sub-
sampling strategy is applied to each of the sample
landings, we have, ignoring contribution due to
second-stage sampling units,
Vjffij) =
nj(nj ~ 1)
W
(R^ - R3)2. (17)
Another estimator v2(R3) is the jackknife
v&lj) = ■ - Z (Ri3- - R3f (18)
thi
412
SEN: SAMPLING COMMERCIAL FISH LANDINGS
where R ,
+ 72 W
and i?
l^y + ... + W{l_1)rlj + W(l+l)Ki + ... + W%i
(19)
i-^z*;,
Thus i? y is obtained by omitting trip i from the
sample for sort j and calculating &.■ instead of Rrj
as in Equation (16).
Hence, for category j of a species
or
v(y3.) = w^o^
(20)
where vx(Rj) and v2(-R/) are given by Equations (17)
and (18).
For estimate of total over all sort groups for a
species
ya„ = I y,
AR
(21)
v(?4*) = I i;(iy + 2 1 1 cov(fv fy (22)
A simpler formula viY^) = Z. v(Y„) can be used
'j '
where subsamples from different categories are
from different boat trips and are, therefore, in-
dependent.
It is, however, more reasonable to assume that the
frequency distribution of fish caught is more uniform
within a category so that cluster weight would be
approximately a constant within a category. If so,
the estimates of mean and total are given by
Y5R = I W&lL Wfi Y5R = I Y} (23)
J 3 3
where y3 = X W^fL WtJ;
Y3 =
^W^ WJ
1 W,
(24)
Wa
and Wj is the simple mean weight of clusters in the
jth group. Where the assumption of constant cluster
weight within a category is not valid, the more
general results given in Equations (14) and (15)
should be used.
Comparison of Methods:
Ignoring Category Variation Versus
Poststratification by Categories
We will compare the efficiency of the estimators
(3), ignoring variation due to categories, with the
estimators (9), based on poststratification of land-
ings by categories at a port during a month. The
analyses were based on Eureka and Monterey data
for 1982. The coefficients of variation (c.v.) of mean
catch per cluster for a species based on categories
as domains of study (method 2) were in almost all
cases lower (Table 2) than ignoring category varia-
tion (method 1). Since method 1 results in under-
estimation of c.v.'s because sampling is actually
based on a stratified random sample instead of a
simple random sample, the increased precision of
method 2 is all the more striking.
The c.v. of the estimated mean catch by sex-age
groups for a species for which the number of sam-
ple landings were MO (Table 3) were in all cases less
for method 2 than for method 1. It may, however,
be pointed out the c.v.'s are likely to be affected by
factors such as growth, maximum age, and max-
imum size of fish. These have not been considered
in this study. Thus, estimates based on categories
as domains of study proved more efficient than
ignoring categories altogether. Besides, method 2
has the added advantage of providing estimates by
Table 2.— Coefficient of variation (c.v., in percent) of mean catch
by species at Eureka and Monterey based on the two methods
during 1982.
Location
and
species
Sample size
(number of
boat trips
sampled)
c.v.
(0/0)
Method 11
Method 22
Eureka
Widow rockfish
Chilipepper
Bocaccio
Monterey
Widow rockfish
Chilipepper
Bocaccio
88
88
88
54
54
54
11.48
30.83
26.01
18.31
15.68
12.57
7.33
32.12
24.40
6.62
13.92
10.32
1Method 1, based on random categories (i.e., ignoring stratification by
categories).
2Method 2, based on categories as domains of study.
413
FISHERY BULLETIN: VOL. 84, NO. 2
Table 3.— Coefficient of variation (c.v., in percent) of mean catch by species-sex-age1
group at Eureka and Monterey based on the two methods during 1982.
Eureka
Monterey
Number
of boat
Sex
Age
(yr)
c.v.
(%)
Number
of boat
trips
sampled
Sex
Age
(yr)
c.v.
(%)
trips
sampled
Method
1
Method
2
Method
1
Method
2
17
18
11
11
15
19
M
F
F
F
M
F
7
7
13
12
6
6
19.71
13.50
39.98
34.77
30.10
35.87
Widow rockfish
18.83 10
10.94 10
Chilipepper
24.89 24
31.21 21
Bocaccio
19.82 14
32.45 20
F
F
F
F
M
F
13
12
9
7
7
7
39.98
35.16
18.48
22.09
27.46
24.34
24.29
20.49
7.63
9.81
12.45
10.06
1Age-sex groups for which primary sampling units (landings) are >10.
market categories which is of considerable economic
importance.
COST FUNCTION
The components cx and c2 were estimated at
Consider the cost function
C = cxn + c2nm
(25)
where cx is the average cost (in minutes) per boat
trip due to transport, contact, and delay in making
a contact, c2 the average cost in data collection
(identification of species, sex, length, otoliths, etc.)
per cluster within clusters per boat trip and C is the
total cost involved in visiting the primary sampling
units (boat trips) and collecting data from the n boats
with an average of m clusters per boat sampled.
Data collected at Tiburon by the California Depart-
ment of Fish and Game and the National Marine
Fisheries Service show that c = 111.80 min, c2 =
58.3 mm so that — = 2 apply. However, from more
C2
recent studies conducted — = 3.
c2
Activity
Transport
Contact
Delay (off loading, etc.)
Data collection
Species1
Sex, length
Otolith
Preparation time
Percent
50.0
5.0
13.0
68.0
Percent
7.7
5.8
10.8
7.7
32.0
Mean (in minutes)
81.7
8.7
21.4
111.8
Mean (in minutes)
14.0
10.6
19.7
14.0
58.3
Excluding samples dominated by single species.
Minimizing Equation (4) subject to Equation (25)
for the optimum allocation we have
™opt =
(26)
Table 4. — Optimum values of m for estimating species catch per cluster by categories
for different variance and cost ratios, 1978.
Species
Category1
n
si
s2
m
clc - ^as
C1'C2 - 2
cjc2 = 3
Eureka
Bocaccio
250
25
1.80
3.01
2.16
3.86
4.73
Chilipepper
250
13
24.45
3.13
1.92
0.52
0.64
Widow rockfish
250
11
59.49
8.71
2.46
0.56
0.68
Monterey
Bocaccio
253
31
95.15
4.20
1.97
0.63
0.77
Chilipepper
253
33
43.71
4.16
1.94
0.45
0.55
Widow rockfish
253
12
22.38
4.66
2.00
0.68
0.84
'Code numbers of categories which are based on size, species and quality.
414
SEN: SAMPLING COMMERCIAL FISH LANDINGS
The variation among clusters (sf) in different land-
ings at Eureka and Monterey for 1978 was in almost
all cases greater than between clusters within the
same landings (Table 4); also the optimum number
of clusters per boat for estimating species number
was mostly unity. Data from other ports follow the
same pattern. Since a minimum of two clusters is
needed to provide an estimate of between cluster
within trip variation, a subsample of two clusters
per category per trip is recommended. In practice,
it is preferable to select a systematic sample of
clusters separated in time.
VARIANCE COMPONENTS:
SPECIES-AGE AND LENGTH GROUPS
A two-level nested analysis of variance for length
and age with unequal sample size for species based
on sample landings at ports during 1979 (Table 5)
shows that both the variation, because of length and
age, was generally high among sample landings
compared with clusters within landings. Also, varia-
tion between clusters was generally of the same
order as within clusters, and the optimum number
of clusters was <2. Data for other ports and years
(not shown in the table) mostly supported the
findings.
On the whole, both the variation in species number
(Table 4) as well as in length and age (Table 5) was
consistently high among sample landings relative to
between clusters within landings; also, variation
among clusters was not significant compared with
variation within clusters. Hence, for precise estima-
tion of species number, length, and age„composition
for a category at a port during a season, data should
be collected from a large number of landings and
from few clusters (two) from a category within a
sample landing.
RELATIVE EFFICIENCY OF ESTIMATORS
USING POSTSTRATIFICATION
Consider the three estimators of total catch for
a sort of a species at a port during a year. We will
use the same selection procedure with poststratifica-
tion by sorts but different estimation procedures.
Y, =
7I»
nj i=1
Vij
(27)
^ W&q Wj
Yj
i w*
W:
Yk = RjWj
(28)
(29)
where Rj is given by Equation (16), y{j is the simple
mean of species number per cluster for sort j from
the ith sample, Yj is the same as Equation (24) with
a constant cluster weight within a sort group, and
Yj is a more general estimator based on the
assumption that cluster weight varies among trips.
For v(Yj) use W2jv2{R]) where v2(Rj) is the jack-
Table 5.— Two-level nested ANOVA of length and age of
pie sizes by ports during 1979. MS = mean square; F
observed probablity level.
species with unequal sam-
= F-RATIO, Statistic; P =
Age
Length
Source
df
MS
F
P
df
MS
F
P
Widow rockfish at Eureka
Samples
15
34.45
4.75
<0.005
37.86
3.09
<0.025
Clusters
(within
samples)
13
7.25
1.19
0.35
12.27
1.43
~0.18
Within
clusters
320
6.09
8.58
Chilipepper at Monterey
Samples
43
31.74
4.05
<0.001
48
145.20
4.02
<0.001
Clusters
39
7.84
1.80
~0.001
44
36.10
1.43
~0.035
Within
clusters
320
4.35
971
25.25
Bocaccio at San Francisco
Samples
10
84.97
6.95
<0.001
10
317.88
6.98
<0.001
Clusters
15
12.23
1.20
~0.30
16
45.55
0.80
~0.75
Within
clusters
225
10.20
227
57.11
415
FISHERY BULLETIN: VOL. 84, NO. 2
knife estimator of Equation (18) and for v(Y.) see
Sukhatme (1954). Yj is generally subject to
considerable bias.
The c.v. of total catch of bocaccio, chilipepper, and
widow rockfish for different categories by port-year
groups (Table 6) show that the estimators Yj and
Yj are highly efficient compared with Yj', also, Yj
turns out to be slightly superior to Yj since the
jackknife estimator v2(Yj ) is an underestimate and
does not take into account the contribution of the
within component of variance. Thus, the empirical
evidence supports strongly the use of the estimator
Yr
Table 6.— Coefficient of variation (in percent) of estimates of total
catch of bocaccio, chilipepper, and widow rockfish per cluster by
ports during 1978 and for different categories for the three
estimators 9\, Yh and V", .
Port
Number
of boat
trips
Category sampled
*7
%
\
Bocaccio
San Francisco
Fort Bragg
Monterey
Eureka
253
250
253
250
20
86
31
25
Chilipepper
13.51
16.21
12.07
40.11
10.24
7.36
17.93
26.00
11.64
8.14
19.51
29.84
Eureka
250
13
Widow rockfish
37.66
34.52
42.33
Monterey
Eureka
250
250
12
11
111.20
72.69
43.47
27.81
68.29
33.90
AGE-COMPOSITION: DOUBLE
SAMPLING
Studies mentioned in the Introduction section
have shown that since aging from otoliths of each
individual fish in a sample is more expensive than
an easily measured quantity such as length, it may
pay 1) to choose a random subsample from the whole
sample of length measurements for age determina-
tion or 2) stratify the sample according to length
classes and choose a subsample from each class for
age determination. The technique is profitable only
if the correlation between length and age is fairly
high.
It may be recalled that considerable bias is in-
troduced by applying age-length keys developed dur-
ing a year to subsequent years. Both Kimura (1977)
and Westrheim and Ricker (1978) showed that age-
length keys can yield most inefficient estimates of
numbers-at-age with substantial overlap of lengths
between ages. In the latter case the correlation be-
tween length and age will be low for the larger and
the very small sizes. Consequently, we will need a
higher sampling intensity at the tails to provide
reliable estimates of age for such sizes.
In the construction of length strata for selection
of the subsample, additional questions arise on 1)
number of strata to choose, 2) strata boundaries to
decide, and 3) the number of sampling units to be
allocated to each stratum for deriving maximum
gain from double sampling. These are discussed as
follows.
Number of Strata
The values of V(yst)/V(y) (Cochran 1977) are
given below as a function of L, the number of strata
using the linear model
y = a + fix + £
(30)
where y is the length, x the age of female widow
rockfish and
ViVst)
V(y)
L2
+ (1 - p2)
(31)
where P is the correlation between length and age
in the unstratified sample and L the number of
strata. It can be shown for this model that when L
> 6 and p > 0.95, there is hardly any gain due to
stratification (Table 7). The improvement in
stratification is highest for data set 1 for which p2
= 0.7004 and lowest for set 3 for which P2 =
0.5278. The results for the regression model indicate
that unless p exceedes 0.95, little reduction in
variance is to be expected beyond L = 6. Data sets
1, 2, and 3 support this conclusion. In fact, there
does not seem to be any profit resulting from in-
crease in strata beyond L = 5.
Strata Boundaries
For the length-age strata on 239 females (widow
rockfish) landed during 1982 at San Francisco and
the rule based on the cumulative of \Jf{y) (Cochran
1977) where y denotes the length in centimeters, the
nearest available points for the two strata are
Stratum
Boundaries
36-47 cm
48-55 cm
Intervals on
cum \fi
18.70
23.72
416
SEN: SAMPLING COMMERCIAL FISH LANDINGS
Table 7.— V(yst)IV(y) as a function of L for the linear regression and for some actual
data.
Linear regression
nodel p =
Data set
L
0.99
0.95
0.90
0.85
1
2
3
2
0.265
0.323
0.392
0.458
0.4747
0.5114
0.6041
3
0.129
0.198
0.280
0.358
0.3774
0.4209
0.5308
4
0.081
0.154
0.241
0.323
0.3434
0.3892
0.5052
5
0.059
0.134
0.222
0.306
0.3276
0.3746
0.4933
6
0.047
0.123
0.212
0.298
0.3154
0.3740
0.4890
oo
0.020
0.098
0.190
0.277
Type of data
X
Age
y
Length
Set
Data
(yr)
(cm)
Source
1
Female widow rockfish (532)
1982
1982
Department
Monterey, San Fi
ancisco
(Jan. -Mar.
) (Jan.-Mar.)
of
and Bodega Bay
California
Fish
2
Female widow rockfish (444)
1981
1981
and
Eureka
(Jan. -Sept.) (Jan. -Sept.)
Game
and
3
Female widow rockfish (328)
1980
1980
Tiburon
Eureka
(Apr.-Dec.) (Apr.-Dec.)
Laboratory
It turns out that the division point is approximate-
ly the same for young as well as old widow rockfish.
For length-age data (1981) based on 444 females
(widow rockfish) landed at Eureka, the boundaries
using 2 and 3 strata are
Stratum
Boundaries
Intervals on
cum y£
1
31.5-47 cm
17.70
46.5-55 cm
29.01
Stratum
1
2
3
oundaries
31.5-46 cm
46.5-49 cm
49.5-55 cm
itervals on
cum \/f
17.70
13.12
15.89
Optimum Allocation Plan
Double sampling with regression is more efficient
than single sampling (when the first sample is
measured for age alone) for the same cost if
p2>
44
c
1 +
(32)
where P is the correlation between length and age
of fish, c and c are respectively the costs of aging
and measuring a fish. Assuming that the average
cost of aging a rockfish (including small and large
fish) is 6 min and of measuring it is 1.2 min
(estimates based on measurements by W. Lenarz of
Tiburon Laboratory), we have from Equation
(32)
or
p2 > 0.5555
p > 0.7453.
For the three data sets (Table 7) the values of p2
are respectively 0.7004, 0.6515, and 0.5278 so that
Equation (32) is approximately satisfied. However,
neither p nor — - are large enough to suggest that
double sampling will be much more efficient than
single sampling.
We will illustrate the use of double sampling for
stratification by analyzing 1981 length-age data at
Eureka to estimate the proportion of female in age
group 11, based on a sample of 444 fish. For the
three length strata, h = 1, 2, 3 with stratum bound-
aries based quadratic fit of length on age are 31.5-43,
43.5-49, 49.5-55. (Note this is different than bound-
aries based on length only.) Also
417
FISHERY BULLETIN: VOL. 84, NO. 2
= 1.2 min, Cj =
w1 =
Si =
3.8 min, c2 = 3.8 min, and c3 = 8 min
0.0653, w2 = 0.5451, and w3 = 0.3896
0.1825, s2 = 0.4966, s3 = 0.1503,
and s = 0.4343
where wlf w2, and w3 are the proportions of fish in
the sample, c0 is the cost of measuring a fish and
c1( c2, c3 are respectively the costs of aging them in
the three length groups. From Cochran (1977, p.
331) we have
(Pst) =
J_
C*
I whshy/ch + (S2 - Z whsl)m\f&
(33)
= 0.8915/C*
where pst is the estimated proportion and C* =
E(c) = £"(c0 n + Z. chnh) with nj = 14, n2 = 120,
n3 = 48 and ri = 444. The efficiency of double
sampling with respect to single sampling is given
by
Vsr,(p)IVmm(Pst) = 1-21
where vsrs(p) = 0.1885/-^-, i.e., double sampling
is 27% more efficient than single sampling. How-
ever, as noted by Ricker (1975) the increase in ac-
curacy achieved by combining a length sample with
a smaller age sample may not be great unless fish
used for age determination is taken from the same
stock, during the same season and using gear having
the same selective properties as the length-fre-
quency samples. This point will generally be met if
fish are subsampled systematically for age from fish
arranged in increasing (or decreasing) order of
length from a port-month stratum. Our studies have
shown that the best length-age fit does not change
significantly if age determination is made on every
other fish arranged in ascending order of length.
It is difficult to obtain reliable estimates of the
numbers at age for the extremely small or larger
sizes because lengths cannot be used for estimating
age. There is need for search for other auxiliary
variables (other than length) associated with age and
for increase in sampling rate at the tails. In double
sampling where lengths are obtained in the first
phase, a number of small clusters may be used
separated in space and time to provide a large
number of fish at the tails for estimating numbers
at age. The extent of bias in estimation of numbers
at age through length-age key approach may be
tested by Monte Carlo simulation.
COLLECTION OF REPRESENTATIVE
DATA-MEASUREMENT ERRORS
Owing to uncertainty of arrival times and vary-
ing unloading procedures, no objective method is
available to ensure random sampling of the trips.
When the vessels return to port, they are usually
available for sampling except when they are tran-
shipped immediately due to inclement weather, lack
of processing facilities, uncooperative buyers, or
unscheduled deliveries at short notice. It is, how-
ever, not unreasonable to regard a set of sample
landings during a week at a port as random and
representative of the totality of all landings at the
port for the month.
Although rockfish are landed by categories, which
are mostly determined by market agreement based
on size, composition, and condition of the catch, the
number of categories per delivery cannot be pre-
determined. This number would vary from delivery
to delivery and from dealer to dealer. Also, there
are no guarantees that a complete boat sample,
covering clusters from each category, can be taken
on any sampling day and some of the categories are
actually missed in sampling. Some of the possible
reasons for missing the categories are 1) when
landing weight would not occur during regular
hours, one of the sorts may have already been
shipped before the sample could arrive at the spot;
2) often one of the sorts may be quite small and there
may be a buyer at the dock waiting for the fish to
be taken away; 3) while the sampler is working on
a sort, the other sort(s) will have either been pro-
cessed or shipped away; and 4) the sampler may
418
SEN: SAMPLING COMMERCIAL FISH LANDINGS
be prevented from taking a sample from another
sort by the skipper who may not like some of his
fish being cut and otoliths removed for biological
studies. This may happen at ports where either pro-
cessing facilities are inadequate or fish are bought
by local merchants immediately after landing. The
question arises if failure to sample from all cat-
egories of a sample landing as originally planned
would cause appreciable bias and loss in efficiency
in the estimates of species catch and its distribution
and whether a more efficient method could be
developed that is operationally feasible. This point
has been examined in the present paper.
The present technique of selecting a cluster (box)
of fish as second stage sampling unit is preferred
to random selection of a specified number of in-
dividual fish because in practice the potential of per-
sonal bias of the sampler could be considerable.
Often fish chosen by the latter technique are ones
closest to the sampler or those that fell in a certain
position. Tomlinson (1971) felt that in this approach
the sampler may tend to choose a fish with certain
qualities and thus may introduce procedural bias.
The selection of a representative cluster would de-
pend whether samples after sorting on the vessel
come from bins, strap boxes, or off conveyor belts.
Buyers from small markets occasionally select fish
from the top of bins. Hence, to avoid this bias, it
is preferable to select the cluster from the conveyor
belt which exposes unsorted fish from the lower por-
tion of the bin. However, where small market buyers
do not buy fish, a cluster may be selected from a
bin. Where many bins are present a systematic sam-
ple of two clusters, preferably from the beginning
and end of the trip may be selected. Where fish are
graded on a conveyor belt before they enter the
plant (e.g., Fieldslanding at Eureka) the sampler
should try to intercept the landings prior to sec-
ondary sorting or obtain separate weights for each
subsort category. In general, selection of a cluster
for a market category should be done before any
presorting is done at the port.
It has been pointed out earlier that bias may result
from personal selection of fish within a cluster. If
the sampler were to select a number of clusters with
few fish per cluster, a cluster will on the average
contain more big fish. This would lead to high non-
sampling bias. Sometimes, the top few fish in a bin
are selected and put there to impress small buyers.
The resulting bias in selection can be avoided by
taking all the fish in a cluster (e.g., 50 lb) from one
side of the box.
For obtaining reliable and comprehensive infor-
mation on population characteristics, it is essential
for the sampler to maintain good relationships with
both the skipper and the buyer; this will depend to
a large extent on the expertise of the sampler gained
in the course of the field work.
SUMMARY
1. The sampling scheme at a port during a month
with poststratification of sampled trips into
categories and subsampling of clusters from
each category (see sections on Estimation with
poststratification and Estimation ignoring
category variation) is not workable for esti-
mating rockfish catch since some of the
categories may be missed in sampling due to in-
adequate field staff and/or management
problems.
2. For other commercial fish where the above
problem does not exist and landing weights by
categories are not available at the end of the
season, the methods (see sections on Estima-
tion with poststratification and Estimation ig-
noring category variation) are recommended,
e.g., for single species where the categories are
based on size.
3. For estimating the catch of rockfish, a two-
stage sampling plan is recommended with boat
trips as first stage units poststratified into
categories and clusters subsampled from a
category; estimates are based on categories as
domains of study with landing weights available
for each category. A minimum of four landings
or boat trips should be used for each category,
to provide efficient estimates. With few categ-
ories, this number is likely to be large.
Where only one category is subsampled for
each boat in the sample, v(Y3R) = ^ V(YX In
3
all other cases Equation (13) should be used.
4. The design described in the above paragraph is
recommended for use in other fisheries where
landing weights are available for each category.
Equations (9) and (21) are recommended for the
estimation of catch according as the clusters are
of equal or unequal size. Equations have been
provided for the more practical case when
cluster weight can be treated as constant with-
in a category but different among catego-
ries.
5. Estimates of species catch by sex and age based
on method 1 are less efficient than those based
on method 2 which is based on categories as do-
mains of study (Tables 2, 3).
6. Method 2 is preferred to method 1 when there
419
FISHERY BULLETIN: VOL. 84, NO. 2
is variation among categories. This is true for
all fish.
7. With few categories (species-size-qualities) the
chance of missing a category is reduced. Equa-
tions (9) and (13) should be used for clusters of
equal size and Equations (21) and (22) for un-
equal size clusters. This result is, of course, ap-
plicable to all commercial fish.
8. As far as practicable, selection of a cluster for
a market category should be done before any
presorting is done at the port either from bins,
strap boxes, or off conveyor belts.
9. Variation (within categories) in length and age
for a species was considerably higher among
boat trips than among clusters within boat trips.
Also, variation among clusters was not signifi-
cant, compared with variation within clusters
(Table 5). Hence, for precise estimation of
species number, length, and age composition for
a category at a port during a season data should
be collected from a large number of landings
and from few clusters from a category within
a sample landing. This result should hold for all
commercial fish.
10. For the cost function C = cxn + c2nm where
Cj is the average cost (in minutes) per boat trip
due to transport, contact, and delay in making
a contact, c2 the average cost of data collection
(identification of species, sex, length, otoliths,
etc.) per cluster per boat trip and C is the total
cost involved in visiting the primary sampling
units (boat trips) and collecting data, the opti-
mum number of clusters per sampled trip for
a fixed cost for a category is two (Table 4). This
should provide valid estimates of error as re-
quired in Equations (13) and (22).
11. The principal contribution of the paper is that
a minimum of four sample landings be sub-
sampled for each category from a port-month
stratum, i.e., about 1 per week and two clusters
of 50 lb (25 lb for small fish) each should be
sampled to provide port-year estimates with a
reasonable degree of accuracy.
If a category is infrequently landed, sampling
should be directed towards the infrequent
category, as long as the number of landings for
the category is less than four per month.
12. The efficiency of the ratio estimator (Equation
(28)) based on poststratification by categories
at port-year level and using constant cluster
weight within a category was compared with
two other estimators, including the ratio esti-
mator based on jackknife. Empirical evidence
indicated that the ratio estimator using constant
cluster weight within a category proved most
efficient for estimation of species catch.
13. Age-length keys can yield most inefficient
estimates of the numbers at age for extremely
small and large fish. It is suggested that cluster
sampling for length be based on a number of
clusters separated in space and time; also, sam-
pling for age should be intensified for small and
large fish. This approach is applicable to all
fish.
14. Double-sampling was adopted for estimating
proportion of widow rockfish in 11-yr age group.
A sample of fish was divided into 3 strata and
optimum allocation for age was adopted within
strata. The estimated proportion was 27% more
efficient than if single sampling were adopted.
The best length-age did not change significantly
if age determination is made on every other fish
selected in ascending order of length.
The method is general and is applicable to all fish.
ACKNOWLEDGMENTS
Thanks are due to William Lenarz of Tiburon
Laboratory for providing information on problems
related to widow rockfish landings on the Califor-
nian coast, to Candis Cooperider and Mark Allen for
the computations done on data collected, to the field
staff of the California Department of Fish and Game
responsible for collection of relevant data, and to
Norman Abramson, Director, Tiburon Laboratory
for all the assistance rendered to me during my work
in the Laboratory. My thanks are also due to Pat
Dalgetty, Department of Mathematics and
Statistics, University of Calgary, for assistance in
typing the paper and finally to the referees for
helpful comments.
LITERATURE CITED
Bartoo, N. W., and K. R. Parker.
1983. Stochastic age-frequency estimation using the von Ber-
talanffy growth equation. Fish. Bull, U.S. 81:91-96.
Clark, W. G.
1981. Restricted least-squares estimates of age composition
from length composition. Can. J. Fish. Aquat. Sci. 38:
297-307.
Cochran, W. G.
1977. Sampling techniques. 3d ed. Wiley and Sons, N.Y.,
428 p.
Fridriksson, A.
1934. On the calculation of age-distribution within a stock of
cod by means of relatively few age-determinations as a key
to measurements on a large scale. Rapp. P. -v. R6un. Cons.
Perm. int. Explor. Mer 86:1-14.
420
SEN: SAMPLING COMMERCIAL FISH LANDINGS
KETCHEN, K. S.
1950. Stratified subsampling for determining age determina-
tions. Trans. Am. Fish. Soc. 79:205-212.
Kimura, D. K.
1977. Statistical assessment of the age-length key. J. Fish.
Res. Board Can. 34:317-324.
KUTKUHN, J. H.
1963. Estimating absolute age composition of California
salmon landings. Calif. Dep. Fish Game, Fish. Bull. 120,
47 p.
Mackett, D. J.
1963. A method of sampling the Pacific albacore (Thunnus
germo) catch for relative age composition. F.A.O. Fish.
Rep. 3:1355-1366.
Ricker, W. E.
1975. Computation and interpretation of biological statistics
offish populations. Fish. Res. Board Can., Bull. 191, 382 p.
Southward, G. M.
1976. Sampling landings of halibut for age composition. Int.
Pac. Halibut Comm. Sci. Rep. 58:1-31.
SUKHATME, P. V.
1954. Sampling theory of surveys with applications. Iowa
State College Press, Ames, 491 p.
Tanaka, S.
1953. Precision of age-determination of fish estimated by
double sampling method using the length for stratification.
Bull. Jpn. Soc. Sci. Fish. 19:657-670.
Tomlinson, P. K.
1971. Some sampling problems in fishery work. Biometrics
27:631-641.
WESTRHEIM, S. J., AND W. E. RlCKER.
1978. Bias in using an age-length key to estimate age-
frequency distributions. J. Fish. Res. Board Can. 35:184-
189.
421
A VARIABLE CATCHABILITY VERSION OF THE LESLIE MODEL WITH
APPLICATION TO AN INTENSIVE FISHING EXPERIMENT ON
A MULTISPECIES STOCK
Jeffrey J. Polovina1
ABSTRACT
A variable catchability version of the Leslie model is developed which permits the catchability of one
species to vary inversely with the abundance of competing species. This model is used to fit data from
an intensive fishing experiment conducted on a multispecies bottom fish stock in the Marianas where
catchability of a subordinate species is inversely related to the abundance of a more dominant species.
Analysis of this multispecies intensive fishing experiment produced estimates of exploitable bottom fish
density in the 150-275 m depth range of 10,156 fish per nmi2 or 1,354 fish per nmi of 183 m (100-fathom)
contour.
Intensive fishing of a closed population can produce
data to estimate the initial population size and the
catchability coefficient of fish stocks. Two frequently
used models applied to intensive fishing data are the
Leslie model and the Delury model (Ricker 1975).
The Leslie model expresses catch per unit effort
(CPUE) at any point during the period of intensive
fishing as a linear function of the cumulative catch
to that point, whereas the Delury model expresses
the logarithm of CPUE at any point during the in-
tensive fishing experiment as a linear function of
the cumulative effort. From a statistical viewpoint
the Leslie model is often preferable to the Delury
model, since a predictive linear regression is used
to estimate the parameters of both models and since
typically catch is measured more accurately than
effort.
Both the Leslie and Delury models assume that
catchability is constant during the period of inten-
sive fishing. However, experience indicates that this
assumption may not always be satisfied (Pope and
Garrod 1975; Schaaf 1975; MacCall 1976; Ulltang
1976; Garrod 1977; Peterman and Steer 1981; Fox2).
Several authors have found that competition for
baits between fish of different size or species can
alter catchability (Allen 1963; Rothschild 1967). In
this paper a variable catchability Leslie model will
be developed for multispecies application where, due
1 Southwest Fisheries Center Honolulu Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 3830, Honolulu, HI
96812.
2Fox, W. W. 1974. An overview of production modelling.
U.S. National Marine Fisheries Service, Southwest Fisheries
Center, Administrative Report LJ-74-10, La Jolla, CA.
to species interactions, the catchability of one
species is altered by the presence of other species.
This variable catchability Leslie model will be ap-
plied to multispecies intensive fishing data from
snapper (family Lutjanidae) populations where the
application of the constant catchability Leslie model
leads to biologically untenable results.
VARIABLE CATCHABILITY
LESLIE MODEL
The CPUE during a time interval t (CPUE(O) is
defined as the product of catchability (q) and the
mean population size (number of individuals) pres-
ent during the period t (N(t)), thus
CPUE(0 - qN(t).
(1)
Suppose that up to the beginning of period t, K(t)
fish have been caught and removed. If the period
t is relatively short, the population of fish closed or
isolated, and the fishing pressure heavy enough so
that it can be assumed that mortality from other fac-
tors is negligible, then N(t) can be expressed as
N(t) = N(0) - K(t),
where N(0) is the initial population size at the begin-
ning of the experiment (t = 0). Inserting this ex-
pression for N(t) in Equation (1) produces the Leslie
model:
CPUE(0 = q(N(0) - K(t)).
Manuscript accepted August 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
(2)
423
FISHERY BULLETIN: VOL. 84, NO. 2
Henceforth, this model will be referred to as the con-
stant catchability Leslie model.
In a multispecies situation, competition between
species for baited hooks may produce a dominance
hierarchy where some species are more aggressive
feeders than others and effectively out compete the
less aggressive feeders for baited hooks. The catch-
ability of the species at the top of the dominance
hierarchy, is independent of the presence of more
subordinate species, while the catchability of those
species not at the very top of the hierarchy will vary
inversely with the abundance of the more dominant
species. A simple model which describes the catch-
ability of a subordinate species (q(s,t)) as a function
of the cumulative catch and initial population size
of the more dominant species, K(d,t) and N(d,0)
respectively is
q(s,t) = q(s)(K(d,t)/N(d,0))
(3)
where q(s) is the catchability of the subordinate
species in the absence of the dominant species. Com-
bining Equations (2) and (3) produces
CPUE(s,0 = q(s)(K(d,t)/N(d,0))
x (N(s,Q) - K(s,t)) (4)
where V( ) and E( ) represent the variances and
means, respectively.
APPLICATION OF
MULTISPECIES LESLIE MODEL TO
SNAPPER INTENSIVE FISHING
A 13-d intensive fishing experiment covering the
period 10-19 April and 5-7 May 1984 was conducted
at Pathfinder Reef (lat. 16°30'N, long. 143°05'E) in
the Mariana Archipelago. Pathfinder Reef is a cir-
cular pinnacle rising steeply from a depth of about
1,600 to 16 m beneath the surface At the 200 m con-
tour, the diameter is about 0.8 nmi (Fig. 1). The snap-
per population at Pathfinder Reef is a closed popula-
tion for purposes of the intensive fishing since the
closest bank is a small pinnacle 40 nmi to the north.
Intensive fishing was conducted from the NOAA
ship Townsend Cromwell using four bottom hand-
lines on hydraulic gurdies targeting species in the
150-275 m depth range. Each day during the 13-d
experiment, fishing was conducted around the en-
tire perimeter of the bank. During the experiment
1,467 bottom fish were caught. Three lutjanids,
Pristipomoides zonatus, P. auricilla, and Etelis car-
bunculus, accounted for 1,317 fish or about 90% of
the catch (Table 1). Fishing effort was measured in
and by defining K(ds,t)
q{s)(N(s,0)/N(dM^dB2
(3) becomes
K(d,t)K(s,t), B\ =
q(s)IN(d,0) Equation
CPUE(s,0 = BlK(d,t) - B2K(ds,t).
Estimates of SI and .62 are obtained from multiple
linear regression and the estimates of N(s,0) and q(s)
are computed as
N(s,0) = B1IB2, and q(s) = N(d,0)B2.
The estimate ofN(d,0) is determined from the con-
stant catchability model. As is evident from Equa-
tion (4), the estimate of N(s,0) is independent of the
estimate oiN(d,0). Estimates of the variance of the
estimate of N(s,0) are obtained from estimates of
the means and variances of the estimates of 61, and
B2 and an exact expression for the variance of a
ratio (Frishman 1975). Thus,
V(N(s,0j) = V01IB2)
V(Bl)[E(B2)f - V(B2)[E(Bl)f
(E(B2)f [V(B2) + [E(B2)f]
(5)
Figure 1— Bathymetric chart of Pathfinder Reef showing the
segments of the 100-fathom (183 m) contour used to partition daily
fishing effort.
424
POLOVINA: CATCHABILITY VERSION OF LESLIE MODEL
Table 1 .—Species composition of bottom fish catch at Pathfinder
Reef.
Percent
Species
Number caught
of catch
Lutjanidae
Aphareus rutilans
4
0.27
Aprion virescens
1
0.07
Etelis carbunculus
314
21.40
Pristipomoides auricilla
262
17.86
P. filamentosus
16
1.09
P. flavipinnis
7
0.48
P. zonatus
741
50.51
Carangidae
Caranx lugubris
83
5.66
Seriola sp.
32
2.18
Serranidae
Cephalopholis igarasiensis
2
0.14
Epinephelus cometae
2
0.14
Saloptia powelli
3
0.20
Total
1,467
100.00
line-hours. As is indicated in Figure 1, the circum-
ference of the reef can be divided into three
segments— north, west, and south-southeast, each
having similar species composition (Table 2). Further,
an attempt was made daily to allocate a consistent
proportion of the day's fishing effort to each seg-
ment. The proportion allocated to each segment was
influenced by the length of each segment and wind
Table 2. — Species composition for the three segments of the cir-
cumference of Pathfinder Reef (see Figure 1).
South-
Southeast
North
West
Species
No.
%
No.
%
No.
Pristipomoides
zonatus
P. auricilla
Etelis carbunculus
358 51
170 24
171 25
160 68
37 16
39 17
223
55
104
58
14
27
and current conditions. On the average, the propor-
tion of the total daily effort allocated to each seg-
ment was 0.45 on the south-southeast, 0.21 on the
north, and 0.34 on the west. A chi-squared test ap-
plied to the daily allocation of fishing effort indicates
that there was no significant departure (P = 0.89)
from this allocation during the course of the fishing
experiment. Since the effort was reasonably con-
stant over the duration of the experiment and the
entire reef was fished each day, catch, effort, and
CPUE computed on a daily basis were used in the
analysis. An adjustment to cumulative catch sug-
gested by Chapman (1961) was subsequently shown
to improve the model fit in the Delury model
(Braaten 1969). This adjustment computes cumula-
tive catch for interval i as the cumulative catch to
interval i plus one half the catch during interval i.
This adjustment compensates for the decline in
CPUE within each time interval. The adjusted
cumulative catch is used as the independent variable
in all subsequent analyses (Table 3).
Plots of CPUE against adjusted cumulative catch
for each of the three species of snappers show a
decline in CPUE for P. zonatus, a slight decline for
E. carbunculus, and an increase for P. auricilla (Fig.
2). A regression line fitted to these data results in
negative slopes for P. zonatus (P = 0.0007) and E.
carbunculus (P = 0.05) and a positive slope for P.
auricilla (P = 0.008). The constant catchability
Leslie model fitted the P. zonatus data well and
resulted in an R2 of 0.71 and a pattern of residuals
which supports the linear model. The estimates of
N(0) and q for P. zonatus from this fit are 1,066 fish
and 0.0038 per line-hour. Due to the selectivity of
the fishing gear, N(0) estimated from this intensive
fishing data does not represent total population size
Table 3.— Daily catch, effort, catch per unit of effort (CPUE), and adjusted cumulative catch for Pristipomoides zonatus, P. auricilla, and
Efe//'s carbunculus
Effort
Tota
I
Pristipomoides zonatus
Adjusted
P. auricilla
£fe//s carbunculus
Adjusted
Adjusted
Adjusted
Date
(line-
Catch
cumulative
Catch
cumulative
Catch
cumulative
Catch
cumulative
1984
hours)
(no.)
CPUE
catch
(no.)
CPUE
catch
(no.)
CPUE
catch
(no.)
CPUE
catch
Apr. 10
27.5
152
5.53
76
98
3.56
49
12
0.44
6
42
1.53
21
Apr. 11
23.7
150
6.33
227
111
4.68
153.5
17
0.72
20.5
22
0.93
53
Apr. 12
21.3
100
4.67
352
47
2.21
232.5
12
0.56
35
41
1.93
84.5
Apr. 13
29.7
139
4.68
471.5
91
3.06
301.5
29
0.98
55.5
19
0.64
114.5
Apr. 14
29.3
112
3.82
597.0
66
2.25
380
17
0.58
78.5
29
0.99
138.5
Apr. 15
17.5
84
4.80
695.0
50
2.86
438
13
0.74
93.5
21
1.20
163.5
Apr. 16
30.7
129
4.20
801.5
67
2.18
496.5
26
0.85
113
36
1.17
192.0
Apr. 17
21.4
65
3.04
897.5
38
1.78
548
12
0.56
132
15
0.70
217.5
Apr. 18
22.4
81
3.62
970.5
41
1.83
587.5
15
0.67
145.5
25
1.12
237.5
Apr. 19
21.6
60
2.78
1,041
28
1.30
622.0
17
0.78
161.5
15
0.69
257.5
May 5
20.3
82
4.04
1,112.5
40
1.97
656
29
1.43
184.5
13
0.64
271.5
May 6
22.8
91
3.99
1,199.0
35
1.54
693.5
35
1.54
216.5
21
0.92
288.5
May 7
24.1
72
2.99
1,281
30
1.25
726.0
27
1.12
248.5
15
0.62
306.5
425
FISHERY BULLETIN: VOL. 84, NO. 2
5.0 1 r
4.0
UJ
a.
u
3.0
2.0
1.0-
-i r
Pristipomoides zonotus
Table 4.— Percent of catch by depth (in fathoms, 1 fathom
= 1 .83 m).
UJ
a.
u
I00
200 300 0 100
CUMULATIVE CATCH
200
300
400
Figure 2.— Daily catch per unit effort (CPUE) and adjusted
cumulative catch for Pristipomoides zonatus, P. auricilla, and
Etelis carbunculus.
but rather the population size of those fish that can
be caught by the fishing gear which will be termed
the exploitable population. Although the constant
catchability Leslie model does not explain as much
of the variation for E. carbunculus (R2 = 0.35) as
it does for P. zonatus, the regression is significant
and the pattern of residuals supports the linear fit.
The estimates for catchability and initial exploitable
population size for E. carbunculus from the fit of
this model are 0.0025 per line-hour and 583 fish. The
positive slope for the regression of CPUE on
cumulative catch for P. auricilla does not make
sense biologically under the constant catchability
Leslie model.
The depth of capture data show that P. zonatus
and P. auricilla were caught in the same depth
range, whereas E. carbunculus was typically caught
at somewhat greater depths (Table 4). Thus, species
interactions would most likely occur between P.
zonatus and P. auricilla. If P. zonatus is more ag-
gressive than P. auricilla in pursuing fishing baits
or in some other way affects the behavior of the lat-
ter, then the initial catchability for P. auricilla will
Depth
Species
<100
100-120
>120
Pristipomoides zonatus
P. auricilla
Etelis carbunculus
15.1
12.6
1.9
71.7
79.0
46.5
13.2
8.4
51.6
be low but will rise as the population of P. zonatus
is reduced. Applying the variable catchability Leslie
model to the P. auricilla data, with the assumption
that P. zonatus is the dominant species and that P.
auricilla is the subordinate species so that the catch-
ability of P. auricilla depends on the population size
of P. zonatus, results in the following relationship:
CPUE(a,0 = q(a)(K(z,t)/N(z,0))
x (N(a,Q) - K(a,t)),
(6)
where q(a) is the catchability of P. auricilla in the
absence of P. zonatus and N(z,0) and N(a,0) are the
initial exploitable population sizes of P. zonatus and
P. auricilla, respectively, and K(z,t) andK(a,t) are
the cumulative catch of P. zonatus and P. auricilla
to time t, respectively.
Using the estimate of N(z,0), 1,066 fish, from the
fit of the constant catchability model to P. zonatus
data, Equation (6) has two unknowns to be esti-
mated— q(a) and N(a,0). A multiple linear regression
model estimates the initial exploitable population
size of P. auricilla, N(a,0), at 2,007 fish and q(a) at
0.00087. The variable catchability Leslie model fits
the P. auricilla CPUE data well and produces an
R2 of 0.89 (Fig. 3). The estimates of initial popula-
tion sizes for the three species are summarized in
Table 5 together with their 95% confidence inter-
vals. For the constant catchability model, the
population size confidence interval is computed from
a relationship derived by Delury (1958), whereas the
confidence interval for the variable catchability
model is computed from the variance expression
given in Equation (5).
DISCUSSION
The constant catchability Leslie model fit the P.
zonatus and E. carbunculus data well but was not
appropriate for the P. auricilla data. The variable
catchability Leslie model fit the P. auricilla data
well and provided a plausible explanation for the
observed increase in CPUE. Given that there was
a time delay between the first 10 d of the intensive
426
FOLOV1NA: CATCHABILITY VEKS1UN OE LESLIE MODEL
fishing (10-19 April) and the last 3 d (5-7 May), and
that the greatest increase in the catchability of P.
auricilla occurred after the time delay, it is possible
that the increase in catchability might have a time
lag component associated with it. However, given
the short time series of data, it would be difficult
to test the appropriateness of a more complicated
time lag model.
Based on the fit of these two models the initial
exploitable population of the three species in the
150-275 m depth range at Pathfinder Reef is esti-
mated at 3,656 fish (Table 5). If we assume, based
on the species composition data (Table 1), that these
three species represent 90% of the exploitable
population then the total exploitable population at
the beginning of the intensive fishing is 4,062 fish.
18
1.6
Q.
O
Pristipomoides ouricillo
J I I L
0 25 50 75 IOO 125 150 175 200 225 250 275
CUMULATIVE CATCH
Figure 3.— Daily catch per unit effort (CPUE) and predicted
CPUE based on the variable Leslie model as a function of adjusted
cumulative catch for Pristipomoides auricilla.
From Figure 1 the length of the 183 m (100-fathom)
contour is estimated at 3.0 nmi, and the area in the
180-300 m depth range is estimated to be 0.4 nmi2.
With these area measures, density estimates of
1,354 fish per nmi of (183 m) 100-fathom contour
and 10,156 fish/nmi2, are obtained for Pathfinder
Reef.
Estimates of bottom fish densities based on visual
observation from a submersible at Johnston Atoll
were 57,281 fish/nmi2 for the 92-183 m (50-100
fathom) depth range and 66,199 fish/nmi2 for the
1983-274 m (100-150 fathom) depth range (Ralston
et al. 1986). These figures are considerably larger
than both the point and interval estimates presented
here. Significantly, the study of Ralston et al. (1986)
also employed the Townsend Cromwell, and the
catch rates were comparable at Pathfinder and
Johnston (e.g., 3.18 bottom fish/line-hour for the
latter). Thus the difference between estimates of
standing stock is likely not due to differences in ab-
solute abundance but rather to differences between
exploitable population size and total population size.
For example, at Johnston Atoll at least 69 species
of fish were observed from the submersible, whereas
only 10 species were taken by fishing gear in the
same depth (Ralston et al. 1986).
If the constant catchability Leslie model is applied
to the pooled data for the three species, an estimate
of exploitable population size of 2,689 is obtained,
about 71% of the estimate of the exploitable popula-
tion size for the three species when they are
estimated separately (Table 5).
Size-specific behavior has been raised as a factor
which might affect catchability (Allen 1963). For all
three species, there is no evidence of intraspecies
size-specific behavior affecting catchability since for
two of the species the constant catchability model
fits well and for the third species, catchability
depends only on the population size of an interact-
ing species. Further, under the hypothesis that
within a stock catchability is size-specific across the
Table 5.— Estimates of population size and catchability for three species.
Species
Model
f?
Catch-
ability
SE
Initial Confidence
population interval
size (95%)
Pristipomoides Constant
zonatus catchability 0.71 0.0038 0.0075
Efefe Constant
carbunculus catchability 0.35 0.0025 0.0010
P. auricilla Variable
catchability 0.89 0.00087 0.00031
Three species Constant
pooled catchability 0.66 0.0022 0.0047
1,066
(803-1,691)
583
(361-3,011)
2,007
(261-5,727)
2,689
(1,955-4,535)
427
FISHERY BULLETIN: VOL. 84, NO. 2
range of exploitable size, intensive fishing would
produce a substantial change in the population size
structure. A plot of the mean fork length by day of
fishing for the three species (Fig. 4) shows very lit-
tle change in fork length even for P. zonatus where
68% of the exploitable stock is estimated to have
been removed. Thus, the mean size of the fish in a
catch may be a much less sensitive indicator of
changes in the population size than catch rates, at
least over the short term.
ACKNOWLEDGMENTS
I wish to thank Alec D. MacCall and William E.
Schaaf whose reviews resulted in an improvement
in the formulation of the variable catch Leslie model.
This paper is a result of the Resource Assessment
Investigation of the Mariana Archipelago at the
Southwest Fisheries Center Honolulu Laboratory,
National Marine Fisheries Service, NOAA.
41
40
39
E
o 38
x
K
O
5 37
O 36
35
h ! r
Pristipomoides zonotus
Pristipomoides ouricillo
i i i i i
_i_
23456789 10
DAY
12 13 14
Figure 4.— Mean fork length for each day of fishing for Pristi-
pomoides zonatus, P. auricilla, and Etelis carbunculus.
LITERATURE CITED
Allen, K. R.
1963. The influence of behavior on the capture of fish with
baits. In The selectivity of fishing gear, Vol. 5, p. 5-7.
Proceedings of Joint ICNAF/ICES/FAO, Special Scientific
Meeting, Lisbon, 1957, Special Publications No. 5.
Braaten, D. 0.
1969. Robustness of the Delury population estimator. J.
Fish. Res. Board Can. 26:339-355.
Chapman, D. G.
1961 . Statistical problems in dynamics of exploited fisheries
populations. Proc. Berkeley Symp. Math. Stat. Probab.
4:153-168.
Delury, D. B.
1958. The estimation of population size by a marking and
recapture procedure. J. Fish. Res. Board Can. 15:19-25.
Frishman, F.
1975. On the arithmetic means and variances of products and
ratios of random variables. In G. P. Patil et al. (editors),
Statistical distributions in scientific work, Vol. I, p. 401-406.
Garrod, D. J.
1977. The North Atlantic cod. In J. A. Gulland (editor), Fish
population dynamics, p. 216-242. John Wiley & Sons, N.Y.
MacCall, A. D.
1976. Density dependence of catchability coefficient in the
California Pacific sardine, Sardinops sagax caerula, purse
seine fishery. Calif. Coop. Oceanic Fish. Invest. Rep. 18:
136-148.
Peterman, R. M., and G. J. Steer.
1981. Relation between sport-fishing catchability coefficients
and salmon abundance. Trans. Am. Fish. Soc. 110:585-593.
Pope, J. G., and D. J. Garrod.
1975. Sources of error in catch and effort quota regulations
with particular reference to variation in the catchability coef-
ficient. Int. Comm. Northwest Atl. Fish. Res. Bull. 11:
17-30.
Ralston, S., R. M. Gooding, and G. M. Ludwig.
1986. An ecological survey and comparison of bottom fish
resource assessments (submersible versus handline fishing)
at Johnston Atoll. Fish. Bull., U.S. 84:141-155.
Richer, W. E.
1975. Computation and interpretation of biological statistics
of fish populations. Fish. Res. Board Can., Bull. 191, 382 p.
Rothschild, B. J.
1967. Competition for gear in a multiple-species fishery. J.
Cons. 31:102-110.
Schaaf, W. E.
1975. Fish population models: potential and actual links to
ecological models. In C. S. Russell (editor), Ecological
modeling in a resource management framework, p. 211-239.
Johns Hopkins Univ. Press, Bait.
Ulltang, 0.
1976. Catch per unit of effort in the Norwegian purse seine
fishery for Atlanto-Scandian (Norweigian spring spawning)
herring. FAO Fish. Tech. Pap. 155:91-101.
428
EARLY DEVELOPMENT OF
THE LOPHIID ANGLERFISH, LOPHIUS GASTROPHYSUS
Yasunobu Matsuura and Nelson Takumi Yoneda1
ABSTRACT
Using larval specimens collected in bongo nets in southern Brazilian waters (between lat. 23° and 29 °S),
early development of the lophiid anglerfish, Lophius gastrophysus, is described and compared with other
lophiid species. Larval morphology of L. gastrophysus is very similar to that of L. americanus, having
three conspicuous melanophores on the trunk and caudal region, but the former can be easily distinguished
from the latter by the presence of two melanophores on the preopercular and suborbital regions and
positions of the melanophores on the elongate ventral fin.
The peculiar larvae of Lophius have been known
since the description of the early developmental
stage of L. americanus by Agassiz (1882). Their
characteristic form with elongate dorsal and ven-
tral fin rays makes them easily identifiable. Of the
25 species of the Lophiidae (Caruso 1981), larvae
have been repeatedly described and discussed for
L. piscatorius (Prince 1891; Williamson 1911;
Stiasny 1911; Allen 1917; Lebour 1919, 1925; Bow-
man 1920; Taning 1923; Arbault and Boutin 1968
Russel 1976) and for L. americanus (Agassiz 1882
Connolly 1920, 1922; Taning 1923; Berrill 1929
Dahlgren 1928; Procter et al. 1928; Bigelow and
Schroeder 1953; Martin and Drewry 1978; Fahay
1983; Pietsch 1984). The larvae of two other species
also have been described: L. budegassa (Stiasny
1911; Padoa 1956) and L. litulon (Tanaka 1916; Mito
1966). There is no literature on larval morphology
of L. gastrophysus.
During ichthyoplankton surveys along the south-
ern Brazillian coast, many Lophius larvae were col-
lected and identified as L. gastrophysus. This report
gives a detailed comparative description of larval
development based on 136 specimens collected dur-
ing the past 13 years.
MATERIALS AND METHODS
Larval specimens used in this report were ob-
tained from the collections of ichthyoplankton at the
Instituto Oceanografico da Universidade de Sao
Paulo. These samples were collected from the south-
ern Brazillian coast using a 61 cm bongo net follow-
ing the sampling method of Matsuura (1979) and
preserved in 10% Formalin2 solution. Notochord
length (NL) was taken from the tip of the upper jaw
to the tip of the notochord. A total of 136 larvae
(3.3-15.7 mm NL) of L. gastrophysus was used in
this study. Specimens were measured with a
micrometer in a stereoscopic dissecting microscope
and illustrations were made with the aid of a camera
lucida.
MORPHOLOGY OF LARVAE
The smallest identified specimens which were col-
lected with plankton nets as free-living forms were
about 3.3 mm NL, but they still had a large yolk sac.
Fahay (1983) showed that the newly hatched larvae
of L. americanus was as small as 2.5 mm long, and
they were still encased in the egg veils (Fahay3). The
reported size of newly hatched larvae of L. pisca-
torius was 4.5 mm TL (Lebour 1925).
Since the 3.3 mm larvae were not in perfect con-
dition, we used larger specimens for the morpho-
logical description. Preflexion larvae of L. gastro-
physus have a slender body (Fig. 1A, B, C, D), but
they later become robust form (Fig. IE, F). This
change of body shape is partly a result of increase
in body depth and partly due to enlargement of
subepidermal space (Fig. 1C, D, E, F), which ap-
pears, firstly, on the head region and later becomes
larger and extends posteriorly, giving the larvae a
balloonlike appearance. This subepidermal space
consists of transparent, gelatinous connective tissue
and is considered an adaptation to planktonic life
'Instituto Oceanografico da Universidade de Sao Paulo, Butanta,
Sao Paulo 05508, Brasil.
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
3M. P. Fahay, Northeast Fisheries Center Sandy Hook Labora-
tory, National Marine Fisheries Service, NOAA, Highlands, NJ
07732, pers. commun. July 1985.
Manuscript accepted August 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
429
FISHERY BULLETIN: VOL. 84, NO. 2
430
Figure l.—Lophitis gastrophysus larvae from
southern Brazil: A. 3.8 mm NL,
B. 4.5 mm NL. Scale bar is 1.0 mm.
MATSUURA and YOXEDA: EARLY DEVELOPMENT OF LOPHIID ANGLERFISH
Figure 1.— Continued— Lophius gastrophysus larvae
from southern Brazil: C. 5.6 mm NL,
D. 7.8 mm NL. Scale bar is 1.0 mm.
431
rionr^ivi dullliu1!. vul, o1*, n\j. c
Figure 1.— Continued— Lophius gastrophysus larvae
from southern Brazil: E. 9.2 mm NL,
F. 14.9 mm NL. Scale bar is 1.0 mm.
(Tarring 1923). Notochord flexion starts at about 9
mm NL (Fig. IE).
As shown in L. piscatorius larvae (Taning 1923),
the laterally compressed larval form changes gradu-
ally during their planktonic stage toward the dorso-
ventrally depressed shape of juvenile and adults. The
largest larvae examined, 15.7 mm NL, had not yet
achieved the juvenile stage, but a similar tendency
was observed. For example, the maximal breadth
of the head in 3.5 mm larva is only 22%, but that
in 15.7 mm larva is about 40% of body length. The
proportion of body depth also shows a similar
tendency, i.e., it starts at 30% at 4 mm and attains
45% of body length at 15.7 mm. The proportion of
head length starts at about 23% at 4.5 mm and at-
tains almost 45% at 15.7 mm NL.
Statistics describing regressions of different body
parts in relation to body length are shown in Table
1. The regressions lines of head length and body
depth showed an inflexion at the size of 7.6 mm NL,
while those of other body parts were linear for the
size range 3.2-15.7 mm NL. Thus, the regressions
432
MATSUURA and YONEDA: EARLY DEVELOPMENT OF LOPHIID ANGLERFISH
Table 1 .—Statistics describing regressions relating notochord length with length of different body
parts of Lophius gastrophysus larvae, a and b = constant (y = a + bx), r = correlation coeffi-
cient, n = number of specimens.
Characters (x)
Size range of
notochord length
(V) (mm)
a
b
r
n
Head length
3.2- 7.5
-0.18334
0.27117
0.68827
97
7.7-15.7
-2.11501
0.56058
0.94483
27
Body depth
3.2- 7.5
0.10498
0.28333
0.74299
99
7.7-15.7
-2.49286
0.65397
0.92825
27
Preanal distance
3.2-15.7
- 1 .54475
0.77254
0.96482
27
Predorsal distance
3.2-15.7
- 1 .65336
0.74641
0.96717
27
Eye diameter
3.2-15.7
- 0.00095
0.10383
0.94353
124
Length of the second dorsal
spine
3.2-15.7
-3.19397
0.99987
0.90707
96
Length of the third ventral fir
i ray
3.2-15.7
-3.47484
1.14083
0.90497
102
lines of the former were calculated in two size
ranges.
PIGMENTATION
Lophius gastrophysus larvae develop a distinct
pattern of melanophores. Since early stage (Fig.
1 A), there are three large pigment bars on the trunk
and caudal region and they remain at the same posi-
tion during larval stage. The larva of 14.9 mm NL
(Fig. IF) has a heavily pigmented body, but the three
large pigment bars on the trunk and caudal region
are still visible. There are dense melanophores over
the occipital region of the head and shoulder (Fig.
1A). Pigments on the elongate ventral fin ray is also
visible in the smallest specimen, but the positions
and number of them change gradually. In the
earliest stage (3.8 mm NL) there are two melano-
phores on the ventral fin: one at the fin ray base
and another at the middle of the ventral fin. At the
size of 4.5 mm NL (Fig. IB), there appears another
small melanophore at one-third the length of the fin
ray. The melanophore at the fin ray base remains
at the same position, but the distal large one moves
to the position three-fourths the length of the fin
ray. After this size, positions and number of melan-
ophores on the elongate third ventral fin ray remain
the same up to 15.7 mm NL. When distal part of
other ventral fin rays start to separate from the
third one, there appears some melanophores on the
distal edge of each fin ray.
There appears a patch of melanophores on the
preopercular region at 3.8 mm NL and another small
one appears on the suborbital region at 4.5 mm NL.
The small melanophore, which appears on the tip
of the elongate second dorsal spine at 4.5 mm NL,
will later become a large pigment bar (Fig. 1C,
D).
FIN DEVELOPMENT
The most remarkable change can be seen in
lengths of the dorsal and ventral fins. Since the
earliest stage (Fig. 1A), the larvae have elongate
dorsal spine and ventral fin ray, which later become
the second dorsal spine and the third ventral fin ray,
respectively. The length of the second dorsal spine
relative to body length changed from 28% at 3.3 mm
NL to 90% at 8.3 mm NL (Fig. 2A). In larger lar-
vae the proportion of the second dorsal spine length
relative to body length decreased gradually to 70%
at 15.7 mm NL. A similar tendency was observed
for the length of the third ventral fin ray: it varied
from 45% of body length at 3.3 mm NL to 121% at
11.6 mm NL (Fig. 2B). Unfortunately, these fin rays
are in many cases lost or damaged at the distal tip,
making it difficult to say whether we measured the
total length of fin rays or the partial length of a
damaged ray. In any case, the figure shows a clear
tendency of rapid increase of fin rays during larval
stage.
The number of fin rays increases during larval
stage. For example, the origin of the first dorsal
spine firstly appears anterior to the elongate sec-
ond dorsal spine in 9.2 mm NL larva (Fig. IE). The
tip of the first dorsal spine which will transform in-
to the illicium in the adult fish, emerges from the
epidermal skin at about 10 mm NL. At this size, all
fin rays are well developed and number of fin rays
on the second dorsal, anal, and caudal fins attains
the adult number.
Another remarkable change in fin development
is a forward advancement of the dorsal spines. At
3.3 mm NL larva, the elongate second dorsal spine
lies behind the head (Fig. 1A) and it moves gradu-
ally forward during larval stage; at 14.9 mm NL,
433
FISHERY BULLETIN: VOL. 84, NO. 2
%
80
60
40
20
0
120
100
80
60
40
20
•••
• •
* ••<
•: •*
• •• . .• * •
. ••••
i i i t ' i ' ' ' L
IT? '
oMv
••if*. •
i i i i i
j i i_
_i i i_
5 7 9 II
BODY LENGTH
13
15 mm
Figure 2.— Relationships between changes of proportion of second
dorsal spine (A) and third ventral fin ray (B) and body length (NL)
of Lophius gastrophysus.
it becomes the position anterior to the eyes (Fig.
IF).
DISCUSSION
Based on a study of world-wide collections, Caruso
(1981, 1983) recently concluded that the Lophiidae
is represented by 4 genera and 25 species, of which
only 2 species inhabit the western Atlantic: Lophius
americanus in the western North Atlantic and L.
gastrophysus in the western Central and South
Atlantic. The geographic ranges of the two species
overlap between Cape Hatteras, NC, and Florida.
The two western Atlantic species are very similar,
but they can be easily distinguished by differences
in dorsal and anal fin ray counts, size of the third
and fourth dorsal spines, and differences in pigment
pattern (Caruso 1983).
It is well known that lophiid anglerfishes spawn
over deep water producing large gelatinous ribbons
of spawn which often contain more than a million
eggs (Berrill 1929). Spawning behavior is not known,
but some authors have suggested that it may occur
at or near the bottom (Taning 1923; Dahlgren 1928).
After hatching, the larvae emerge from the gela-
tinous capsules and pass a long planktonic stage.
Upon attaining a length of about 60 mm TL, young
fish probably take to the bottom (Connolly 1922;
Taning 1923; Bigelow and Schroeder 1953).
As shown previously, Lophius larvae can be easily
distinguished from those of other species. Because
there is only one species in the western South Atlan-
tic, there is no doubt about the identification of our
larvae as L. gastrophysus. Therefore, we have
documented morphological differences in early
developmental stages of our specimens and com-
pared them with those of other well-known species
(Table 2).
Meristic characters and adult forms of L. ameri-
canus and L. piscatorius are very similar, but their
larval forms are quite different (Taning 1923). The
most remarkable difference is the presence of three
large pigment bars on the trunk and caudal region
in L. americanus from the yolk-sac stage. He also
pointed out that the larval development of L. ameri-
canus was more rapid than that of L. piscatorius.
The larvae of L. gastrophysus are very similar to
that of L. americanus. Both species have three large
pigment bars on the trunk and caudal region from
the very earliest stages. Larval development of L.
gastrophysus is more rapid than that of L. ameri-
canus, e.g., formation of the bases of the second dor-
sal and anal fins and the five dorsal spines occurs
at sizes 8.1 mm, 8.5 mm, and 11.5 mm, respective-
ly, for L. gastrophysus, L. americanus, and L.
piscatorius. In the same way, the first appearance
of canine teeth on both jaws occurs at sizes of 4.2
mm, 6.5 mm, and 9.8 mm, respectively, in the same
order for the three species.
Another difference is in the position of the mela-
nophore of the ventral fin, present on the distal part
of this fin in larvae of L. americanus and L. pisca-
torius, but at three-fourths the length of the fin in
L. gastrophysus larvae. The presence of pigmenta-
tion in the preopercular and suborbital regions is
also peculiar to L. gastrophysus larvae.
ACKNOWLEDGMENTS
The authors wish to thank Edward D. Houde
of the University of Maryland for revision and
critical reading of the manuscript.
They are also grateful to June Ferraz Dias and
Kazuko Suzuki for sorting and drawing the larvae.
The financial support of this work came from the
434
MATSUURA and YONEDA: EARLY DEVELOPMENT OF LOPHIID ANGLERFISH
Table 2.— Comparison of development stages of three Atlantic species of lophiid anglerfishes.
Characters
L gastrophysus
L. americanus
L. piscatorius
General development
Formation of bases of second dorsal and anal
fins, the five dorsal spines, and the elongate
ventral fin
First dorsal spine
Completion of anal fin rays
Completion of soft dorsal fin rays
Size at first appearance of canine teeth in
both jaws
Size of newly hatched larva
Pigment on distal edge of the second dorsal
spine
Position of pigment on distal part of the
ventral fin
Pigment bars on the trunk and caudal region
Meristic characters7
Dorsal fin rays
Anal fin rays
Pectoral fin rays
Vertebrae
8.1
about 10-11 mm
9.3 mm
9.3 mm
4.2 mm
about 3.5 mm
since 5.2 mm
3/4 of ventral fin
three bars since
early stage
9-11
8-9
22-26 (24.6)
26-27 (26.2)
8.5 mm'
about 12-14 mm1'2
10.5 mm2
10.5 mm2
6.5 mm2
about 2.5 mm4
no pigment ' 2
far distal edge2, 6
three bars since2
early stage
11-12
9-10
25-28 (26.1)
28-30 (29.1)
11.5 mm2
about 15-16 mm2 3
16 mm3
16 mm3
9.8 mm2
about 4.5 mm3
since 6 mm3 5
far distal edge5
anterior two bars5
since 11 mm
11-12
9-10
23-27 (25.2)
30-31 (30.4)
'Martin and Drewry 1978; 2Taning 1923; 3Russel 1976; "Fahay 1983; 5Lebour 1925; 6Agassiz 1882; 7Caruso 1983.
Note: For comparative purpose, the body length was given in total length for all species. Notochord length of L gastrophysus larvae
was converted to total length with an equation: TL = 1.024 mm NL + 0.1168 (r = 0.999), for larvae smaller than 10.0 mm NL.
Financiadora de Estudos e Projetos (FINEP). The
senior author received the research fellowship of the
Conselho Nacional de Desenvolvimento Cientifico
e Tecnologico (CNPq) and the junior author received
the scholarship of the Fundacao de Amparo a Pes-
quisa do Estado de Sao Paulo (FAPESP). This is
contribution n? 620 of the Institute Oceanografico
da Universidade de Sao Paulo.
LITERATURE CITED
Agassiz, A.
1882. On the young stages of some osseous fishes. Part III.
Proc. Am. Acad. Arts Sci. 17:271-303.
Allen, E. J.
1917. Post-larval teleosteans collected near Plymouth during
the summer of 1914. J. Mar. Biol. Assoc, U.K. 11:207-250.
Arbault, S., and N. L. Boutin.
1968. Ichthyoplancton. Oeufs et larves de poissons t6l6o-
steens dans le Golfe de Gascogne en 1964. Rev. Trav. Inst.
Peches Marit. 32:413-476.
Berrill, N. J.
1929. The validity of Lophius americanus Val. as a species
distinct from L. piscatorius Linn., with notes on the rate
of development. Contrib. Can. Biol. (N.S.) 4:145-151.
Bigelow, H. B., and W. C. Schroeder.
1953. Fishes of the Gulf of Maine. U.S. Fish Wildl. Serv.,
Fish. Bull. 53, 577 p.
Bowman, A.
1920. The eggs and larvae of the angler (Lophius piscatorius)
in Scottish waters. A review of our present knowledge of
the life history of the angler. Sci. Invest. Fish. Board Scotl.
1919, No. 1, p. 1-42.
Caruso, J. H.
1981. The systematics and distribution of the lophiid angler-
fishes: I. A revision of the genus Lophiodes with the descrip-
tion of two new species. Copeia 1981:522-549.
1983. The systematics and distribution of the lophiid angler-
fishes: II. Revisions of the Genera Lophiomus and Lophius.
Copeia 1983:11-30.
Connolly, C. J.
1920. Histories of new food fishes. III. The angler. Bull.
Biol. Board Can., Ottawa, No. 3, 17 p.
1922. On the development of the angler (Lophius piscatorius
L.). Contrib. Can. Biol. 1921(7):113-124.
Dahlgren, U.
1928. The habits and life history of Lophius, the angler fish.
Nat. Hist. 28:18-32.
Fahay, M. P.
1983. Guide to the early stages of marine fishes occurring
in the western North Atlantic Ocean, Cape Hatteras to the
southern Scotian shelf. J. Northwest Atl. Fish. Sci. 4:1-423.
Lebour, M. V.
1919. Feeding habits of some young fish. J. Mar. Biol.
Assoc, U.K. 12:9-21.
1925. Young anglers in captivity and some of their enemies.
A study in a plunger jar. J. Mar. Biol. Assoc, U.K. 13:
721-734.
Martin, F. D., and G. E. Drewry.
1978. Development of fishes of the Mid-Atlantic Bight: an
atlas of eggs, larval and juvenile stages. Vol VI, Strom-
ateidae through Ogcocephalidae. U.S. Fish Wildl. Serv. Off.
Biol. Serv., 78/12, 416 p.
Matsuura, Y.
1979. Distribution and abundance of eggs and larvae of the
Brazilian sardine, Sardinella brasiliensis, during 1974-75
and 1975-76 seasons. Bull. Jpn. Soc Fish. Oceanogr. 34:
1-12.
Mito, S.
1966. Fish eggs and larvae. [In Jpn.] In S. Motoda (editor),
Illustrations of the marine plankton of Japan, Vol. 7, 74 p.
Soyo-Sha, Tokyo.
435
Padoa, E.
1956. Triglidae, Peristediidae, Dactylopteridae, Gobiidae,
Echneidae, Jugulares, Gobiesocidae, Heterosomata, Pedicu-
lati. [In Ital.] In Uova, larve, e studi giovanili di Teleostei,
p. 627-880. Fauna Flora Golfo Napoli 38.
PlETSCH, T. W.
1984. Lophiiformes: development and relationships. In H.
G. Moser et al. (editors), Ontogeny and systematics of fishes,
p. 320-322. Am. Soc. Ichthyol. Herpetol., Spec. Publ. No. 1.
Prince, E. E.
1891. Notes on the development of the angler-fish (Lophius
piscatorius). 9th Ann. Rep. Fish. Board Scotl., (1890), p.
343-348.
Procter, W., H. C. Tracy, E. Helwig, C. H. Blake, J. E.
Morrison, and S. Cohen.
1928. Fishes— a contribution to the life history of the angler
(Lophius piscatorius). In Biological survey of the Mount
Desert region, Part 2, p. 1-29. Philadelphia.
Russel, F. S.
1976. The eggs and planktonic stages of British marine fishes.
Acad. Press, Lond., 524 p.
Stiasny, G.
1911. Uber einige postlarvale Entwicklungsstadien von Lo-
phius piscatorius L. Arb. Zool. Inst. Univ. Wien 19:57-74.
Tanaka, S.
1915-1919. Figures and descriptions of the fishes of Japan.
J. Coll. Sci., Imp. Univ. Tokyo 24:419-440.
Taning, A. V.
1923. Lophius. Rep. Dan. Oceanogr. Exped. 1908-1910
Mediterr. Adjacent Seas 2, Biol. A. 10, 30 p.
Williamson, H. C.
1911. Notes on the eggs of the angler (Lophius piscatorius),
halibut (Hippoglossus vulgaris), Conger vulgaris and tusk
(Brosmius brosme), a young Arnoglossus sp.; abnormalities
in Lophius, Gadus, Raia; diseases in Gadus, Pleuronectes,
Onos, Zoarces; occurrence of Himantolophus rheinhardti,
and Clupea pilchardus; the effectiveness of a seine-trawl in
a small pond. 28th Ann. Rep. Fish. Board Scotl, (1909),
Part III, p. 46-66.
436
EX-VESSEL PRICE LINKAGES IN
THE NEW ENGLAND FISHING INDUSTRY
Dale Squires1
ABSTRACT
This study examines the direction of ex- vessel price linkages between the three New England ports of
Boston, New Bedford, and Gloucester. Within-sample, bivariate tests of Granger causality are applied
for monthly data from 1965 through 1981. It is found that cod and haddock prices are formed in New
Bedford, that pollock prices are simultaneously formed between Boston and Gloucester, and that a spurious
relationship exists for flounder prices between the three ports. The hypothesis is advanced that this
spurious relationship may be due to flounder price leadership from outside the region, most probably
the New York Fulton Fish Market.
The direction of price linkages between various
market and production centers in an industry is im-
portant to studies of marketing and prices. Although
these spatial and hierarchical relationships are
generally well understood in domestic agriculture,
they have received little or no attention in natural
resource utilization and in the domestic commercial
fishing industry in particular. This study therefore
examines the spatial characteristics of round ex-
vessel price linkages of the most important species
in the New England fishing industry from 1965
through 1981.
Three ports— New Bedford, Boston, and Glouces-
ter—dominate the New England fishing industry,
as both home ports or production centers and as
marketing centers. By both volume and value of
landings, New Bedford is the most important port,
followed by Gloucester and then Boston. The most
important species of groundfish in New England are
cod; haddock; yellowtail, winter, and other
flounders; ocean perch or red fish; and pollock. Sea
scallops and lobsters also provide a significant con-
tribution to the industry in both value and volume
of landings. This study accordingly focuses upon the
ports of Boston, New Bedford, and Gloucester, and
the species of cod, haddock, yellowtail and winter
flounders, and pollock. Additional attention is given
to ocean perch and sea scallops, though rigorous con-
clusions are not possible.
In New Bedford and Boston, fishermen sell their
catches to the highest bidder in an open auction. The
New Bedford auction begins at 8:00 a.m. and ends
at 8:22 a.m. The Boston market begins at 7:00 a.m.,
and invariably overlaps with the New Bedford
market. There is significant communication between
the two markets during the auctions. The volume
and total value of fish harvested is substantially
greater in New Bedford than in Boston. Bidders pur-
chase an entire vessel's landings in New Bedford,
while in contrast, purchasers offer individual bids
for each species in Boston. In most of the ports other
than Point Judith in Rhode Island (where an impor-
tant fishermen's cooperative exists), the catch is sold
directly to fish processors or by prior arrangements
between individual vessels and purchasers. Further,
it is generally believed that Gloucester prices for
most fresh groundfish species are set in Boston, and
differ only by a transportation cost.
Fishermen of all ports are free to land their
harvests at any port offering the highest prices,
which, however, must be balanced against steam-
ing time. Few vessels land exclusively at a single
port, since the distances between the three are not
great. A definite limit exists to port switching due
to the prevalence of market transactions costs.
Wilson (1980) indicated that personal and financial
relationships tend to bind particular fishermen and
fish buyers. In contrast to many other natural
resource and primary production industries, a
futures market does not exist for fresh fish.2
Different ports and markets have developed
singular reputations. These specializations are based
in large part upon proximity to resource stocks. New
Bedford has developed a reputation as a flounder
and sea scallop port, while Boston has become
known as a cod, haddock, and, to a lesser extent,
'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038.
2Trading on futures markets involves buying and selling stan-
dardized contracts for the future delivery of a specific grade of
a commodity at a specific location(s).
Manuscript accepted August 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
437
KISHLKY BULLETIN; VUL. 84, NO. Z
pollock port. Although Gloucester fishermen direct
much of their effort towards cod, haddock, and
flounders (generally joint products), Gloucester has
developed a reputation as a port for both pollock and
ocean perch.
Conventional wisdom in the New England ground-
fishery market holds that New England round (fish
as harvested) ex- vessel prices of fresh flounders are
formed in the New Bedford auction market, while
fresh cod, haddock, and pollock round ex-vessel
prices are set in the Boston auction. These widely
held beliefs serve as the null hypotheses to be tested
in this study of the ex-vessel groundfish price link-
ages in New Bedford, Gloucester, and Boston.
Knowledge of ex-vessel price linkages has a num-
ber of applications. Efforts at improving market ef-
ficiency would find this information useful. The
broadcasting of daily ex- vessel fish prices by the Na-
tional Marine Fisheries Service can properly focus
upon the most crucial markets. Infrastructural or
institutional improvements can be more judicious-
ly targeted, an important consideration in a time of
tight public and private budgets. Price forecasts to
improve industry functioning can concentrate upon
those prices formed in markets which demonstrate
price leadership. Fishermen may want to land their
harvests in the market in which ex-vessel prices are
first formed, should fishermen want to affect the
pricing process, be less dependent upon the land-
ings of others, or capture advantageous prices.
Similar considerations apply to buyers. Knowledge
of the price formation process allows government
price policies to target the appropriate markets.
Finally, price linkage information is crucial to
studies of marketing margins, length of price trans-
mission, and asymmetric pricing.
THE DATA
The data are taken from the vessel weighout files
of the National Marine Fisheries Service. After
every trip of a commercial fishing vessel of any gear
type, port agents in each port obtain the value and
volume of landings for each species harvested. The
entire collection of this information constitutes the
weighout file. The output vector from the weighout
file is then linearly aggregated over vessels and trips
to form monthly round ex-vessel prices for each
port. The resulting nominal prices are subsequent-
ly deflated by the consumer price index for food. As
Sims (1974) and Feige and Pierce (1980) noted, the
use of seasonally adjusted data may confound lag
distributions and causality relationships. Conse-
quently, the data are left in their unseasonalized
state. However, to account for seasonal differences,
quarterly dummy variables are employed. The time
domain of the data set extends from 1965 through
1981.
METHOD OF ANALYSIS
Granger (1977) provided a definition of causality
among a set of variables that is based upon predic-
tability as well as the fact that the effect of a change
in an exogeneous variable upon an endogeneous
variable requires time. A variable X causes another
variable Y, with respect to a given universe or in-
formation set that includes X and Y, if present Y
can be better predicted by using past values of X
than not doing so, all other information in the past
of the universe being used in either case. Causality
from Y and X is defined in the same manner. Feed-
back occurs if X causes Y and Y causes X. A causal
relationship between X and Y does not exist if
causality does not run from X to Y or from Y to X,
and feedback does not occur.
Causality tests may be classified into two funda-
mental types at their most basic level, within-sample
and out-of-sample tests. The within-sample test is
widely applied and is the first one developed. This
test is developed over the full-time domain of the
data set, and essentially relies upon a measure of
fit. The definition of causality in the out-of-sample
test requires evidence of improved forecasts. This
approach is implemented by identifying and esti-
mating different models using the first part of the
sample and then comparing their respective fore-
casting abilities on the latter part of the sample. This
study utilizes the within-sample test, the one most
commonly applied, since the properties of the out-
of-sample test have yet to be systematically
examined.
Two basic approaches have been advanced by
which to apply empirically the within-sample
bivariate Granger criterion to time series. The first
approach is represented by the test proposed by
Pierce (1977) based upon Haugh (1976). The proce-
dure first estimates whitening filters for each time
series, then subsequently estimates the cross-
correlation function for the first step's residuals.3
However, Sims (1977) and Geweke (1981) indicated
that this approach may be limited.4 A second basic
3Whitening filters remove serial correlation from a time series.
Each time series used in a test of causality will be a white noise
process, and any relationships will be based on actual, systematic
relationships between the two time series, instead of a spurious
relationship caused by the common serial correlation.
4Prefiltering each time series with separate autoregressive inte-
grated moving average (ARIMA) filters biases the test toward
438
SQUIRES: EX-VESSEL PRICE LINKAGES
approach relying directly upon distributed lag rela-
tionships between dependent and independent
variables has led to three widely used tests: those
suggested by Sims (1977), the direct Granger test
forwarded by Sargent (1976), and the Modified Sims
test advanced by Geweke et al. (1983).
The small-sample properties of the Sims (1972),
direct Granger, and Modified Sims tests have
recently been examined within Monte-Carlo frame-
works by Guilkey and Salemi (1982) and Geweke et
al. (1983). Although the two studies differ somewhat
in their specifications, both found that the Sims test
was outperformed by the other two. Since the Sims
test is more time-consuming and expensive to
employ and requires more decisions about param-
eterizations, both studies unequivocally recommend
against its use.
The two studies reach slightly different conclu-
sions on the efficacy of the direct Granger and
Modified Sims test. These contradictory results can
be attributed to differences in research design.
Geweke et al. (1983) concluded that the two tests
essentially perform equally well. In contrast, Guilkey
and Salemi (1982) determined that the direct
Granger test consistently outperforms the Modified
Sims procedures by small amounts. Since the direct
Granger test is computationally the least expensive
of the three and results in the fewest degrees of
freedom lost from formation of leads and lags,
Guilkey and Salemi recommend its use over the
Modified Sims and Sims procedures. Nonetheless,
they do note that the Granger procedure's advan-
tage over the other two diminishes with increases
in sample size.
Several additional findings of Guilkey and Salemi
(1982) are also worth reporting. They observed that
for sample size <200, the shorter versions of all
three tests are superior to the longer versions.5 They
further noted that in their Monte-Carlo study the
direct Granger and Modified Sims procedures ac-
curately recover the coefficients of the relevant
population projections of the statistical model used
to generate experimental time series in small
samples. Consequently, it may be unlikely to observe
"large" coefficient estimates arising spuriously.
Finally, test performance is extremely sensitive to
sample size, strength of causation, and length of test
parameterization employed.
The direct Granger test as applied in this study
is based upon ordinary least squares regression of
the current observation of the time series of round
ex-vessel prices from one port upon its own past
observations and the past observations of the other
port's round ex-vessel prices for species k:
4 J
P2k(t) = a, + I bkl D% + cLT + I dkj P2k
J
x(t-j)+ Z fkj Plk (t - j) + ekt. (1)
Here, LT refers to a linear time trend, Dt is the
zero-one variable for quarter i, Plk(t) is the round
ex- vessel price of species k in month t in port 1, J
is the number of periods lagged, and ekt is a vector
of stochastic, white noise residuals. The presence
of lagged dependent variables in Equation (1) is
counted on to remove serial correlation from the
estimated residuals.6
The test of the null hypothesis that P\k does not
cause P2k is a test that fkj = 0, j = 1,2,. . .,J.
Guilkey and Salemi (1982) indicated that the F-test
statistic is calculated by estimating Equation (1) in
both constrained (fkj = 0, j = 1,2,. . . ,J) and un-
constrained forms, and may be written as7
F =
(SSEC - SSEJJ
SSEJ(T - (2J + 2))
(2)
where SSEU and SSEC are the residual sum of
squares from the unconstrained and constrained
regressions, respectively, and T represents the
number of monthly observations on round ex- vessel
prices. Under the null hypothesis, F is an F-test
statistic with J and T - (2J + 2) degrees of free-
dom. This procedure is then repeated reversing the
roles of P\k and P2k to test the null hypothesis that
P\k does not cause P2k.
The direct Granger test requires selection of a lag
length, J, large enough to purge serial correlation
from estimated residuals. Several factors require
consideration before specifying the lag length.
Chilled fresh fish is a commodity that rapidly
deteriorates in quality. Consequently, definite limits
exist to the length of time which inventories of
failing to reject the null hypothesis of independence of the two
series more often than the specified level of significance suggests.
Because of this limitation, the second basic approach is applied.
5Longer versions of these tests include additional lead and lag
variables.
"Serial correlation exists when the error terms from different
observations in a time series are correlated. Serial correlation tends
to give unbiased but inefficient estimators, and a biased sampling
variance, which then affects the results from significant tests such
as the F- or -t-tests.
7A constrained F-test includes one or more restrictions, such as
one or more coefficients constrained to zero. An unconstrained F-
test does not include these restrictions.
439
chilled fresh fish can be held. Since most ground-
fish harvested in New England waters are not pro-
cessed into frozen fish products, long-term storage
of New England groundfish is unlikely, and fresh
fish prices are likely to adjust more quickly than
those of most other food commodities. In addition,
previous exploratory analysis with adaptiver filter-
ing methods on the weighout file suggests that two
sets of round ex-vessel prices for any species k are
particularly important, the previous month's price
and the price within one month on either side of the
previous year. In order to account for these charac-
teristics and to provide both short and long versions
of the test, lags of 8 and 14 mo were specified. These
lag lengths are sufficiently long to encompass price
lags with monthly data. The diagnostic Q test of Box
and Pierce (1970) is used to detect serious serial
correlation.
EMPIRICAL RESULTS
The empirical results from the direct Granger
causality tests lead to somewhat unexpected con-
clusions for most species. The null hypothesis that
monthly round ex-vessel prices of cod and haddock
in all three ports are first formed in the Boston auc-
tion market is rejected in almost all instances. The
findings in Table 1 instead suggest that the cod and
haddock prices established in the New Bedford auc-
tion lead the prices formed in the Boston market.
Several factors may account for this. The New Bed-
ford auction's volume of landings is substantially
higher than that of Boston. In addition, the two
market times ordinarily overlap, and frequent com-
munication occurs between economic agents during
the auctions. Further, the proximity of New Bed-
ford to Boston allows fresh fish to be easily trucked
to Boston from New Bedford. The markets are thus
physically linked, before the auctions by fishermen
and after the auctions by fish buyers. One element
of conventional wisdom may perhaps be substan-
tiated, however. Although the Q-test statistic in-
dicates severe serial correlation (and thereby
possibly refuting the F-test statistic), the empirical
results indicate that Boston cod prices do lead
Gloucester cod prices at the ex-vessel level for the
shorter lag length parameterization.
Rejection of the null hypothesis that Boston prices
lead New Bedford and probably Gloucester cod and
haddock round ex-vessel prices and the finding that
New Bedford prices lead Boston prices suggest a
second null hypothesis for consideration. This sec-
ond hypothesis states that Gloucester cod and had-
dock prices are directly led by New Bedford prices.
In addition, the possibilities that Boston prices lead
Gloucester prices and that New Bedford prices lead
Boston prices suggest an additional, indirect price
linkage between Gloucester and New Bedford via
Boston.
The results for this second null hypothesis are also
given in Table 1. Since this is an unplanned com-
parison, a Scheffe interval is used.8 Strictly followed,
8An unplanned comparison occurs when in the course of exam-
ining results a hypothesis is tested which was not specified prior
to the experiment. The initial region is altered by the additional
information, so that the level of significance has changed. A Scheffe
interval allows for a more cautious test by providing a larger
critical value than that given by a t or F table. This pre-test bias
is accounted for by a conservative test. The F-test statistic now
Table 1 .—Direct Granger causality tests for monthly fresh round ex-vessel cod and haddock
prices.
Cod
Haddock
Direction1
Lags2 F-test3 Q-test4
Direction1
Lags2 F-test3 Q-test4
B
B
G
G
B
B
NB
NB
G
G
NB
NB
->G
->G
->B
->B
->NB
->NB
->B
->B
->NB
->NB
->G
->G
8
14
8
14
8
14
8
14
8
14
8
14
2-37*
1.17
1.59
1.02
1.67
0.74
2.52*
1.89*
1.78
0.91
52.96
1.40
35.67*
2.61
10.98
12.35
13.52
21.85*
8.82
16.27
16.46
28.42
7.84
6.86
B
B
G
G
B
B
NB
NB
G
G
NB
NB
->G
->G
->B
->B
->NB
->NB
->B
->B
->NB
->NB
->G
->G
8
14
8
14
8
14
8
14
8
14
8
14
1.69
1.09
1.07
1.29
0.08
0.09
3.15*
1.76*
0.56
1.36
52.90
1.65
9.60
4.49
10.98
15.07
12.54
7.06
8.62
8.74
11.71
15.09
11.76
8.37
'Variable abbreviations are B (Boston), G (Gloucester), NB (New Bedford).
2J indicates J months lagged.
3Null hypothesis that past values of the causal variable do not significantly affect current values of the
dependent variable. An asterisk indicates rejection of the null hypothesis at the 5% level.
4Null hypothesis that regression residuals are white noise. An asterisk indicates rejection of the null
hypothesis at the 5% level.
5F-test statistic is significant at the 5% level, but not significant at the 5% level when a Scheffe interval is used.
440
SQUIRES: EX-VESSEL PRICE LINKAGES
the results indicate that the cod and haddock price
linkage does not run from New Bedford to Glouces-
ter. If a Scheffe interval is not used, then the New
Bedford cod and haddock prices do lead those of
Gloucester. Therefore, with this caveat, New Bed-
ford auction market monthly round ex-vessel cod
and haddock prices lead the prices of Gloucester and
Boston, and Boston prices may lead those of
Gloucester. In any case, it appears that the New
Bedford auction market dominates the formation of
round ex-vessel prices for cod and haddock.
The empirical results for yellowtail and winter
flounder of Table 2 also contradict the null hypoth-
esis that monthly fresh round ex-vessel prices for
both species are formed first in New Bedford. In-
stead, the findings indicate that pricing feedback ex-
ists between both New Bedford and Gloucester and
between New Bedford and Boston. These conclu-
sions must be tempered by the significant Q-test
statistics for several relationships.
These conclusions lead to a second null hypothesis
between the prices of New Bedford and Gloucester,
New Bedford and Boston, and possibly between
Gloucester and Boston rests with a spurious rela-
tionship. Although New Bedford is the most impor-
tant flounder port by landings in New England, New
York City is even more important on the eastern
seaboard by volume of consumption. New York
City's Fulton Fish Market is primarily a wholesale
market without substantial landings. Much of the
New England flounder harvested is sent to Fulton
on consignment without an ex-vessel price being
established in New England. The Fulton Fish
Market also begins much earlier in the morning than
New Bedford's auction market. Thus the apparent
feedback among the ex-vessel yellowtail and winter
flounder prices in the New England ports is prob-
ably due to their following of the wholesale prices
set in the Fulton Fish Market.
Table 3 presents the results for pollock. As with
the other species, consistent results are obtained for
different lag lengths. Again, the null hypothesis dic-
Table 2.— Direct Granger causality tests for monthly fresh round ex-vessel yellowtail and
winter flounder prices.
Yellowtail flounder
Winter flounder
Direction1
Lags2 F-test3 Q-test4
Direction1
Lags2 F-test3 Q-test4
NB
NB
G
G
NB
NB
B
B
G
G
B
B
->G
->G
->NB
->NB
->B
->B
->NB
->NB
->B
->B
->G
->G
8
14
8
14
8
14
8
14
8
14
8
14
2.05*
2.27*
1.96*
2.48*
2.02*
1.76*
0.75
2.83
2.275
2.50s
1.48
1.27
20.19
19.42
23.56*
26.78*
10.56
9.89
17.63
21.83*
9.41
12.74
16.86
18.82
NB
NB
G
G
NB
NB
B
B
G
G
B
B
->G
->G
->NB
->NB
->B
->B
->NB
->NB
->B
->B
->G
->G
8
14
8
14
8
14
8
14
8
14
8
14
7.52*
8.71*
2.88*
2.97*
11.87*
7.66*
23.57*
5.25*
3.875
4.375
4.15s
3.56s
5.68
1.78
16.98
22.19*
18.45
7.92
9.94
3.99
12.43
4.70
18.16
17.34
'Variable abbreviations are B (Boston), G (Gloucester), NB (New Bedford).
2J indicates J months lagged.
3Null hypothesis that past values of the causal variable do not significantly affect current values of the
dependent variable. An asterisk indicates rejection of the null hypothesis at the 5% level.
"Null hypothesis that regression residuals are white noise. An asterisk indicates rejection of the null
hypothesis at the 5% level.
5F-test statistic is significant at the 5% level, but not significant at the 5% level when a Scheffe interval is used.
to be tested on the yellowtail and winter flounder
price linkages between Gloucester and Boston. Since
this test is also an unplanned comparison, a Scheffe
interval is required. Again, the strict test results in-
dicate that neither port's prices lead the other, nor
that feedback exists.
The most probable explanation for the feedback
becomes significant only if it exceeds in magnitude ((a-l]Fh)'k,
where F is the b ■ 100% critical value for F (a-1, N-a) and N is the
number of observations. See Snedecor and Cochran (1976, p. 271)
for more details.
Table 3.— Direct Granger causality tests for monthly fresh round
ex-vessel pollock prices.
Direction1 Lags2 F-test3 Q-test4
B >G 8 4.34* 12.54
B >G 14 4.99* 10.15
G >B 8 5.28* 18.27
G >B 14 4.77* 22.96*
'Variable abbreviations are B (Boston), G (Gloucester), NB (New Bedford).
2J indicates J months lagged.
3Null hypothesis is that past values of the causal variable do not significantly
affect current values of the dependent variable. An asterisk indicates rejec-
tion of the null hypothesis at the 5% level.
"Null hypothesis that regression residuals are white noise. An asterisk in-
dicates rejection of the null hypothesis at the 5% level.
441
FISHERY BULLETIN: VOL. 84, NO. 2
tated by widely held industrial perceptions is re-
jected. The results indicate that feedback exists
between the monthly fresh round ex-vessel prices
of pollock in both Gloucester and Boston. Both ports
dominate pollock landings and are close to one
another.
A complete time series of prices for sea scallops
exists only for New Bedford. Since New Bedford
greatly dominates this fishery by both volume and
value of landings, it may be safely concluded that
monthly round ex-vessel sea scallop prices are
formed in New Bedford. Finally, Gloucester is the
only one of these ports to possess a complete time
series of prices and landings of ocean perch or red
fish. Since Gloucester dominates this fishery,
monthly fresh round ex-vessel ocean perch prices
appear to be formed in this port, at least among
these three.
CONCLUDING COMMENTS
The within-sample bivariate direct Granger
causality tests of monthly round ex-vessel price
linkages for the three most important New England
ports (Boston, New Bedford, and Gloucester) and
the most important groundfish species lead to unex-
pected results. Conventional wisdom considers the
round ex-vessel cod and haddock prices formed in
the Boston auction market to lead the comparable
prices of the other New England ports. However,
the empirical results indicate that New Bedford's
prices lead those of the other ports, although in cer-
tain cases Boston's cod prices may lead those of
Gloucester as well.
The common industry perception also holds that
the yellowtail and winter flounder round ex-vessel
prices are first formed in New Bedford and lead
those of Boston and Gloucester. Instead, the em-
pirical findings suggest that feedback and simul-
taneous price formation occur among all three ports
for both species. Since flounder landings in Boston
and Gloucester are negligible in comparison to those
of New Bedford, a spurious relationship due to the
leading wholesale prices formed in the even earlier
and more flounder-important Fulton Fish Market
of New York City is suggested. Feedback is likely
for fresh round pollock ex-vessel price formation in
Boston and Gloucester. Finally, it is suggested that
the New Bedford auction market dominates fresh
ex-vessel sea scallop price formation and that
Gloucester dominates among these three ports for
ocean perch. New Bedford thus generally dominates
ex-vessel price formation among the major New
England ports for the most important species
harvested.
ACKNOWLEDGMENTS
Helpful comments from David Bessler, Joseph
Mueller, Robert Reidman, Patricia Kurkul, and
DanieJ Huppert and an anonymous reviewer are
gratefully acknowledged.
LITERATURE CITED
Box, G. E. P., and D. Pierce.
1970. Distribution of residual autocorrelations in autoregres-
sive-integrated moving average time series models. J. Am.
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Feige, E. L., and D. K. Pearce.
1980. The casual causal relationship between money and in-
come: some caveats for time series analysis. SSRI Pap. No.
7809, 39 p. Social Syst. Res. Inst., Univ. Wisconsin,
Madison.
Geweke, J.
1981. The approximate slopes of econometric tests. Econo-
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Geweke, J., R. Meese, and W. Dent.
1983. Comparing alternative tests of causality in temporal
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1977. Investigating causal relations by econometric models
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491-504.
442
COMMUNITY STUDIES IN SEAGRASS MEADOWS: A COMPARISON
OF TWO METHODS FOR SAMPLING MACROINVERTEBRATES
AND FISHES1
Kenneth M. Leber2 and Holly S. Greening3
ABSTRACT
r
The effectiveness of using an otter trawl for estimating macrofaunal species ranks and abundances in
seagrass meadows is unknown. In this study, we compare the catch effectiveness of the commonly used
5 m otter trawl with that of a 0.9 m wide epibenthic crab scrape for fishes, decapod crustaceans, molluscs,
and echinoderms, using data from both day and night collections from a northeast Gulf of Mexico sea-
grass meadow. The crab scrape collected significantly more individuals and species of all taxa except (water-
column) fishes. Clear discrepancies existed between trawl and scrape estimates of species ranks and relative
abundances, with trawl collections estimating a higher degree of dominance within groups of shrimps
and demersal fishes, and lower dominance among crabs. Whereas the crab scrape was clearly superior
to the trawl for sampling macroinvertebrates and demersal fishes, the trawl was the better device for
collecting water-column fishes. Explanations for observed differences in the sampling effectiveness of
these gears are discussed. Sampling was considerably more productive at night than during the day. The
combined approach of day-night sampling with both a crab scrape (for demersal fishes and epibenthic
invertebrates) and an otter trawl (for water-column fishes) is recommended for community-wide studies
in seagrass meadows.
Hypotheses concerning ecological community
dynamics should be based upon accurate descriptions
of the habitats and species involved. It is thus essen-
tial that collection methods maximize sampling ef-
ficiency in "community" (sensu Pielou 1977) studies.
Because estimates of species composition, relative
abundances, and biomass in aquatic environments
may vary with different sampling devices (eg., Lewis
and Stoner 1981; Stoner et al. 1983), knowledge of
sample gear effectiveness allows a more rigorous ap-
proach to sampling design and interpretation of
results from studies of aquatic communities.
Seagrass community studies often employ a small,
semiballoon otter trawl (try net) for sampling fishes
and epibenthic invertebrates (Kikuchi 1966; Living-
ston 1975, 1976, 1982; Heck 1976, 1977, 1979; Hooks
et al. 1976; Heck and Wetstone 1977; Weinstein and
Heck 1979; Heck and Orth 1980; Orth and Heck
1980; Ryan 1981; Dugan and Livingston 1982;
Dugan 1983). Although a small otter trawl may be
one of the most effective samplers for estimating
relative abundances of juvenile and small pelagic
Contribution No. 439 of the Harbor Branch Foundation, Ft.
Pierce, FL 33450.
department of Biological Science, Florida State University,
Tallahassee, FL 32306; present address: The Oceanic Institute,
Makapuu Point, Waimanalo, HI 96795.
department of Biological Science, Florida State University,
Tallahassee, FL 32306; present address: Martin Marietta Environ-
mental Systems, 9200 Rumsey Road, Columbia, MD 21045.
Manuscript accepted January 1985.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
fishes in shallow nonvegetated waters (Kjelson and
Johnson 1978; Orth and Heck 1980), there are few
published accounts of its effectiveness in sampling
benthic fishes or epibenthic invertebrates in vege-
tated habitats. Greening and Livingston (1982) noted
that a Chesapeake Bay crab scrape appeared to col-
lect more invertebrate species per sample effort in
vegetated habitats than did an otter trawl. Miller et
al. (1980) found a crab scrape to be more effective
than either an otter trawl or a push net for collect-
ing juvenile blue crabs, Callinectes sapidus, in the
Chesapeake Bay area. Blue crab fishermen routine-
ly use crab scrapes, rather than trawls, in grassbeds
in Chesapeake Bay (Warner 1976).
In this study, the catch effectiveness of a 5 m otter
trawl is compared with that of a 0.9 m epibenthic
scrape in the shallow grassbeds of Apalachee Bay,
FL. Species richness and abundance are examined
within four taxonomic groups (decapod crustaceans,
molluscs, echinoderms, and fishes). Because many
grassbed organisms are more susceptible at night
to certain sampling methods (Ryan 1981; Greening
and Livingston 1982), both day and night samples
are considered.
METHODS
Day and night samples were taken in about 1.7 m
of water from seagrass beds in Apalachee Bay, FL.
443
FISHERY BULLETIN: VOL. 84, NO. 2
The sample site was located 5 km southwest of the
E confirm River mouth (permanent station E-12
(Livingston 1975)). This site is characterized by
relatively uniform, dense stands of the seagrasses,
Thalassia testudinum and Syringodium filiforme,
with seasonal occurrence of red drift algae (mean
annual macrophyte biomass = 320 g dry wt/m2; see
Zimmerman and Livingston 1979 for a description
of macrophytes). Station E-12 was polyhaline, with
salinities during collections ranging from 22 to 30
ppt (x = 27.0 ppt). Water temperatures ranged from
12.0° to 31.0°C (x = 19.9°). Depth varied from 1.6
to 2.1 m. Physical characteristics are summarized
in Table 1.
Table 1.— Physical characteristics of the
sampling station for collection dates,
Apalachee Bay, FL.
Temp.
Salinity
Depth
(°C)
(PPt)
(m)
Jan. 1979
Day
12
31
2.0
Night
10
30
1.8
Apr. 1979
Day
22
23
2.1
Night
21
22
1.6
July 1979
Day
31
25
1.7
Night
30
25
2.1
Oct. 1979
Day
17
30
2.1
Night
16
30
1.7
A 90 cm wide commercial Chesapeake Bay crab
scrape (Miller et al. 1980) was fitted with the cod
end of a 5 m otter trawl (6 mm mesh liner). The crab
scrape was towed at about 1.4 knots for 1 min (after
Greening and Livingston 1982; Leber 1983), yielding
a standardized tow of 42 m (mean of 10 preliminary
measured 1-min tows). A 42 m weighted line was
then used to standardize scrape tows during collec-
tions. A 5 m otter trawl (19 mm mesh wings, 6 mm
mesh liner in the cod end) was towed at the same
speed for 2 min (as in Livingston 1975, 1982; Hooks
et al. 1976; Heck 1977, 1979; Orth and Heck 1980;
Stoner 1980; Stoner and Livingston 1980; Dugan
and Livingston 1982; Dugan 1983), covering an
average measured distance of 84 m. Under tow, the
trawl mouth tickler chain fished a 2.1 m wide path
over the substratum (Leber, pers. obs.). Hence, each
individual trawl tow fished over 4.6 times the sub-
stratum surface area sampled by each tow of the
crab scrape (176 m2 vs. 38 m2). Because the scrape
collected larger amounts of dead vegetation, it was
logistically difficult to sample as much surface area
with it as was sampled by the trawl.
Collections were made quarterly (January, April,
July, and October). On each sampling date eight
scrape and four trawl tows were taken (in the se-
quence two trawls, eight scrapes, two trawls) dur-
ing the day, and again beginning 1 h after dark.
Greening and Livingston (1982) determined that
eight 1-min scrapes were sufficient for sampling
>95% of the species of macroinvertebrates at our
sample site in Apalachee Bay. Because each scrape
was towed for only half the 2-min towing time used
for each trawl (scrape tows lasting longer than 1 min
often resulted in clogging the net with red drift
algae), only four trawls were taken during each sam-
pling period. Thus, the combined length of the eight
scrape tows (8 x 42 m = 336 m) matched that of
the four trawl tows. All samples were collected from
a 0.25 km2 area immediately south of the station
marker. Replicate tows were taken along transects
spaced at least 30 m apart to prevent overlapping
samples.
Organisms were preserved in 10% Formalin4 (buf-
fered with seawater) in the field, then identified,
counted, and measured in the laboratory. A two-way,
Model II, factorial ANOVA design for unequal but
proportional cell sizes (Sokal and Rohlf 1969) was
used to compare mean numbers of species and in-
dividuals of each taxon group in scrape vs. trawl
(Factor 1) and day vs. night (Factor 2) samples.
Log10 transformations were used where F-max
tests indicated heterogeneity of variance Rather
than extrapolating our data to numbers per unit
area, we compared the collections made with these
two gears using absolute numbers per tow in our
calculations (which are biased in favor of the trawl
by a factor of 4.6). We used these absolute abun-
dances because 1) we wanted a strongly conservative
test of our premise that the scrape is the more ef-
fective of these two sample gears in vegetated
aquatic habitats, and 2) we believe that extrapola-
tions of semiquantitative data to abundances per unit
area yield highly unrealistic results, which may be
misinterpreted by readers as accurate densities (cf.
Howard 1984, who determined that a towed beam
trawl was only 4.7% efficient in estimating densities
of shrimp in an Australian seagrass meadow).
RESULTS
Factor 1: Trawl vs. Scrape
Although the surface area sampled by the otter
"Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
444
LEBER AND GREENING: COMMUNITY STUDIES IN SEAGRASS MEADOWS
trawl during each tow exceeded that sampled with
the crab scrape by a factor of 4.6, mean numbers of
individuals collected in scrape samples were signifi-
cantly greater than those in trawl samples in 44%
of the 16 scrape-trawl comparisons (Table 2). The
trawl was a significantly more effective collecting
device for number of individuals of fishes (Table 2;
April, July, and October fishes), but interaction terms
were significant for April and October analyses (see
Interactions, below). Mean numbers of individuals
were greater in trawl, than in scrape, samples in two
other cases (Fig. 1, January and July decapods in
night samples); however, scrape-trawl differences on
those dates were nonsignificant (Table 2). The crab
scrape was clearly the better gear for sampling
epibenthic individuals.
Species numbers were never significantly greater
in trawl, than in scrape, samples (Fig. 1). In contrast,
the crab scrape collected significantly more species
than the trawl in 75% of the scrape-trawl com-
parisons (Table 2). Because the scrape often sampled
greater numbers of individuals than the trawl, the
presence of more species in scrape, than in trawl,
samples may be simply a sampling phenomenon. By
chance alone, one would expect to encounter more
rare species in larger samples. Using rarefaction
analysis (Simberloff 1978), we have factored out the
influence of sample size on species number for a
better comparison of scrape vs. trawl sampling ef-
fectiveness (Fig. 2). Eight of the 12 cases in which
the scrape sampled significantly more species than
the trawl (Table 2) can be attributed to a sampling
phenomenon; there were generally more species in
scrape samples because so many more individuals
were collected in each scrape tow. However, it is clear
in Figure 2 that the greater numbers of decapod
species in January and July scrape samples, and fish
species in April and October scrapes, represent real
differences in the catch effectiveness of these gears
for species within these two taxa.
Factor 2: Day vs. Night
Day-night differences were clear. None of the com-
bined (scrape-trawl) daytime collections contained
significantly more species or individuals than night
collections. But nocturnal samples contained signifi-
cantly more individuals than daytime samples in
69%, and more species in 62%, of the 16 day-night
comparisons (Table 2).
Interactions
Significance of an interaction term indicates
dependence of one factor upon the other; in this case,
when sampling differences between scrape and trawl
exist but are dependent upon time of day. Scrape-
trawl vs. day-night interactions were significant in
8 of the 32 ANOVAs in Table 2. For these eight cases,
either the trawl sampled better only at night for a
certain taxon/month combination (one of the eight
interactions), or the scrape sampled better only dur-
ing the day (five of the eight cases), or both of these
events occurred (two of the eight cases, scrape was
better during the day but the trawl was better at
night).
Although fish were taken in greater abundances
by the trawl on three of the four sampling dates,
interactions were significant on two of those dates
(April and October, Table 2). With the exception of
July collections, fish were equally as abundant in day-
time scrape samples as in trawls (see Figure 1).
Table 2.— Two-way ANOVA, F-values. Underlined values indicate trawl samples significantly larger, all other significant values
are scrape samples. All significant day-night values indicate night significantly larger than day samples.
Decapods
Molluscs
Echinoderms
Fishes
No.
No.
No.
No.
No.
No.
No.
No.
Date
Sample
indiv.
species
indiv.
species
indiv.
species
indiv.
species
Jan.
Day Night
0.48
35.81***
0.02
0.31
0.73
1.22
57.98***
42.14***
1979
Scrape Trawl
0.02
27.77***
56.71***
58.48***
1.92
4.29
0.44
0.08
Interaction
0.00
5.07*
0.01
0.15
1.73
0.03
0.35
0.33
Apr.
Day Night
37.72***
31.16***
63.17***
21.41***
0.00
1.01
103.02***
29.93***
1979
Scrape Trawl
106.26***
68.13***
206.89***
55.30***
111.27***
29.71***
61.55***
27.47***
Interaction
5.24*
0.62
22.51***
2.21
0.51
0.50
68.10***
0.03
July
Day Night
97.55*
139.64***
16.93***
24.75***
6.64*
2.79
14.06**
4.00
1979
Scrape Trawl
4.16
66.94***
70.39***
30.56***
3.06
1.72
6.93*
0.35
Interaction
55.35***
3.67
4.32
0.29
2.57
2.48
0.03
0.09
Oct.
Day Night
7.29*
45.12***
8.03*
20.32***
1.87
3.27
20.36***
5.04*
1979
Scrape Trawl
0.42
32.14***
34.46***
99.21***
10.12**
7.91*
5.04*
9.62**
Interaction
10.63**
0.02
5.01*
1.43
8.28**
3.20
23.85***
0.13
= P < 0.05.
= P< 0.01.
= P< 0.001.
445
FISHERY BULLETIN: VOL. 84, NO. 2
co
—
o
LlI
Q.
CO
16
8
Day
161
8
Night
J A J 0
DECAPODS
Scrape
Trawl
o
UJ
8s
12
6
Night
\r—
"—I -I
J A J 0
MOLLUSCS
co
_i
<
Q
>
CO
UJ
o
UJ
a.
co
J A J 0
ECHINODE RMS
60"
CO
30
Day
| .01
— 30
Night
CO
UJ
o
UJ
a.
CO
8-
Day
4-
T ^-—^**
""■*-
Night
A J
FISHES
0
Figure 1— Mean numbers of individuals and species (±1 SD) collected by the crab scrape (solid
line) and trawl (dashed line) during day and night sampling in January, April, July, and October 1979.
446
LEBER AND GREENING: COMMUNITY STUDIES IN SEAGRASS MEADOWS
150 450 750
Decapods
10
Molluscs Echinoderms
NUMBER OF INDIVIDUALS
Fishes
Figure 2— Rarefaction curves for crab scrape (closed circles) and trawl data (open circles) from 1979 night samples. Expected numbers
of species ( ± 2 SD) are plotted against numbers of individuals. Length of curves indicates maximum number of individuals taken in any
single tow.
Hence, with only one exception (July fish abundance),
the otter trawl never outperformed the scrape dur-
ing daylight collections.
The trawl was more effective in sampling a tax-
onomic group other than fish in only one case Sig-
nificantly more decapod individuals were taken in
July trawl samples at night, reflecting high densities
of two caridean shrimps, Tozeuma carolinense and
Periclimenes longicaudatus, which appear to be
more susceptable to night trawl, rather than scrape,
sampling. However, decapod abundances were
notably higher in July daytime collections made with
the crab scrape (see Figure 1), thus the highly sig-
nificant interaction term for the July analysis
(decapod individuals, Table 2).
Relative Abundance
Numerical rankings of the most abundant or-
ganisms in each taxonomic group (combined over all
sample dates) taken in night scrape samples are com-
pared with those from night trawl samples in Table
3. Clear discrepancies exist between scrape and trawl
estimates of species ranks and relative abundances.
Relative to scrape samples, trawl collections over-
estimated the degree of dominance (DI = combined
proportions of the two most abundant species, {nx
+ n2)/N, McNaughton 1967) contributed by the
most abundant shrimp Tozeuma carolinense and
demersal fish Gobiosoma robustum, and under-
estimated dominance of the most important crab
Pagurus maclaughlinae and mollusc Argopectin ir-
radians in our samples (Table 3). Relative to trawl
collections, the scrape underestimated dominance
for the most abundant water-column fishes, Lagodon
rhomboides and Bairdiella chrysura. Species ranks
of subdominants in trawl samples also differed from
rankings based on data from scrape samples.
DISCUSSION
Scrape-trawl and day-night differences in sampling
effectiveness were conspicuous and generally con-
stant throughout the year. Although more (by a fac-
447
FISHERY BULLETIN: VOL. 84, NO. 2
Table 3.— Species ranks, relative abundances, and dominance for each taxonomic group. Combined night samples, x = mean number
of individuals per sample (per group), Dl = dominance (McNaughton 1967).
Scrape
Trawl
Scrape
Trawl
Relative
Relative
Relative
Relative
Rank
abundance
Rank
abundance
Rank
abundance
Rank
abundance
Shrimp
Molluscs
1
0.324
Tozeuma carolinense
1
0.667
1
0.413
Argopectin irradiens
1
0.383
2
0.157
Penaeus duorarum
4
0.027
2
0.145
Modulus modulus
4
0.118
3
0.143
Periclimenes longicaudatus
2
0.191
3
0.130
Cerithium muscarum
6
0.077
4
0.127
Hippolyte zostericola
3
0.066
4
0.096
Anachis avara
2
0.169
5
0.099
Thor dobkini
6
0.016
5
0.086
Columbella rusticoides
3
0.131
6
0.049
Latreutes fucorum
5
0.018
6
0.064
Turbo castanea
5
0.101
7
0.049
Ambidexter symmetricus
8
0.003
7
0.025
Urosalpinx perrugata
7
0.009
8
0.038
Alpheus normanni
10
0.0002
8
0.013
Nassahus vibex
8
0.006
9
0.009
Palaemon floridanus
7
0.010
9
0.008
Hyalina veliei
—
0
10
0.006
Periclimenes americanus
9
0.001
10
0.007
Fasciolaria hunteri
—
0
X
= 219.98
X
= 423.38
X
= 48.92
X
= 13.32
Dl
= 0.481
Crabs
Dl
= 0.858
Dl
= 0.558
Demersal Fishes
Dl
= 0.501
1
0.735
Pagurus maclaughlinae
1
0.578
1
0.360
Gobiosoma robustum
1
0.544
2
0.117
Neopanope packardii
3
0.101
2
0.291
Opsanus beta
4
0.097
3
0.039
Epialtus dilatatus
4
0.055
3
0.246
Paraclinus fasciatus
2
0.194
4
0.032
Libinia dubia
5
0.048
4
0.086
Centropristis melana
3
0.106
5
0.027
Podochela riisei
6
0.041
5
0.017
Ophidion beani
5
0.058
6
0.026
Metaporaphis calcerata
2
0.133
X
= 7.2
X
= 2.6
7
0.016
Neopanope texana
9.5
0.007
Dl
= 0.651
Dl
= 0.738
8
0.004
Pitho anisodon
9.5
0.007
9
0.003
Pilumnus sayi
7
0.018
Water-Column Fishes
10
0.002
Pilumnus dasypodus
8
0.011
1
0.345
Lagodon rhomboides
1
0.621
X
= 75.1
X
= 10.9
2
0.158
Monacanthus ciliatus
4
0.044
Dl
= 0.852
Dl
= 0.711
3
0.154
Syngnathus floridae
5
0.042
4
0.151
Orthopristis chrysoptera
3
0.099
Echinoderms
5
0.067
Hippocampus zosterae
7
0.007
1
0.659
Echinaster sp.
1
0.824
6.5
0.052
Micrognathus crinigerus
8.5
0.002
2
0.255
Ophiothrix angulata
2
0.176
6.5
0.052
Haemulon plumieri
6
0.013
3
0.056
Lytechinus variegatus
—
0
8
0.015
Bairdiella chrysura
2
0.168
4
0.027
Ophioderma brevispinum
—
0
9
0.004
Monacanthus hispidus
8.5
0.002
X
= 8.42
X
= 5.12
X
= 11.5
X
= 31.7
Dl
= 0.914
Dl
= 1.00
Dl
= 0.503
Dl
= 0.789
tor of 4.6) substratum surface area was sampled per
tow by the otter trawl, the crab scrape collected more
species and individuals per tow, across taxa, with few
exceptions. The trawl was the better faunal collect-
ing gear in this seagrass habitat only for numbers
of individuals of certain water-column fishes and for
two species of caridean shrimps. The scrape was
notably more effective than the trawl (day and night)
for collecting penaeid, alpheid, and processid
shrimps, brachyuran and pagurid crabs, molluscs,
echinoderms, syngnathid fishes, and demersal fishes
(Opsanus, Paraclinus, Gobiosoma, and Centropris-
tis).
The otter trawl appears to collect fewer species
and individuals of demersal animals in grassbeds
than does the scrape because the weighted (tickler)
chain on the trawl is not in contact with the sub-
stratum. Under tow, the cylindrical bottom crossbar
of a crab scrape bends grassblades flat against the
substratum, sweeping demersal and epifaunal
organisms over the bar and into the net, whereas
the otter trawl tickler chain is generally supported
8-10 cm above the substratum by the buoyant vege-
tation (Leber, pers. obs.). Grassblades do not yield
as much to the relatively light weight of a tickler
chain (as they do to a scrape crossbar), and any
organisms remaining close to the substratum as the
chain passes over them evade capture Most epi-
benthic inhabitants of grassbeds, including several
fishes, are more closely associated with seagrasses
and red drift algae than with the water column above
the vegetation or bare patches within beds (Hooks
et al. 1976; Heck and Wetstone 1977; Stoner 1980;
Stoner and Livingston 1980; Gore et al. 1981). The
crab scrape is more effective because it samples
more grassblade surface area, including an addi-
tional microhabitat, the region <10 cm above the
substratum (Leber, pers. obs.).
The greater effectiveness of both devices at night
is probably accounted for, in part, by nocturnal in-
creases in faunal activity on the substratum, on blade
tips, and in the water column above vegetation.
448
LEBER AND GREENING: COMMUNITY STUDIES IN SEAGRASS MEADOWS
Several crustaceans emerge from the substratum
and forage at night in grassbeds, including pink
shrimp, Pendens duorarum, some majid crabs
(notably Pitho and adult Libinia at our site), and
alpheid and processid shrimps (Fuss 1964; Fuss and
Ogren 1966; Hughes 1968; Kikuchi and Peres 1977;
Saloman 1979; Greening and Livingston 1982; Leber
1983). Emergence of nocturnal organisms from the
substratum after dark would explain some of the
variability between day and night collections of in-
vertebrates. Higher densities of diurnally active
animals in night samples may be due to nocturnal
vertical migrations up grass-blades. Animals located
near the tips of blades are clearly more vulnerable
to capture by either device; even the scrape misses
individuals trapped between grass-blades and
substratum by the crossbar, an event less likely to
occur to an individual near a blade tip. Fishes were
probably less abundant in daytime trawl collections
because of avoidance reactions to the clearly visible
net.
Emergence and vertical migration do not account
for all of the increases in invertebrate abundance in
night samples. The case of the arrow shrimp,
Tozeuma carolinense, is interesting in this regard.
We expected no day-night sampling differences for
Tozeuma with either device, based on evidence that
Tozeuma inhabit the region near tips of grass-blades,
both during the day and at night (Main in press). As
expected, Tozeuma were collected in roughly equal
numbers in both day and night scrape samples.
However, almost an order of magnitude more
Tozeuma were taken in night trawl samples than dur-
ing daytime collections (Leber and Greening, unpubl.
data). It appears that Tozeuma may be capable of
avoiding the trawl, which is highly visible during the
day. These shrimp have keen vision in daylight and
are capable of rapid movement (up to 30 cm) via a
caridoid escape response (Main in press). They need
only move down blades, closer to the substratum, to
avoid the trawl net.
This study suggests that many demersal fishes and
epibenthic invertebrates may be more important
numerically in seagrass communities than indicated
by collections made with an otter trawl. Species
ranks and relative abundances of these organisms
determined from trawl collections in seagrass beds
should be interpreted with care Whereas trawl col-
lections may be satisfactory for monthly or year-to-
year comparisons of single species abundances
within a seagrass habitat, application of such data
to examination of predatory-prey relationships (e.g,
energy flow and optimal-diet models) or other biotic
interactions in grassbeds may lead to erroneous
interpretations. The combined approach of day-night
sampling with both an otter trawl (for water-column
fishes) and a crab scrape (for demersal organisms)
is recommended for seagrass studies.
ACKNOWLEDGMENTS
We thank B. J. Freeman, J. Gerritsen, R. Howard,
C. Koenig, F G. Lewis, K. Main, G. Morrison, and
J. Ryan for comments and reviews of earlier drafts
of this manuscript. R. J. Livingston provided
technical support and M. Babineau provided help
with the graphics.
LITERATURE CITED
DUGAN, P. J.
1983. Seasonal and geographic distribution of seven decapod
crustaceans in Apalachee Bay, Florida. Contrib. Mar. Sci.
26:65-79.
Dugan, P. J., and R. J. Livingston.
1982. Long-term variation of macroinvertebrate assemblages
in Apalachee Bay, Florida. Estuarine Coast. Shelf Sci. 14:
391-403.
Fuss, C. M., Jr.
1964. Observations on burrowing behavior of the pink shrimp,
Penaeus duorarum Burkenroad. Bull. Mar. Sci. Gulf Caribb.
14(l):62-73.
Fuss, C. M., and L. H. Ogren.
1966. Factors affecting activity and burrowing habits of the
pink shrimp, Penaeus duorarum Burkenroad. Biol. Bull.
(Woods Hole) 130:170-191.
Gore, R. H., E. E. Gallaher, L. E. Scotto, and K. A. Wilson.
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450
NOTES
A PRELIMINARY INVESTIGATION OF
THE STOCK STRUCTURE OF
THE DOLPHIN, CORYPHAENA HIPPURUS,
IN THE WESTERN CENTRAL ATLANTIC
Dolphin, Coryphaena hippurus, are fast swimming,
migratory, pelagic fish, which support commercial
and sport fisheries throughout the western central
Atlantic (Erdman 1956; Zaneveld 1961; Beardsley
1967; Rose and Hassler 1969; Sacchi et al. 1981;
Olsen and Wood 1982). In terms of weight and
revenue, they are the most important large pelagic
fish landed by the commercial fisheries in the south-
eastern Caribbean (Mahon et al. 1981). In the north-
west, they are the most important sport fish, being
taken on more trips and in greater numbers by
charter boats in Florida (Ellis 1957; Iversen 1962)
and in North Carolina (Hassler and Hogarth 1977;
Rose and Hassler 1969) than any other species.
Rapid expansion of the dolphin fishery fleets is cur-
rently underway in the eastern Caribbean, but the
biological data necessary for management have not
been gathered. For example, we remain ignorant of
the number and distribution of stocks of C. hippurus
in the western central Atlantic.
Regional dolphin fisheries are markedly seasonal
and this presumably results from migration; but
migration patterns remain largely unknown (Palko
et al. 1982). However, Beardsley (1967) believed that
dolphin migrate northwards during spring and sum-
mer, and Gibbs and Collette (1959) suggested that
the spring abundance of C. hippurus in the Carib-
bean may be a prespawning migration, mostly by
females. A preliminary survey of regional catch
records indicates a staggering of the peak fish-
ing seasons, which supports the assumption
that migration is large-scale (Hunte and Mahon
1982).
In the present paper, we take three approaches to
our investigation of C. hippurus in the western cen-
tral Atlantic: 1) We use commercial and sport fishing
data from several countries to examine seasonality
and size structure of catch throughout the region;
2) we compare growth, age/size at sexual maturity,
fecundity, and egg size of dolphin from different
parts of the region; 3) we use electrophoretic tech-
niques to compare dolphin sampled from Miami and
Barbados, two widely spaced fisheries in the region.
Electrophoretic techniques, combined with histo-
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
chemical staining for isozymes, are now widely
recognized as a useful tool for examining genetic af-
finities between fish stocks (Iwata 1975; Allendorf
1979; McGlade 1981; Ihssen et al. 1981; Ferris et al.
1982). By these means, we address the question of
whether the dolphin fisheries in the western central
Atlantic exploit a single stock migrating through the
region or distinct units located in geographically con-
tiguous areas. Resolution of this question will affect
the extent to which individual territories should ex-
pand their dolphin fisheries, will determine whether
management programs need be regional or territory-
specific, and will identify which territories need to
collaborate for joint management of stocks.
Methods
Dolphin monthly catch data, recorded by commer-
cial or sport fisheries, were obtained either by let-
ter, personal visit to fisheries departments, and/or
published literature (Table 1). The catch data, re-
corded as numbers, weights, catch per day or per
boat, and over time periods of 1 to 12 years, were
standardized and plotted as percentages of total an-
nual catch landed each month. Where more than 1
year's data were available, the average catch each
month was calculated.
Tissue samples for the electrophoretic survey were
collected off Barbados between December 1982 and
March 1983, and off Miami in May and June 1983.
Samples of eye, heart, liver, gonad, and white mus-
cle were taken from a total of 1,669 freshly landed
dolphin and were deep frozen for later analysis. A
survey of 22 enzymes encoded by 55 presumptive loci
was conducted to identify polymorphic enzyme
systems. The allelic frequencies of the highly poly-
morphic isocitrate dehydrogenase, Idh-2, locus were
compared in Miami and Barbados dolphin. The
horizontal starch gel electrophoresis methodology
follows that of May et al. (1979) and McGlade et al.
(1983). Allelic nomenclature follows that of Allen-
dorf and Utter (1979).
Life history data were obtained from the literature,
from records of length and weight of specimens
caught in the Bahamas, Bermuda, and North
Carolina, and from our own studies of 624 dolphin
landed during the peak of the sport fishery in Miami
and 3,126 dolphin landed by the commercial fishery
in Barbados.
451
Table 1.— Countries from which catch data on the dolphin, Coryphaena hippurus, were obtained, with the data source for each country.
Territory
Data source
Time period
Territory
Data source
Time period
Curacao
Zaneveld (1961)
1957-58
Puerto Rico
Erdman (1956)
1951-56
Grenada
J. Finlay, Fisheries Officer,
Ministry of Agriculture, National
Resources and Industrial
Development, St. George's,
1981-83
0. Munoz-Roure, Executive
Director, Caribbean Fisheries
Management Council, Hato Rey,
Puerto Rico.
Grenada.
Bahamas
P. Major, Fisheries Biologist,
1976, 1978
St. Vincent
K. Morris, Fisheries Officer, Min-
istry of Agriculture and Fish-
eries, Kingstown, St. Vincent.
1975-81
Ministry of Agriculture, Fisheries,
and Local Government, Nassau,
Bahamas.
Barbados
R. Hastings and P. McConney,
Fisheries Officers, Fisheries
Division, Bay Street, Bridge-
1973-82
Florida
A. Jones, Fisheries Scientist,
Southeast Fisheries Center,
NMFS, NOAA, Miami, Florida.
1970-80
town, Barbados.
Fable et al. (1981)
1971-79
St. Lucia
P. Murray, Fisheries Biologist,
1978,
Georgia
A. Jones, see Florida
1978-79
Ministry of Agriculture, Lands,
1980-82
South Carolina
A. Jones, see Florida
1976-80
Fisheries, and Cooperatives,
Fisheries Division, Castries, St.
North Carolina
A. Jones, see Florida
1978-80
Lucia.
Manooch and Laws (1979)
1977
Martinique and
Rose and Hassler (1969)
1961
Guadeloupe
Sacchi et al. (1981)
1980
Bermuda
B. Luckhurst, Fisheries Officer,
1973-80
Virgin Isles
R. Wood, Fisheries Biologist,
Department of Conservation and
Cultural Affairs, Division of Fish
and Wildlife, St. Thomas, Virgin
Islands.
Olsen and Wood (1982)
1967-78
Ministry of Fisheries and
Agriculture, Naval Base,
Southampton, Bermuda.
RESULTS AND DISCUSSION
Seasonality and Size Structure
of Catch
The seasonality of dolphin catch in 14 territories
is shown in Figure 1. Martinique and Guadaloupe
supplied no data, but information was given on the
duration and peak of the dolphin season. It should
be noted that the U.S. Virgin Islands is the only ter-
ritory with a distinctly bimodal catch pattern.
The peak months of catch in each territory are
superimposed on a map of the western central Atlan-
tic in Figure 2. Grenada peak catch is in February/
March; Barbados, St. Vincent, and St. Lucia in
March/April; Martinique and Guadeloupe in April;
and the Virgin Islands in April/May, giving the
Virgin Islands their first and largest annual peak.
This pattern of catch seasonality is suggestive of a
stock (subsequently called the southern stock)
moving northwest through the island arc. If the
stock then turned west and moved past Puerto Rico,
we would expect peak catch there to be between
June, July, and August; but this is when Puerto Rico
catches the least dolphin (see Figure 1). We therefore
suggest that, on leaving the Virgin Islands, the stock
moves northeasterly into the Atlantic, completing a
circuit and returning to Grenada by February/March
of the following year. This implies that there is a sec-
ond stock (subsequently called the northern stock)
located in the northwest region of the western cen-
tral Atlantic. It occurs near Puerto Rico between
December and February. It next moves northwest-
erly past the Bahamas in April/May Florida and
Georgia in May/June, South and North Carolina in
June/July and Bermuda in July/August. It then com-
pletes its circuit by passing through the Virgin
Islands, giving that territory its second and smaller
peak in November and returning to Puerto Rico by
December/February.
The mean size of fish caught in five territories dur-
ing peak fishing season is shown in Figure 3, and
the size structure of the catch throughout the fishing
season in Barbados is shown in Figure 4. The data
are consistent with the migration circuits proposed.
In the northern stock, small presumably young-of-
the-year fish are predominant during the summer
when the stock is near Florida, North Carolina, and
Bermuda. The mean size taken by the sport fishery
in Florida is 1.69 kg; in North Carolina, where they
occur 1 mo later, it is 2.92 kg and in Bermuda, where
they occur 2 mo later, it is 3.85 kg. These differences
presumably reflect growth within the cohort. The
largest fish are taken by Puerto Rico, where Erd-
man (1956) reported that dolphin up to 23 kg in
weight occur during the peak winter fishing season,
and by the Bahamas where the mean weight during
the peak fishing months is 6.45 kg. This suggests
452
40 -
20 -
40
20
>-
o
a
LU
a:
LL.
6-S
40
20
40
40
20
CURACAO
GRENADA
ST, VINCENT
BARBADOS
ST. LUCIA
MARTINIQUE &
GUADELOUPE
US VIRGIN ISLES
PUERTO RICO
RGIA
SOUTH CAROLINA
NORTH CAROLINA
BERMUDA
J F M A M J J A S O N D
JFMAMJJASOND
i — i — i — i — i — i — i — i — i — i — i — r
JFMAMJJASOND
MONTHS
Figure 1.— Seasonality of the dolphin, Coryphaena hippurus fisheries in the western central Atlantic, shown in geographical order from
south to north. Note that raw catch data were not available from Martinique and Guadeloupe, but the duration of season and peak month
were known.
453
ATLANTIC
OCEAN
Figure 2— Months of peak catch of the dolphin, Coryphaena hippurus, and proposed migration circuits for northern and southern dolphin
stocks in the western central Atlantic. Letter symbols (eg., A-M) indicate months of peak catch. M^t indicate proposed migration.
i S indicate proposed migration where catch data were not available • indicate locations from which samples for electrophoresis
were collected.
continued growth of the cohort as it leaves Bermuda
and returns southwards into the northern Caribbean
for the winter. Note that since dolphin are serial
spawners and since fecundity is proportional to size
(Beardsley 1967; Oxenford and Hunte in press), most
spawning by a cohort will occur when the dolphin
comprising it are large For the northern dolphin,
this would be when the stock is near Puerto Rico,
i.e, at the southeastern or up-current limit of their
range Peak spawning near Puerto Rico is reported
to occur in early spring (Erdman 1976) and presum-
ably produces the small young-of-the-year fish caught
near Florida during the summer.
The size structure of dolphin caught at Barbados
(Fig. 4) is consistent with the proposed migration
for the southern stock. In February, the main cohort
is composed of fish about 5V2 mo old with a mean
standard length of 812.24 mm. Growth within this
cohort occurs throughout the fishing season to June,
when the average fish size is 1,007.83 mm SL (Oxen-
ford and Hunte 1983). After this, abundance drops
sharply (Fig. 1) as the cohort leaves Barbados
10 -,
en
u
s
6 -
2 -
BARBADOS
FLORIDA NORTH BERMUDA BAHAMAS
CAROLINA
Figure 3— Mean weights of individuals of the dolphin, Coryphaena
hippurus, landed during peak fishing seasons at five locations in
the western central Atlantic.
migrating northwards. During early summer (June/
July) and early autumn (October), the presence of
454
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V
o
h
O)
Q.
J3
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01
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1
a.
0/
3
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o
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a) ■£
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k. r.
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t5 SB
e8 5
M &s
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1*3
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AONBnoayd %
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455
a few very small dolphin (<2% of the annual catch
by weight), landed as bycatch of the flying fish
fishery (see Figure 4), indicates the arrival of the
first of the young-of-the-year group, with a few very
large mature adults from the previous year. Note
that many of these young-of-the-year are already
mature on reaching Barbados in November, and all
are ripe by the time the cohort leaves Barbados in
June Note too, that aging of the cohort (Oxenford
and Hunte 1983) suggests that the cohort was
spawned between September and January, when the
parent stock would be towards the southeastern, up-
current extreme of the proposed migration circuit.
Life History Comparisons
Data on life history parameters of dolphin from
northern and southern circuits are summarized in
Table 2.— Life history characteristics of the dolphin Coryphaena hippurus in the western central Atlantic.
Life history characteristics
Location
Data Source
Northern area:
Average 1st year growth
k 1.64
N. Carolina
Rose and Hassler (1968)
rate (mm SL/d)
= 1.82
Florida
Beardsley (1967)
Length-weight relationship
Males:
in the form y = ax6
y = 0.05
X
10
-8 ^.75
N. Carolina
Rose and Hassler (1968)
(y is weight (kg)
y ~ 1 .45
x ■
10
-7^.58
Florida
Beardsley (1967, fig. 7)
x is SL (mm))
Females:
y = 1.27
X
10
-7x2.59
N. Carolina
Rose and Hassler (1968)
y ~ 5.75
x •
10
-8 ^.71
Florida
Beardsley (1967, fig. 7)
Fecundity-length relationship
y = 2.52 x
10
-4
K312
Florida
Beardsley (1967, fig. 11)
in the form y = ax*3
(y is mature egg numbers
x is FL (mm))
Size at first maturity
Males: I
393
(mm SL)
Females !
324
Florida
Beardsley (1967)
Age at first maturity
« 6-7
Florida
Beardsley (1967)
(months)
Mature egg size range
1-1.7
Florida
Beardsley (1967, fig. 9)
(mm diameter)
Mean mature egg size
1.3
N. Carolina
Hassler and Rainville
(mm diameter)
(1975)
Spawning season
Extended
Atlantic
Florida
Current
Shcherbachev (1973)
Fahay (1975)
Johnson (1978)
Gibbs and Collette (1959)
Beardsley (1967)
Age structure
(% which are <2 yr)
96
98
N. Carolina
Florida
Rose and Hassler (1968)
Beardsley (1967)
Southern area:
Average 1st year growth
= 4.17
Barbados
Oxenford and Hunte
rate (mm SL/d)
(1983)
Length-weight relationship
Males:
in the form y = ax*3
y = 1.24
X
10
-8 ^.94
Barbados
Oxenford and Hunte
(y is weight (kg)
Females:
(in press)
x is SL (mm))
y 2.22 x
10
-8
x284
Fecundity-length relationship
in the form y = ax6
y = 2.7 x
10
-6
x367
Barbados
this study
(y is mature egg numbers
x is FL (mm))
Size at first maturity
Males:
735
Barbados
this study
(mm SL)
Females:
610
Age at first maturity
ss 4
Barbados
this study
(months)
Mature egg size range
0.86-1.00
Barbados
this study
(mm diameter)
Mean mature egg size
0.97
Barbados
this study
(mm diameter)
Spawning season
Extended
Barbados
this study
Age structure
100
Barbados
Oxenford and Hunte
(% which are <2 yr)
(1983)
456
Table 2 and are not supportive of a single stock
hypothesis. Dolphin in Barbados waters appear to
grow faster (Oxenford and Hunte 1983) than those
in North Carolina (Rose and Hassler 1968) and
Florida (Beardsley 1967). Note that scale annuli are
found in northern dolphin but not in southern
dolphin; a difference supportive of the assertion that
the two groups are distinct. Beardsley (1967) sug-
gested that the formation of the dolphin scale an-
nuli at Florida was correlated with the temperature
reduction occurring in the Florida Current during
winter.
Dolphin from Barbados are larger but younger at
first sexual maturity than those from Florida.
Fecundity increases with fish size in both groups, but
Florida dolphin have higher fecundity at size than
Barbados dolphin (Oxenford and Hunte in press).
Mature eggs taken from Florida and North Carolina
dolphin are apparently larger than those from Bar-
bados dolphin. Intraspecific variation in egg size is
seldom environmental and is typically a function of
fish age (Bagenal 1971; Kazakov 1981). Mature egg
size does not increase with fish size/age for Barbados
dolphin (linear regression, r = 0.353 b = 0.0001).
Therefore, assuming that the differences observed
in egg size of southern and northern dolphin do not
result merely from differences in investigators'
methodologies, they are suggestive of separate
stocks as shown for different spawning groups of
herring (Blaxter and Hempel 1963; Cushing 1967)
and sockeye salmon (Foerster 1968; Bagenal 1971).
Electrophoretic Comparisons
In the electrophoretic survey, 55 presumptive loci
could be consistently scored. Of these, 39 were fixed
for the same alleles in both samples, and a further
12 were close to fixation. Two isocitrate dehydro-
genase loci (Idh-2,3) and two esterase loci (Est-1,2)
had alternate alleles at a frequency >0.05, i.e. were
significantly polymorphic
Seven phenotypes were observed at the Idh-2 locus
expressed in heart tissue (Fig. 5). The pattern of ac-
tivity at this locus is typical of an active dimeric en-
zyme with disomic inheritance (Darnall and Klotz
1972; Kirpichnikov 1981) and four alleles with
relative mobilities to 100, 123, 86, and 68. Thus,
putative genotypes could be assigned to the observed
phenotypes as indicated in Figure 5, and allelic fre-
quencies calculated (Table 3). Unequivocal assigna-
tion of genotypes to the phenotypes, observed at the
remaining polymorphic loci, was not possible in the
absence of inheritance data, since the loci have alleles
with overlapping mobilities. Idh-3 and Idh-2, ex-
pressed together in liver tissue, both have alleles with
relative mobilities to 100, 123, and 86, and although
the asymmetrically banded phenotypes could be
easily read, the presence of a null allele at Idh-3
meant that certain phenotypes could have been pro-
duced by a number of different genotypes. Est-1 and
Est-2 share all or some of four alleles, but the band-
ing intensity ratios of individual phenotypes could
not be determined. Hence, assignation of genotypes
to phenotypes at these loci was not possible In sum-
mary, only the Idh-2 locus, expressed indepen-
dently from Idh-3 in heart tissue, was considered
suitable for a comparison of Miami and Barbados
dolphin.
The frequencies of alleles at Idh-2 differed signifi-
cantly in the two populations (chi-square 2x4 con-
tingency test: x2 = 12.725, df = (r - 1) (C - 1) =
3, 0.01 > P > 0.0005; Table 3). Note that the varia-
CO
I—
Q
O
£ 123 _
o
+
100
86
68 — '
PHENOTYPE
ca
o
123/123 100/100 86/86 123/100 100/86 123/86 100/68
(1) (1) (1) (1-2-1) (1-2-1) (1-2-1) (1-2-1)
GENOTYPE
BANDING
INTENSITIES
Figure 5.— A starch-gel zymogram of the dimeric enzyme isocitric dehydrogenase, showing
the phenotypes observed and putative genotypes at the Idh-2 locus in heart extracts of the
dolphin, Coryphaena hippurus, from the western central Atlantic. Values in parentheses are
ratios of allele products.
457
Table 3— Observed allelic frequencies (obs. freq.) and number (obs. no.) of alleles
at the ldh-2 locus in heart tissue of the dolphin, Coryphaena hippurus. from Miami
and Barbados. Expected values (exp. no.) refer to the number expected if the
samples do not differ.
Sample
location
No. of
fish
539
Alleles
68
86
100
123
Miami
obs. freq.
0.0009
0.3154
0.6660
0.0176
obs. no.
1
340
718
19
exp. no.
(0.47)
(304.14)
(751.56)
(21.83)
Barbados
597
obs. freq.
0.0000
0.2521
0.7253
0.0226
obs. no.
0
301
866
27
exp. no.
(0.53)
(336.86)
(832.44)
(24.17)
tion observed at ldh-2 did not differ from that
predicted under Hardy-Weinberg equilibrium for
either population (chi-square goodness of fit: for Bar-
bados, x2 = 6.337, df = 3, 0.25 > P > 0.1; for Miami,
X2 = 9.9145, df = 6, 0.25 > P > 0.1; Table 4).
The differences in life history traits of Miami and
Barbados dolphin could in principle be environmen-
tal. The genetic differences observed at the ldh-2
locus suggest that there may be little gene flow be-
tween the northern and southern groups; but could
in theory result from a regional cline. The primary
evidence supporting our suggestion of more than one
dolphin stock in the western central Atlantic is there-
Table 4.— The number of each phenotype observed (obs.)
at the ldh-2 locus in heart tissue of the dolphin, Coryphaena
hippurus, from Barbados and Miami. Expected values (exp.)
refer to the numbers expected if the populations are in
Hardy-Weinberg equilibrium.
Sample
location
Putative
genotype for
ldh-2
Barbados
(n = 597)
Miami
(n = 539)
86/86
obs.
47
64
exp.
(37.94)
(53.62)
100/86
obs.
199
205
exp.
(218.31)
(226.46)
100/100
obs.
325
251
exp.
(314.05)
(239.11)
100/123
obs.
17
10
exp.
(19.58)
(12.65)
123/123
obs.
1
1
exp.
(0.31)
(0.17)
123/86
obs.
8
7
exp.
(6.81)
(5.99)
68/68
obs.
0
exp.
(0.00)
100/68
obs.
1
exp.
(0.67)
123/68
obs.
0
exp.
(0.02)
86/68
obs.
0
exp.
(0.32)
fore the seasonality of catch data and the mean size
of dolphin landed in each territory. Taken together,
the three data sets certainly suggest that the
assumption of a single stock may be unjustified. Ef-
forts should now be made to test the two stock
hypothesis proposed and to investigate the possible
presence of additional dolphin stocks, particularly
in the western Caribbean Sea and in the Gulf of
Mexico.
Acknowledgments
This project was supported by an Inter-University
Council (British Council) grant to Hazel Oxenford,
a University of the West Indies research grant to
Wayne Hunte and a Manual Noreiga Morales Science
Prize from the Organization of American States to
Wayne Hunte. The electrophoresis was carried out
at the Bedford Institute of Oceanography, Dart-
mouth, Nova Scotia, with technical supervision by
J. McGlade, and C. Annand, and with technical
assistance from D. Beanlands. We thank C. Limouzy
for collecting specimens in Miami, R. Mahon for
assistance in compiling regional catch records, and
J. Horrocks and J. Marsden for comments on the
manuscript. Cooperation of fisheries officers and
fisheries biologists in the region is gratefully
acknowledged.
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Hazel A. Oxenford
Department of Biology
459
University of the West Indies
Cave Hill Campus, P.O. Box 6U
Barbados, West Indies
Bellairs Research Institute
ofMcGill University
St. James
Barbados, West Indies
ascent in the early morning and maintenance of a
deeper distribution at night. This pattern was similar
to that observed by Kiefer and Lasker (1975) for this
Wayne Hunte species in the Gulf of California. Vertical chlorophyll
a profiles indicated the cells rose in the morning and
descended in the evening. The present study was
undertaken to measure swimming speeds of G.
splendens under different temperature conditions.
The observed speeds vary with temperature and are
similar to those calculated from field studies.
EFFECTS OF TEMPERATURE ON
SWIMMING SPEED OF THE DINOFLAGELLATE
GYMNODINIUM SPLENDENS
Dinoflagellate blooms or red tides frequently occur
in a stratified water column having low nutrients
near the surface (Huntsman et al. 1981). Under these
conditions dinoflagellates have a competitive advan-
tage over other phytoplankton due to their motility
and diel vertical migration pattern. In the absence
of turbulence, active swimming allows them to over-
come sinking and thereby, remain close to the sur-
face The normal diel vertical migration consists of
an ascent to some minimum depth during the day
and descent to a maximum depth at the night
(reviewed by Forward 1976). Through this pattern
they have access to nutrients over the area covered
by migration and they can migrate to the surface
during the day to obtain more light for photosyn-
thesis (Ryther 1955; Margalef 1978; Huntsman et
al. 1981).
The success of dinoflagellates depends to a great
extent upon their swimming capability. There have
been few measurements of actual swimming speeds
of individual dinoflagellates (eg., Hand et al. 1965)
or estimates of speeds from population movements
during migration (Eppley et al. 1968; Kamykowski
and Zentara 1977). This is unfortunate because such
measurements are necessary to estimate the depth
of the water column available to dinoflagellates for
nutrients during migration.
The most pronounced and widespread dinoflagel-
late blooms off the coast of Peru are caused by Gym-
nodinium splendens Lebour. Blooms occur most
frequently during the summer and are usually asso-
ciated with the phenomenon of El Nino (Rojas de
Mendiola 1979). At the beginning of the 1976 El
Nino, there was a major bloom of G. splendens.
Blasco's (1979) surface measurements during this
bloom indicated the dinoflagellate vertically
migrated with the suggested pattern involving an
Materials and Methods
The dinoflagellate Gymnodinium splendens
Lebour was cultured as described previously (For-
ward 1974) in a Sherer1 environmental chamber
(Model CEL-44) on a 14:10 LD cycle at a salinity of
about 34 ppt. All experiments were performed in the
middle 4 h of the light phase with cultures having
densities of about 2,000 cells/mL. This cell density
was used because it was similar to that used in past
studies (Forward 1974, 1977) and thus past results
can be applied to the present study. Swimming speed
during phototaxis was only measured during a
specific time interval because there is a circadian
rhythm in phototaxis (Forward 1974). Gymnodinium
splendens shows about average levels of phototaxis
during the middle 4 h of the light phase It is not
known whether there is a similar rhythm in swim-
ming.
Subcultures were exposed to two sets of temper-
ature conditions to test for the effects of 1) tem-
perature acclimation and 2) acute temperature
changes upon swimming speed. In the first tests cells
were acclimated to selected temperatures from 13°
to 25 °C for at least 5 d prior to swimming speed
measurements. These temperatures were used
because they encompass the range in which the cells
grow at reasonable rates (Thomas et al. 1973). For
the second tests, cultures were acclimated to 19°C
for at least 5 d. At the time of testing cultures were
exposed to an acute temperature change by placing
the flasks in a water bath set at selected tempera-
tures for 0.5 h, after which time swimming speed
was measured. Room lights were on during this 0.5-h
period. The temperature of the room in which swim-
ming was measured was regulated to approximate-
ly each test temperature Each test was performed
on four separate subscultures.
To measure swimming speeds, a sample of cells
was removed from a subculture and placed in a clear
1 Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
460
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
cuvette The cells were viewed by the closed circuit
video system described by Forward (1974). During
random swimming the cells can move in any direc-
tion and are not necessarily moving in the plane of
view of the video camera. Thus measurements of
swimming speeds during random swimming tend to
underestimate true speed. To prevent this problem,
cells were stimulated horizontally with light and
speed measured during oriented swimming toward
the light (positive phototaxis). Room lights were off
during light stimulation.
The light stimulus was a tungsten light source
filtered with a 4-96 Corning filter. The spectral com-
position of the light was similar to the spectral sen-
sitivity of phototaxis of G. splendens (Forward 1974).
A constant light intensity of 4.79 x 102 Wm~2, as
measured with an EG and G radiometer (Model 550)
and calculated at 465 nm, was used for all tests
because maximum positive phototaxis occurs in this
intensity range, and it was necessary to measure
swimming speed during phototaxis. Swimming was
recorded on video tape and speed analyzed using
previous techniques (Forward 1974).
Results
Swimming speed varied greatly with temperature
(Fig. 1) as mean speeds approximately double upon
acclimation to temperatures between 13° and 25 °C
(0.56 h_1 to 1.16 mh_1). The dinoflagellate seems
capable of limited temperature acclimation. If the
cells were acclimated to 19°C and suddenly exposed
to other temperatures, there was always a signifi-
cant difference (Student's t test; P < 0.001) between
these mean speeds and those upon acclimation. At
a lower temperature of 13 °C the acclimation speed
was higher; while at temperatures above 19 °C, the
acclimation speeds were lower. This trend is expected
with acclimation.
The effects of temperature can be further assessed
by calculating the temperature coefficients upon ac-
climation and exposure to acute temperature
changes (Table 1). The Q10 values for acute changes
are always higher than those upon acclimation, which
is expected if swimming rates are adjusted through
acclimation. When acclimated to temperatures be-
tween 13° and 19°C, the cells showed total compen-
sation (Q10 = 0.98). In contrast, they were less able
to adjust their rates upon acclimation to higher tem-
peratures between 19° and 25°C (Q10 = 3.42). Par-
tial acclimation occurred over this temperature
Table 1.— Temperature coefficient values for the
dinoflagellate Gymnodinium splendens upon tem-
perature acclimation and exposure to acute
changes in temperature.
Temperature
range
Acute
Q10
Acclimation
Q10
13°-19°C
19°-25°C
1.47
4.68
0.98
3.42
13 15 17 19 21 23 25
Temperature (°C)
Figure 1.— Swimming speeds of the dinoflagellate Gymnodinium
splendens upon acclimation to various temperatures (solid line). The
effect of acute temperature change was measured by acclimating the
animals to 19°C and measuring speeds upon exposure to other
temperatures (dashed line). The number beside the points are the sam-
ple sizes and the vertical bars are standard errors.
461
range since the acclimation Q10 is lower than the
acute Q10 (Table 1).
levels can affect migration patterns (Kamykowski
1981).
Discussion
Blooms of G. splendens occur off the coast of Peru
in temperatures ranging from 17° to 23 °C with op-
timum being 18°-21°C (Rojas de Mendiola 1979).
The lower temperature agrees with laboratory
measurements of vertical migration, as Kamykowski
(1981) found migration in the laboratory occurred
at temperatures above 16°C. In the laboratory, this
dinoflagellate can survive and divide at temperatures
from 12° to 29°C. The most rapid growth rates (0.4
divisions/d), however, occur at 20°-27°C (Thomas et
al. 1973). Within the optimum temperature range
suggested from these studies (18°-26°C), swimming
speed of G. splendens approximately doubles (Fig.
1). These speeds and their change with temperature
are similar to those reported for other dinoflagellate
species (Hand et al. 1965).
The speeds of movement calculated from field
studies of vertical migration of G. splendens agree
with the speeds found in the present study. Blasco
(1979) calculated that a speed of 1 m/h was sufficient
to account for the migration off Peru during the 1976
El Nino. In the Gulf of California, G. splendens
migrated over a depth of about 9 m and had a
calculated descent velocity at sunset of 1.7 m/h
(Kiefer and Lasker 1975). The present study pre-
dicted this speed would occur at temperatures above
25°C. Unfortunately Kiefer and Lasker (1975) did
not state the water temperature at the time of
migration.
An objective of the present study was to use the
measured swimming speeds to determine the
distance over which G. splendens should be capable
of migrating. A conservative estimate of distance can
be calculated from the speeds upon acclimation to
optimum temperatures (19°-25°C) and assuming the
dinoflagellate 1) swims continuously in either the up-
ward or downward direction for half of the migra-
tion cycle (12 h) and 2) does not have a diel rhythm
in swimming speed. At 19°, 22°, and 25°C the cal-
culated distances are 6.6, 11.3, and 13.9 m respec-
tively. These distances would increase slightly if a
temperature gradient existed because speed is ap-
proximately constant at 19°C and lower tempera-
tures, and acute exposure to higher temperatures,
which would occur high in the water column, would
elevate speeds above those upon acclimation (Fig. 1).
In addition, these values would probably vary if G.
splendens is exposed to different environmental con-
ditions, since salinity, light intensity, and nutrient
Acknowledgments
This work was supported by an International
Oceanographic Commission travel grant to BRM and
a National Science Foundation Grant No. OCE-
8110702.
Literature Cited
Barber, R. T., and F. P. Chavez.
1983. Biological consequences of El Nino. Science 222:1203-
1210.
Blasco, D.
1979. Changes in surface distribution of a dinoflagellate bloom
of the Peru coast related to time of day. In D. L. Taylor and
H. H. Seliger (editors), Toxic dinoflagellate blooms, p. 209-
214. Elsevier, N.Y.
Eppley, R. W., O. Holm-Hansen, and J. D. H. Strickland.
1968. Some observations on the vertical migration of dino-
flagellates. J. Phycol. 4:333-340.
Forward, R. B., Jr.
1974. Phototaxis by the dinoflagellate Gymnodinium
splendens Lebour. J. Protozool. 21:312-315.
1976. Light and diurnal vertical migration: photobehavior and
photophysiology of plankton. In K. Smith (editor), Photo-
chemical and photobiological reviews, Vol. 1, p. 157-209. Ple-
num Press, N.Y.
1977. Effect of neurochemicals upon a dinoflagellate photo-
response J. Protozool. 24:401-405.
Hand, W. C, P. A. Collard, and D. Davenport.
1965. The effects of temperature and salinity change on swim-
ming rate in the dinoflagellates, Gonyaulax and Gyrodi-
nium. Biol. Bull. 128:90-101.
Huntsman, S. A., K. H. Brink, R. T. Barber, and D. Blasco.
1981. The role of circulation and stability in controlling the
relative abundance of dinoflagellates and diatoms over the
Peru shelf. Coastal Upwelling Coast Estuarine Sci. 1:357-
365.
Kamykowski, D.
1981. Laboratory experiments on the diurnal vertical migra-
tion of marine dinoflagellates through temperature gradients.
Mar. Biol. (Berl.) 62:57-64.
Kamykowski, D., and S. J. Zentara.
1977. The diurnal vertical migration of motile phytoplankton
through temperature gradients. Limnol. Oceanogr. 22:148-
151.
Kiefer, D. A., and R. Lasker.
1975. Two blooms of Gymnodinium splendens, an unarmored
dinoflagellate Fish. Bull., U.S. 73:675-678.
Margalef, R.
1978. Life-forms of phytoplankton as survival alternatives in
an unstable environment. Oceanol. Acta 1:493-509.
Rhyther, J. H.
1955. Ecology of autotrophic marine dinoflagellates with
reference to red water conditions. In F. H. Johnson (editor),
The luminescence of biological systems, p. 387-414. Am.
Assoc Adv. Sci., Wash., D.C.
Rojas de mendiola, B.
1979. Red tide along the Peruvian coast. In D. L. Taylor and
H. H. Seliger (editors), Toxic dinoflagellate blooms, p. 183-190.
462
Elsevier, N.Y.
Thomas, W. H., A. N. Dodson, and C. A. Linden.
1973. Optimum light and temperature requirements for Gym-
nodinium splendens, a larval fish food organism. Fish. Bull., U.S.
71:599-601.
Richard B. Forward, Jr.
Duke University Marine Laboratory
Beaufort, NC 28516-9721
and
Zoology Department, Duke University
Durham, NC 27706
Blanca Rojas de Mendiola
Instituto del Mar del Peru
P.O. Box 22, Callao, Peru
Richard T. Barber
Duke University Marine Laboratory
Beaufort, NC 28516-9721
MORPHOLOGY AND
POSSIBLE SWIMMING MODE OF A
YELLOWFIN TUNA, THUNNUS ALBACARES,
LACKING ONE PECTORAL FIN
In September of 1982, the Mexican bait boat, Paesa,
fishing off Baja California, captured a 36.5 cm fork
length (861.2 g wet weight) yellowfin tuna, Thunnus
albacares, that lacked a left pectoral fin (Fig. 1). The
fish was frozen and was brought to the Inter-Ameri-
can Tropical Tuna Commission, La Jolla, CA, for
study by W. H. Bayliff.
Pectoral fins provide virtually all hydrodynamic lift
in scombrids and are essential for stable and effi-
cient swimming at sustained speeds (Magnuson
1973, 1978). A specimen with only one pectoral fin
raises questions on what ways the fish might have
compensated for an asymmetrical decrease in hydro-
dynamic lift and how the presence of only one pec-
toral fin might have affected its locomotion. We ex-
amined the fish to determine what may have caused
fin loss and whether morphology was noticeably
altered in a manner suggesting some compensation.
Skin in the area where the left pectoral fin should
have been was thin, smooth, and silvery in appear-
ance (Fig. 1). There was neither a trace of pectoral
fin remnants nor a skin groove for it, suggesting the
fin had never formed. On the other hand, the ap-
pearance of the skin and the presence of variably
sized scales in the area around the normal fin posi-
tion is compatible with a healed wound, and we thus
could not rule out the possibility that the fin had been
bitten off cleanly.
Methods
The specimen was X-rayed and maximum body
height and width measured. We measured and
traced its median fins, caudal keel, pectoral fin, and
both pelvic fins, and estimated their surface areas
with a planimeter. The same body and fin measure-
ments were made on similarly sized, preserved
yellowfin tuna in the Scripps Institution of Ocean-
ography Fish Collection (SIO). Morphometric data
were compared with values derived from the litera-
ture (Gibbs and Collette 1967; Fierstine and Walters
1968; Magnuson 1973, 1978; Magnuson and Wein-
inger 1978, app. II). Although some of the specimen's
caudal rays were bent (Fig. 1), all rays were present,
and the fin was extended to a more natural position
before its span was measured and area (which was
well defined) traced. Also, to avoid measurement er-
rors noted by Fierstine and Walters (1968) and
Magnuson (1978), care was taken not to overextend
caudal fins during span measurement.
Density of the thawed fish was determined by
water displacement (density = wet weight/displace-
ment volume). The right and left pectoral girdles
were then removed and the gas bladder was in-
spected. Transverse sections were cut (see Graham
et al. 1983), concentric myotomal rings on the right
and left sides were counted, and red and white
muscle were weighed for each section.
Results
The abundance of comparative morphometric and
anatomical data for the yellowfin tuna permits a
nearly complete assessment of the morphologic and
hydrodynamic status of the one-finned specimen.
The length (L; 36.5 cm)/weight (861.2 g) relationship
and the density (1.080 g-mL-1) agree with values
published for yellowfin tuna by Magnuson (1973,
tables 1, 4). Also, the maximum thickness value (i.e.,
max. height + max. width/2 = 21.6% L) is within
the range (20.5-23.0% L) measured for four SIO
specimens (L from 28.5 to 42.5 cm) and near the
value given by Magnuson (1973, table 7, 22.3% L).
Finally, the point of maximum body thickness in the
study fish (39.7% L) and that of SIO fish (36-40%
L) are near Magnuson's value of 41.2% L (for fish
from 28 to 45 cm L).
The dorsal fin of this fish is normal in shape, with
13 spinous rays, a maximum height of 3.5 cm and
a surface area of 9.5 cm2. The second dorsal fin is
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
463
Figure 1— Left- and right-side close-ups and a full-length, left-side photo of the Thunnus albacares with only one pectoral fin.
464
1 cm high and has an area of 2.0 cm2. The anal fin
is also 1 cm high and has an area of 2.2 cm2. The
combined total surface area of both sides of the sec-
ond dorsal and anal fins is 8.4 cm2, which is larger
than predicted (7.2 cm2) by the Magnuson and
Weininger equation (1978, app. II). The total num-
ber of second dorsal and anal fin rays and dorsal and
ventral finlets agrees with that for other yellowfin
tuna (Gibbs and Collette 1967, table 1).
Table 1 compares caudal keel area and caudal and
right pectoral fin dimensions of the study specimen
and seven SIO fish of differing L. Also shown are
values calculated for several of the same parameters
using allometric equations for T. albacares
(Magnuson 1978, table X; Magnuson and Weininger
1978, app. II). The caudal keel area of the one-finned
fish (6.2 cm2) is smaller than the value expected
from the equation (6.7 cm2) but is well within (i.e,
93%) the range of variation (77-102%) seen in the
SIO specimens (Table 1). Comparison of the
measured and the equation-derived caudal data for
the one-finned fish with the same set of values for
the next smallest (32.5 cm) and largest (37.0 cm) SIO
fish indicates that the caudal fin of the one-finned
fish has a slightly smaller span but larger area than
would be expected for its L. This is further reflected
in its aspect ratio (AR; 4.63), which is lower than that
of any of the SIO specimens. This lower value prob-
ably does not represent an artifact of preservation
because in the other material caudal span and area
increased directly with L. There is also general
agreement between the measured and calculated
values for each, showing that neither preservation
nor measurement protocols affected caudal fin data.
As would be expected from the underlying formulae,
caudal AR calculated from the equations increases
with L. However, among the measured data, there
is no correlation between AR and L. It is also note-
worthy that both the mean and predicted AR values
of all of these small yellowfin (5.64, 5.34, Table 1) are
in good agreement but well below the summary
range (6.8-7.2) given for larger T. albacares by
Magnuson (1978, table IX). This serves to empha-
size that while AR may differ between species of
scombrids (Magnuson 1978), it also varies within
each species as a function of body size
Both the length and area of the right pectoral fin
of the one-finned fish are much less than those of
the 37 cm SIO specimen (Table 1). When measured
and computed pectoral fin areas are compared, there
is good agreement between both values for the 37
and 42.5 cm L fishes but not for the 36.5 cm L one-
Table 1.— Comparative caudal and right pectoral fin measurements for the one-finned
yellowfin tuna (36.5 cm L) and seven specimens of different lengths (L) from the SIO
collection. Data for each fish includes the actual measured values (m) and values
calculated (c) from equations in the footnotes (Magnuson and Weininger 1978, app. II).
Caudal k<
Area1
(cm2)
;el
Caudal fin
Right pectoral fin
Fork
length
(cm)
Length
Span2
(cm)
Area3
(cm2)
Aspect
ratio4
Area5
(cm)
(°/oL)
(cm2)
25.8 m
c
2.7
3.1
9.5
6.8
12.7
9.9
7.11
4.67
5.63
(21.8)
6.7
9.4
28.5 m
c
3.8
3.8
8.0
7.7
12.3
12.1
5.20
4.90
6.00
(21-0)
5.3
11.3
31.5 m
c
3.7
4.8
9.0
8.8
15.8
14.8
5.13
5.23
7.71
(24.5)
11.1
13.5
32.5 m
c
4.8
5.2
10.0
9.1
15.7
15.8
6.37
5.24
7.25
(22.3)
10.6
14.2
636.5 m
c
6.2
6.7
10.0
10.5
21.6
20.0
4.63
5.51
7.50
(20.5)
12.8
17.5
37.0 m
c
5.3
6.9
11.0
10.7
21.6
20.6
5.60
5.56
9.67
(26.1)
17.8
17.9
40.0 m
c
8.5
8.3
12.5
11.7
25.4
24.1
6.15
5.68
10.40
(26.0)
714.3
20.6
45.0 m
c
8.8
10.8
12.2
13.5
30.3
30.7
4.91
5.92
11.00
(25.9)
25.3
25.4
m
c
x, SE 5.64, 0.30
x, SE 5.34, 0.15
'Caudal keel area =
2Caudal span =
3Caudal area =
4Aspect ratio =
5Pectoral fin area =
6One-finned fish.
7Fin was torn.
0.00198 L226.
-2.27 + 0.35 L
0.013 L204
Span2/area
0.116 L178/4.
465
finned fish. In general, application of the pectoral
area equation to the smaller SIO fish (Table 1) does
not result in close correspondence between estimated
and observed areas, suggesting that the relationship
derived from larger individuals does not fit smaller
yellowfin tuna. The relative length of the pectoral
fin in yellowfin tuna changes abruptly with size In
fish between about 35 and 42 cm L, pectoral fin
length should normally be about 25% L (Gibbs and
Collette 1967, fig. 26). This contrasts with the value
for the one-finned fish of 20.5% L.
The left pectoral girdle is present, but clearly ab-
normal in gross examination. The posttemporal is
reduced in overall size; the upper (pterotic) fork is
somewhat reduced and lower (epiotic) fork weakly
developed and without a flattened articular surface
The rear margin of the supracleithrum is eroded, and
the lateral surface rough. The cleithrum is almost
as large as that of the right side, but the lateral
groove for muscle attachment is reduced, and the
upper process that normally curves out over the
scapula is absent. The scapula is a block of bone with-
out an articular facet for the first pectoral ray, and
the scapular foramen is represented by a slit in the
lateral surface The coracoid is much reduced pos-
teriorly, and its reduced lower process is tightly ap-
plied to the cleithrum so that the interosseus space
is almost absent. The pectoral actinosts may be
represented by a small lump of bone that is tightly
attached to the scapula. A number of bone chips
were embedded in the tissue overlying the pectoral
girdle The postcleithra appear to be essentially
normal.
Elements in the left side of the pelvic girdle are
larger and have a different orientation from those
of the right. Also, the left pelvic fin is both smaller
in area and shorter than the right (Fig. 2). Pelvic fin
lengths and areas in the one-finned fish are left 2.9
cm, 3.2 cm2; right 3.5 cm, 4.7 cm2. Comparable
values for the 37.0 L SIO fish are left 3.5 cm, 4.5
cm2; right 3.7 cm, 4.9 cm2. X-rays showed that the
centra of vertebrae 19 and 20 are abnormal (Fig. 3).
They lie parallel to one another and overlap by about
80% in the horizontal axis. There is considerable ero-
sion of the adjoining surfaces of the two centra and
their neural and haemal spines are displaced. This
deformity, together with the reduced left pelvic fin,
the absence of a left pectoral fin, and a deformed
left pectoral girdle, suggests the presence of a con-
genital malformation.
As would be expected from our density findings,
the gas bladder of the one-finned fish was small (17
x 5 mm, length x diameter), but about the same
size as that of other yellowfin tuna (Magnuson 1973,
1978). Finally, we found no differences in the left and
right body myotomes. The total red muscle was
estimated to be 6.7% of wet weight, which is with-
in the 95% confidence limits of the value reported
for yellowfin tuna (5.2-7.8%) by Graham et al.
(1983).
Figure 2— Anterior ventral view showing the
reduced size of the left pelvic fin.
466
h
Figure 3— Tbp: Right-side X-ray of the vertebral column showing the impacted vertebrae and the neural and haemal
spine displacement. Bottom: Dorsal X-ray of the same vertebrae Arrow indicates anterior. Scale is 2.5 cm.
467
Discussion
Our study suggests that congenital defects led to
the absence of a left pectoral fin, the formation of
a small right pectoral and left pelvic fins, and to the
impaction of two vertebrae A smaller caudal span
may also be a result of such defects. On the basis
of age studies (Uchiyama and Struhsaker 1981) we
estimate that this fish (36.5 L) was about 9 mo old
when captured. (But, because of the vertebral
damage, the fish is shorter than it should be and 9
mo is a conservative age estimate) Thus in spite of
significant locomotory handicaps, this fish had been
swimming and feeding effectively at the time it was
taken by hook and line.
Morphological comparisons with SIO specimens
and with equation-derived values for similarly sized
yellowfin tuna did not indicate any major structural
differences in the one-finned fish that can be inter-
preted as having facilitated its swimming. However,
since the absence of one pectoral fin doubtlessly af-
fects the minimum speed required for hydrostatic
equilibrium, the horizontal stability, and the maneu-
verability of a tuna, it is instructive to consider how
the loss might have been compensated. Magnuson
(1973, 1978) has amply demonstrated the role of the
paired fins in providing lift and reducing minimum
equilibrium speed. Total lift (Lt) is calculated as
Lt (dynes) = M[l - - (g)\
(1)
where M is fish wet weight, Pe is seawater density,
Pf is fish density, and g is the acceleration of gravi-
ty (980 cm -sec-2). The amount of lift needed by the
one-finned fish (M = 861 g, Pf = 1.08, Pe = 1.02 at
25°C) is 47,203 dynes.
The minimum speed for hydrostatic equilibrium
U100 is determined by
U
100
PJ2 (CLAp + CLAk_
%
(2)
where CL is the coefficient of lift for the pectoral
fins (p) and caudal keel (A;) and Ap and Ak are their
respective areas (Magnuson 1973). Pectoral fin lift
area includes both fins and the flat section of body
between them (Magnuson 1978, fig. 4). This can be
calculated from an allometric relationship (Mag-
nuson 1973, table 4).
Av = 0.0609 L187,
(3)
and, for a 36.5 cm L yellowfin, Ap = 50.8 cm2. With
this value, a measured keel area (Table 1) of 6.2 cm2,
and assuming a lift coefficient of 1.0 for both sur-
faces (Magnuson 1973, table 4) the calculated (Equa-
tion (2)) minimum speed for a 36.5 cm yellowfin tuna
is 40.3 cm-s-1. The same calculation for the one-
finned fish (Ap = 25.4 cm2) yields a minimum speed
of 54.1 cm-s-1, a 34.3% increase The one-finned
fish would need to swim faster, and thus expend
more energy. Its higher speed would also probably
have required it to make continuous velocity and
position changes in order to keep pace with a school
of, on average, similarly sized and thus slower swim-
ming yellowfin tuna.
Alternatively the fish might have assumed a
pitched (i.e, head up) swimming mode in an attitude
such that its body surface would have contributed
to hydrodynamic lift by having a positive angle of
attack relative to the direction of motion, and the
CL of the caudal keel would be increased (Magnu-
son 1978). Of course this would result in increased
pressure drag and require more swimming power,
but it might have enabled the fish to swim more
slowly.
Under any conditions, it seems likely that this fish
was not highly maneuverable and would have diffi-
culty remaining upright (i.e, not rolling to the left).
It, of course, could not use its left pectoral for
braking and left turns, and its left pelvic fin, which
would also contribute to these actions, was less ef-
fective than normal because of its small size Tunas
normally accelerate with their first dorsal, pectoral,
and pelvic fins appressed (Magnuson 1978), but as
this fish slowed and needed lift it would have likely
began to roll to its left as soon as its right pectoral
fin was extended. This could be countered somewhat
by its dorsal fin, but the necessity for unilateral use
of the right pectoral fin should have always resulted
in some amount of leftward roll and a tendency to
turn to the right. Both the sharpness of the turn and
the net upward or downward spiral movement of the
fish would depend upon the degree of fin extension
and swimming velocity.
Finally, to compensate for the tendency to roll it
is possible that the fish habitually swam with its body
tilted as much as 80° to the right. In this position
it would retain the largest possible pectoral lift area
and might gain sufficient additional lift from the dor-
sal, second dorsal, anal fins and the body surface to
more than compensate for loss of keel lift. It is note-
worthy that the second dorsal and anal fin areas of
this fish are larger than predicted (see above). The
fish would be able to roll from its side to an upright
position merely by extending its pectoral fin a bit
468
farther. Also, side swimming would place both pelvic
fins in a position where they could facilitate rapid
left (now ventral) turns while possibly adding lift.
Acknowledgments
This study benefited from funds provided by the
Foundation for Ocean Research at SIO, and by
University of California, San Diego, Biomedical and
Academic Senate research grants. We thank Cap-
tain Jesus Yamamoto for saving the specimen for
study and W. Bayliff for providing it to us. We also
thank W Klawe, W Bayliff, and A. Dizon for com-
menting on the manuscript.
Literature Cited
FlERSTINE, H. L., AND V. WALTERS.
1968. Studies in locomotion and anatomy of scombroid fishes.
Mem. South. Calif. Acad. Sci. 6:1-29.
GIBBS, R. H., AND B. B. COLLETTE.
1967. Comparative anatomy and systematics of the tunas,
genus Thunnus. Fish. Bull., U.S. 66:65-130.
Graham, J. B., F. J. Koehrn, and K. A. Dickson.
1983. Distribution and relative proportions of red muscle in
scombrid fishes: consequences of body size and relationships
to locomotion and endothermy Can. J. Zool. 61:2087-2096.
Magnuson, J. J.
1973. Comparative study of adaptations for continuous swim-
ming and hydrostatic equilibrium of scombroid and xiphoid
fishes. Fish. Bull., U.S. 71:337-356.
1978. Locomotion by scombrid fishes. In W. S. Hoar and D
J. Randall (editors), Fish physiology, Vol. 7, p. 239-313.
Acad. Press, N.Y.
Magnuson, J. J., and D. Weininger.
1978. Estimation of minimum sustained speed and associated
body drag of scombrids. In G. D. Sharp and A. E. Dizon
(editors), The physiological ecology of tunas, p.
293-311. Acad. Press, N.Y.
UCHIYAMA, J. H., AND P. STRUHSAKER.
1981. Age and growth of skipjack tuna, Katsuwonus pelamis,
and yellowfin tuna, Thunnus albacares, as indicated by daily
growth increments of sagittae Fish. Bull., U.S. 79:151-162.
Jeffrey B. Graham
Richard H. Rosenblatt
Darcy L. Gibson
Physiological Research Laboratory and
Marine Biology Research Division
Scripps Institution of Oceanography
La Jolla, CA 92093
CHROMOSOMAL ANALYSIS OF ALBACORE,
THUNNUS ALALUNGA, AND YELLOWFIN,
THUNNUS ALABACARES, AND SKIPJACK,
KATSUWONUS PELAMIS, TUNA
Chromosomal analysis is being used as part of an
investigation of the population stock structure of the
North Pacific albacore, Thunnus alalunga. There is
a growing body of evidence (Brock 1943; Laurs and
Lynn 1977; Laurs and Wetherall 1981; Laurs 1983)
that North Pacific albacore are not as homogeneous
as usually assumed (Clemens 1961; Otsu and Uchida
1963). Results from recent tagging studies suggest
that northern and southern substocks constitute the
North Pacific albacore population and that these
proposed substocks have different migratory pat-
terns (Laurs and Nishimoto 19791; Laurs 1983).
Laurs and Wetherall (1981) also found that the
growth rates were significantly different in the two
proposed substocks. In addition, the differences in
growth rate are consistent with differences in length
frequencies of albacore caught in commercial fish-
eries off North America (Brock 1943; Laurs and
Lynn 1977).
In this paper we report results from chromosomal
analysis using C-banding for albacore (from the pro-
posed North Pacific southern substock) and compare
them with similar results obtained for yellowfin,
Thunnus alabacares, and skipjack, Katsuwonus pela-
mis, tuna. We demonstrate that there is a chromo-
somal basis for placing the albacore and the yellow-
fin tuna in the genus Thunnus and that recognizable
chromosomal differences exist between the genera
Thunnus and Katsuwonus. These findings corrobo-
rate the taxonomy of the albacore and the yellowfin
and skipjack tuna based on comparative anatomy
(Gibbs and Collette 1967; Collette 1978).
The results reported here are from part of a larger
study, which is helping us to evaluate if genetic
heterogeneity exists in the North Pacific albacore
population. Information on chromosome character-
istics is scarce for fishes, and to our knowledge this
is the first time chromosome analyses have been
reported for scombrid fishes.
Materials and Methods
All blood samples were collected from freshly
caught fish either aboard the NOAA RV David
Starr Jordan (August 1983) or aboard fishing boats
»Laurs, R. M., and R. N. Nishimoto. 1979. Results from North
Pacific albacore tagging studies. U.S. Dep. Commer., Natl. Mar.
Fish. Serv., SWFC Admin. Rep. LJ-79-17, 9 p.
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
469
(October-November 1983). Because albacore have
a high titer of red blood cells (Alexander et al. 1980),
it was expedient to separate the lymphocytes from
the erythrocytes. The lymphocytes were isolated
from the blood on a density gradient of ficoll-sodium
diatrizoate solution using a modification of the tech-
nique developed by Boyum (1968), which is specific
for the concentration of lymphocytes. We found that
it was necessary to isolate the lymphocytes and place
them in culture within a couple of hours after blood
samples were collected. The ficoll gradient pro-
cedure was not successful using undiluted hepari-
nized blood that was retained for more than a few
hours.
Two albacore, three skipjack tuna, and four
yellowfin tuna were sampled. All fish were juveniles
which have virtually no sexual dimorphic character-
istics, and no sex determinations were made. The
estimated fork lengths of the fish ranged from 65
to 85 cm for albacore, 80 to 120 cm for yellowfin,
and 45 to 55 cm for skipjack.
From each fish, an 8-10 mL sample of blood was
withdrawn via sterile intracardial puncture into a
syringe coated with 1,000 units/mL of heparin. Two
mL aliquots of blood were pipetted into each of the
four 15 mL centrifuge tubes, and 4 mL of cell culture
medium2 was added. The mixture was centrifuged
at 20 g for 5 min, and the white cells and plasma
were transferred to another centrifuge tube. This
procedure for the separation of the plasma and white
cell mixture was repeated three times following the
suggestions given by Blaxhall (1981).
Five mL of the white cell-plasma mixture were
layered over 3 mL of ficoll-sodium diatrizoate solu-
tion and centrifuged at 572 g for 30 min. The over-
laying plasma was removed carefully with Pasteur
pipets, and the lymphocytes below were transferred
to a culture tube containing 5 mL of marine teleost
cell culture medium (Michael and Beasley 1973). This
procedure resulted in an erythrocyte free culture of
lymphocytes having a higher mitotic index. The
cultures were incubated at 25 °C for 3-5 d, at which
time they were terminated and the cells harvested.
The techniques for chromosomal analysis were pat-
terned after those of Nowell (1960) for mammals
because tuna are also endothermic (Graham and
Dickson 1981). This work is an extension of the pro-
cedures developed by Kelly and Laurs (19833).
Prior to harvesting the cells, 0.5 \ng colcemid was
added to 5 mL of culture medium and incubated for
2 h at 25° C. The culture was then centrifuged for
5 min at 180 g and the supernatant was replaced
with 5 mL 0.075 M KC1 for 10 min. The culture tubes
were centrifuged again for 5 min at 180 g, and the
supernatant was replaced with 3 mL of freshly
prepared cold fixative which consists of 3 parts
methyl alcohol to 1 part glacial acetic acid and mixed
for 1 h. The tubes were again centrifuged at 180 g
for 5 min, decanted, and fixed. The cell pellet plus
0.5 mL of fixative was retained for slide preparation.
Precleaned slides dipped in methanol and then in
deionized water were used for slide preparations.
Two drops of cell suspension were placed on the slide
and 4 drops of fixative were immediately added. The
slide was dried on a slide warmer at 37 °C and stored
at room temperature for 24-72 h prior to C-banding.
The C-banding procedures were patterned after the
work of Pardue and Gall (1970) and Arrighi and Hsu
(1971).
In preparation for C-banding, the slides were
placed in 0.2 N HC1 for 15 min at 37°C, rinsed in
deionized water, treated with saturated Ba(OH)2 at
room temperature for 7 min, and rinsed in deionized
water. They were then immediately dipped again in
0.2 N HC1 for 10 s and rinsed in deionized water.
After the final rinsing the slides were incubated in
2x sodium chloride-sodium citrate solution at 60 °C
for 90 min and then stained for 90 min in Giemsa
diluted with 1:10 Sorenson's buffer pH 6.8. Suitable
metaphase figures were photographed at 1,008 x
magnification using a Zeiss4 microscope equipped
with a phase planapochromat 63/1.4 oil immersion
lens.
Results
Chromosome Numbers
Kelly and Laurs (fn. 3) found that the diploid
number of chromosomes for albacore was 48. We
have confirmed this observation and have found that
the diploid numbers for yellowfin and skipjack tuna
are also 48. The modal frequencies of about 90 cells
containing 48 chromosomes were 82.2% for alba-
core, 92.6% for yellowfin, and 80.5% for skipjack.
Kelly and Laurs also observed that 85% of albacore
cells had 48 chromosomes. Two polyploid cells with
2RPMI-1640 Sigma Cat. No. R6504.
3Kelly, Raymond M., and R. Michael Laurs. 1983. Summary
of methods developed for investigations of albacore chromosomes
and of findings made on number of chromosomes. Unpubl. field
and laboratory notes and results (April 1983). [Raymond M. Kelly,
School of Medicine, University of California, La Jolla, CA; R.
Michael Laurs, National Marine Fisheries Service, NOAA, La Jolla,
CA.]
4Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
470
96 chromosomes were observed in skipjack, and one
polyploid cell with 96 chromosomes was observed
in albacore. No polyploid cells were observed in
yellowfin.
Chromosome Morphology
The albacore and the yellowfin and skipjack tuna
were observed to have the same diploid chomosome
number; however, their karyotype differed with
respect to chromosome morphology. In this study,
the chromosome pairs were arranged according to
the morphology index (M), developed by Giannelli
and Howlett (1967), which is obtained by dividing
the length of the total haploid chromosome set p +
q by the arm ratio (q/p). Based on our evaluation of
256 metaphase cells (Table 1), we found that the
chromosome morphology of the yellowfin (Fig. 1)
is more similar to that of the albacore (Fig. 2) than
the skipjack (Fig. 3). The differences in chromosome
morphology were most apparent in the three largest
pairs of chromosomes (Table 1). The morphology
index (M) places the metacentric and submetacentric
chromosomes of the albacore and yellowfin in the
number 1 and 2 positions respectively. Chromosome
3 of the albacore is also submetacentric while chro-
mosome 3 of the yellowfin is referred to as sub-
telocentric. The subtelocentric category is used to
describe chromosomes in which the centromeres are
displaced more towards the telomere when com-
pared with submetacentrics. The metacentric
chromosome of the albacore was consistently larger
than the metacentric of the yellowfin. The remain-
ing 42 chromosomes were telocentric in the albacore
and yellowfin. All of the chromosomes of the skip-
jack were telocentric.
C-Banding Patterns
C-banding determinations were done to differen-
tiate individual chromosome characteristics among
the three species of tunas (Table 2). The centromeric
regions of most of the chromosomes of all three
species contained C-band constitutive heterochroma-
tin. However, there were differences in the inten-
sities of staining on comparable chromosomes
among the three species. Intercalary C-banding was
observed only in the skipjack tuna and there was
variability in terminal banding among the three
species.
In the albacore all chromosomes, except pair 10,
showed C-banding in the centromeric regions with
intense, prominent bands notably apparent in
chromosome pairs 2 and 3 (Fig. 2). Terminal band-
ing was restricted to chromosome pair 1 which had
obscure C-bands on one arm of each homologue. No
intercalary C-banding was observed in the albacore.
There were some minor differences in the C-band-
ing patterns between albacore and yellowfin tuna.
In the yellowfin, the centromeric regions of all
chromosomes were banded, the intensity of the
banding in the centromeric region was uniform
Table 1.— Classification of chromosome morphology for albacore and
yellowfin and skipjack tuna.
Chromosome
number
Albacore
Yellowfin
Skipjack
1
2
3
4-48
metacentric
submetacentric
submetacentric
telocentric
metacentric
submetacentric
subtelocentric
telocentric
telocentric
telocentric
telocentric
telocentric
Table 2.— Summary of C-banding characteristics for albacore and yellowfin and skipjack tuna.
Location of
bands
Albacore
Yellowfin
Skipjack
Centromeric Present on all chromosomes Present on all chromosomes Present on all chromosomes
region
Terminal
bands
Intercalary
except pair 10; intensely
prominent on pairs 2
and 3
Present on one arm of each
homologue on pair 1;
weakly developed
None present
with uniform prominent
intensity
Weakly developed on
chromosome pairs 1, 3,
7, 8, 14, 15, 21, & 24
None present
except pairs 10 and 19,
great variability in inten-
sity most prominent on
pairs 1, 3, 4, 7, and 18
Notably prominent in
pair 4
Present on all chromosome
pairs except 17 and 24
471
1
H M
, -
V V
Id ■ t»
(18 DC 53 4'
8
1
4 •
* r
10
11
12
|| Lh |0 #5 II Itf
13 14 15 16 17 18
II 60 10 II
&
Aft
19
20
21
22
23
24
Figure 1.— Giemsa stained karyotype (upper row) and C-banding karyotype (lower row) of the same
yellowfin tuna.
among all chromosomes, and terminal banding was
weakly developed on eight pairs of chromosomes
(Fig. 1). As in the albacore, no intercalary banding
was observed in the yellowfin. The following sig-
nificant differences were observed in the C-banding
patterns between the skipjack and the other two
species: 1) all chromosomes except 10 and 19 had
C-banding in the centromeric region, 2) there was
great variability in the intensity of staining in the
472
centromeric region, 3) terminal banding was notably
prominent in chromosome pair 4, and 4) there were
intercalary bands on all chromosomes except pairs
17 and 24.
Discussion
Our results assist in understanding speciation pro-
cesses that have occurred in the evolution of the
1
7
13
19
(a)
I
|
2
3
4
5
6
U
8
9
10
11
12
14
15
16
17
18
R
20
21
22
23
24
• •
3
8
10
11
12
13
14
15
16
17
18
19
(b)
20
21
22
23
24
Figure 2.— Giemsa stained karyotype (a) and C-banding karyotype (b) from two different fish of the
North Pacific albacore.
tuna. Gibbs and Collette (1967) proposed that seven
species of tuna be included in the genus Thunnus
on the basis of external morphological and internal
anatomical characters. Our results demonstrate that
there is a genetic basis for placing the albacore, T.
alalunga, and the yellowfin tuna, T. albacares, in
one genus Thunnus and the skipjack tuna, Kat-
suwonus pelamis, in a separate genus. These
relationships are based on the assumption that
closely related species will share certain karyotypic
characteristics.
The determination that the albacore, yellowfin
tuna, and skipjack tuna have the same number of
chromosomes suggests that speciation of the genera
of Thunnini might have occurred by intrachromo-
somal rearrangement as opposed to Robertsonian
changes as hypothesized for the rainbow trout,
Salmo gairdneri (Thorgaard 1976). If speciation had
473
3
»"
*
8
m
2
I ft
i
M II
! f
i
§
10
I H
11
•■
It
12
H
13
14
15
16
17
18
i
19
I ft* ft ii •*
20
21
22
23
24
Figure 3.— Giemsa stained karyotype (upper row) and C-banding karyotype (lower row) of the same
skipjack tuna.
involved a reduction in uniarmed chromosomes to
form biarmed chromosomes, we would have ex-
pected to find a difference in the chromosome
number between Katsuwonus and Thunnus.
It is probable that speciation within the genus
Thunnus might also be related to chromosome rear-
rangement because the number of chromosomes is
the same. Pericentric inversion is a type of intra-
chromosomal rearrangement that could result in the
displacement of the centromere to convert a telo-
centric chromosome into a metacentric one. Zenzes
and Voiculescu (1975) suggested that pericentric in-
version was involved in the chromosomal organiza-
tion of the brown trout, Salmo trutta. The extent
to which this mechanism has been related to the
speciation of genera Thunnus and Katsuwonus is
474
uncertain. However, the occurrence of terminal C-
bands on chromosome 1 of the albacore and chromo-
somes 1 and 3 of the yellowfin tuna is consistent with
the hypothesis that these biarmed chromosomes
were derived from a uniarmed condition. Indeed,
White (1951) believed that, in grasshoppers, telo-
centric chromosomes are more primitive than the
metacentric condition. Absence of terminal bands
on chromosomes 2 and 3 of the albacore and chromo-
some 2 of the yellowfin tuna does not preclude the
suggested derivation of metacentric chromosomes.
It is possible that in the metacentric chromosomes
lacking terminal bands, centrometric heterochroma-
tin either was not moved or was lost. It is also possi-
ble that chromosome rearrangement in the specia-
tion of the albacore and yellowfin occurred through
changes in the euchromatic portions of chromo-
somes. To test this hypothesis it will be necessary
to use G-banding techniques (Rishi 1978) to conduct
analysis of these portions of the chromosomes.
In contrast to the albacore and yellowfin tuna, the
telocentric chromosomes of the skipjack tuna
showed a variety of intercalary and terminal C-band-
ing in addition to those of the centromeric regions.
An interesting condition was the polymorphic ter-
minal heterochromatic block that occurred in chro-
mosome pair number 4 of the skipjack, but not in
the albacore or yellowfin. While the four specimens
of skipjack analyzed had this polymorphism, it is not
possible to comment on the frequency with which
it might occur in the population. This type of dif-
ferential banding also occurs in other fishes as
demonstrated by Zenzes and Voiculescu (1975) who
observed a difference in the size of C-bands in Salmo
trutta. The C-band polymorphism we observed in
skipjack could be related to the sex determining
mechanism of the fish. However, we do not have any
information on the sex of the skipjack used in this
study and most fish do not have heteromorphic sex
chromosomes (Zenzes and Voiculescu 1975; Thor-
gaard 1976; Kligerman and Bloom 1977). An excep-
tion occurs in the eels which have highly hetero-
morphic sex chromosomes (Park and Grimm 1981).
Analysis of C-banding patterns associated with the
morphological differences in chromosomes has per-
mitted us to identify all of the chromosome pairs of
the albacore, yellowfin tuna, and skipjack tuna. We
have demonstrated that karyotype analysis may pro-
vide a chromosomal basis for placing albacore and
yellowfin in Thunnus and skipjack in Katsuwonus.
Although C-banding techniques did not allow a
detailed evaluation of the Thunnus chromosomes,
we believe that the use of multiple banding pro-
cedures could provide important information on the
speciation and cytotaxonomy of the species of this
commercially important genus. In addition, use of
G-banding procedures will be an important next step
in determining if genetic heterogeneity exists in the
North Pacific albacore population.
Acknowledgments
We wish to thank A. Dean Stock (City of Hope
Hospital, Duarte, CA) and James Mascarello
(Children's Hospital, San Diego, CA) for many
helpful suggestions, Raymond Kelly (University of
California Medical School, San Diego, CA) for help
in procurement of materials, and the personnel of
the San Diego Sportsfishing Association, Captains
Ed McEwen and Buzz Brizendine for space aboard
their boats to make this work possible.
Literature Cited
Alexander, N., R. M. Laurs, A. McIntosh, and S. N.
Russell.
1980. Haematological characteristics of albacore, Thunnus
alalunga (Bonnaterre), and skipjack Katsuwonus pelamis
(Linnaeus). J. Fish. Biol. 16:383-395.
Arrighi, F. E., and T. C. Hsu.
1971. Localization of heterochromatin in human chromo-
somes. Cytogenetics 10:81-86.
Brock, V. E.
1943. Contribution to the biology of the albacore (Germo
alalunga) of the Oregon coast and other parts of the North
Pacific. Stanford Ichthyol. Bull. 2:199-248.
Blaxhall, P. C.
1981. A comparison of methods used for the separation of
fish lymphocytes. J. Fish. Biol. 18:177-181.
Boyum, A.
1968. Separation of leukocytes from blood and bone marrow.
Scand. J. Clin. Lab. Invest., 21, Suppl. 97:77.
Clemens, H. B.
1961. The migration, age, and growth of Pacific albacore
(Thunnus germo), 1951-1958. Calif. Dep. Fish Game, Fish
Bull. 115, 128 p.
Collette, B. B.
1978. Adaptations and systematics of the mackerels and
tunas. In G. D. Sharp and A. E. Dizon (editors), The
physiological ecology of tunas, p. 7-88. Acad. Press, N.Y.
GlANNELLI, F., AND R. M. HOWLETT.
1967. The identification of the chromosomes of the E group
(16-18 Denver): an autoradiographic and measurement
study. Cytogenetics (Basel) 6:420-435.
Gibbs, R. H., Jr., and B. B. Collette.
1967. Comparative anatomy and systematics of the tunas
Genus Thunnus. U.S. Fish Wildl. Serv., Fish. Bull. 66:
65-130.
Graham, J. B., and K. A. Dickson.
1981. Physiological thermoregulation in the albacore tuna
Thunnus alalunga. Physiol. Zool. 54:470-486.
Kligerman, A. D., and S. E. Bloom.
1977. Distribution of F-bodies, heterochromatin, and nucleo-
lar organizers in the genome of the central mudminnow, Um-
bra limi. Cytogenet. Cell Genet. 18:182-196.
475
Laurs, R. M.
1983. The North Pacific albacore - an important visitor to
California Current water. Calif. Coop. Oceanic Fish. Invest.
Rep. 24:99-106.
Laurs, R. M., and R. J. Lynn.
1977. Seasonal migration of North Pacific albacore, Thun-
nus alalunga, into North American coastal waters: distribu-
tion, relative abundance, and association with Transition
Zone waters. Fish. Bull., U.S. 75:795-822.
Laurs, R. M., and J. A. Wetherall.
1981. Growth rates of North Pacific albacore, Thunnus
alalunga, based on tag returns. Fish. Bull., U.S. 79:293-
302.
Michael, S. M., and A. R. Beasley.
1973. Marine teleost fish tissues. In P. F. Kruse, Jr. and M.
K. Patterson, Jr. (editors), Tissue culture methods and ap-
plication, p. 134. Acad. Press, N.Y.
Nowell, P. C.
1960. Phytohaemagglutinin: an initiator of mitosis in culture
of normal human leukocytes. Cancer Res. 20:462-466.
Otsu, T., and R. N. Uchida.
1963. Model of the migration of albacore in the North Pacific
Ocean. U.S. Dep. Inter., Fish. Wildl. Serv., Fish. Bull.
63:33-44.
Pardue, M. L., and J. G. Gall.
1970. Chromosome localization of mouse satellite DNA.
Science 168:1356-1358.
Park, E. H., and H. Grimm.
1981 . Distribution of C-band heterochromatin in the ZW sex
chromosomes of European and American eels (Anguillidae,
Teleostomi). Cytogenet. Cell Genet. 31:167-174.
Rishi, K. K.
1978. Giesma-banding in fish chromosomes. Current
Science 47:393-394.
Thorgaard, G. H.
1976. Robertsonian polymorphism and constitutive hetero-
chromatin distribution in chromosomes of the rainbow trout
(Salmo gairdneri). Cytogenet. Cell Genet. 17:174-184.
White, M. J. D.
1951. A cytological survey of wild populations of Trimero-
tropis and Circotettix (Orthoptera, Acrididae). II. Racial dif-
ferentiation in T. sparsa. Genetics 36:31-53.
Zenzes, M. T., and I. Voiculescu.
1975. C-banding patterns in Salmo trutta, a species of tetra-
ploid origin. Genetica 45:531-536.
San Diego State University
San Diego, CA 92182
San Diego State University
San Diego, CA 92182
Present address:
Wuhan University
Wuhan, Peoples Republic of China
Southwest Fisheries Center
National Marine Fisheries Service, NOAA
P.O. Box 271,
La Jolla, CA 92038
F. J. Ratty
Y. C. Song
R. M. Laurs
ABUNDANCE, SIZE, AND SEX RATIO OF
ADULT SEA-RUN SEA LAMPREYS,
PETROMYZON MARMUS,
IN THE CONNECTICUT RIVER1
Populations of sea-run sea lampreys, Petromyzon
marinus, occur in many rivers on the east coast of
North America from Labrador to Florida (Bigelow
and Schroeder 1953). The Connecticut River in the
northeastern United States is believed to have the
largest population (Beamish 1980). Although the
historical, upstream range of the sea lamprey in the
Connecticut River is not known, it probably was
similar to American shad, Alosa sapidissima, which
migrated 280 km upstream to Bellows Falls, VT
(Moffitt et al. 1982).
Upstream migration of anadromous fish species
in the Connecticut River main stem was first re-
stricted in 1798 by the construction of Turners Falls
Dam at km 197, and further in 1849 by the construc-
tion of Holyoke Dam at km 140. The first upstream
fish passage facility for anadromous fish was a fish
lift at Holyoke Dam that began operating in 1955.
Until 1969 the sea lampreys using the fish lift were
counted and either killed or thrown back. From 1969
to 1984, they have been passed upstream each year.
Sea lampreys have also used the fish ladders that
were completed in 1980 and 1981 at Turners Falls
and Vernon Dams, respectively. With the comple-
tion of the fish ladder at Bellows Falls Dam in 1984,
migrants now have access to 350 km of main-stem
river and many additional tributaries (Fig. 1).
The present report summarizes the annual counts
of sea lampreys from 1958 to 1984 at the two Holy-
oke fish lifts (a second fish lift was added in 1976).
We also examined the sex ratio, total length, and
weight of adults in 1981-82 and compared these
characteristics with those of the population in the
St. John River, New Brunswick. Beamish et al.
(1979) sampled the St. John River population at km
140, at a fish lift located at Mactaquac Dam.
Methods
Sea lampreys that were lifted above the dam were
counted each year from 1958 to 1984, except for the
period from 1969 to 1974. From 1958 to 1968, sea
lampreys were counted by personnel of the Holyoke
Water Power Company (the owner of the dam), and
Contribution No. 95 of the Massachusetts Cooperative Fishery
Research Unit, which is supported by the U.S. Fish and Wildlife
Service, Massachusetts Division of Fisheries and Wildlife, Mass-
achusetts Division of Marine Fisheries, and the University of
Massachusetts.
476
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
Figure 1.— Map of the Connecticut River showing the location of Holyoke Dam and the other
dams with fishways on the lower 350 km of the main stem and major tributaries. Dams that
sea lampreys can pass are designated by an open bar; dams they cannot pass are designated
by a solid bar.
from 1975 to 1984, they were counted by person-
nel from either the Massachusetts Division of Fish-
eries and Wildlife or the Massachusetts Cooperative
Fishery Research Unit. Until 1975, fish of all species
were lifted, deposited into small carts, carried across
the dam, and counted as they were released. Begin-
ning in 1975, all fish were sluiced directly from the
fish lift bucket into a large flume and were counted
through a glass window in the side of the flume as
they swam upstream. The accuracy of these counts
has not been experimentally determined. However,
the counts are probably very accurate because the
sea lampreys are large and swim slowly through the
flume.
We collected sea lampreys daily at the fish lift trap
from 1 May to 10 June 1981, and from 10 May to
30 June 1982 for determination of total length (TL)
and sex. The number of sea lampreys sampled each
day was proportional to the number lifted the
previous day. The number of sea lampreys lifted and
(in parenthesis) the number collected follow: 0-50
(2); 51-100 (4); 101-200 (6); 201-400 (8); 401-800 (10);
801-1,000 (15); 1,001-2,000 (25); 2,001-3,000 (30);
3,001-5,000 (40); >5,000 (50). in both years, total
477
length was measured to the nearest millimeter and
sex.was determined by dissection. We determined
the sex ratio for each day of the run to observe
changes during the migration. In*1982 each sea lam-
prey was also weighed to the nearest gram. Chi-
square tests were used to compare the sex ratios
for differences from a 1:1 frequency. Student's t-test
was used to compare the males and females for
mean length and weight. We compared males and
females for the length-weight relationship by cal-
culating a separate regression for each sex using the
logarithmic equation: log w = log a + (b) (log 1)
(Ricker 1975).
Results and Discussion
Abundance
The numbers of sea lampreys lifted from 1958 to
1967 were relatively few, and probably reflected the
inefficiency of the fish lift rather than a small popula-
tion (Fig. 2). After the flume and second lift were
added in 1975 and 1976, respectively, 22,000-53,000
adults have been passed upstream each year. The
53,000 counted in 1981 was the largest number ever
passed at Holyoke and the largest run documented
in any river. In 1981, 59% of the total run was lifted
during the week of 24-30 May; and in 1982, 68%
were lifted during the week of 28 May-3 June.
Beamish (1980) reported that about 8,600 sea lam-
preys are lifted annually in the fish lift at Macta-
quac Dam. He estimated the spawning populations
in other northern streams at <8,000.
The sea lampreys that reach Holyoke Dam are
only a portion of the total run, because several
tributaries below the dam support populations
(Whitworth et al. 1976). The sea lamprey popula-
tion may increase as adults gain access to additional
spawning and rearing habitat in headwater streams
by using fish passage facilities constructed for Atlan-
tic salmon, Salmo salar, and American shad (Mof-
fitt et al. 1982). Thus, the restoration program
designed primarily for Atlantic salmon and Ameri-
can shad is also restoring the sea lamprey to addi-
tional habitat. Since 1975, over 20,000 sea lampreys
have been passed each year at Holyoke Dam and
given access to new spawning and rearing habitat.
The estimated life span of sea lampreys in the St.
John River is estimated at 9-12 yr (Beamish and Pot-
ter 1975). Therefore, if the Connecticut River
population returns to their natal stream and has a
similar life cycle, and if the strength of the year
classes after 1975 was enhanced by the additional
rearing habitat above Holyoke, then beginning in
60,000-
50,000-
40,000
(Z 30,000
LU
CD
•^ 20,000
600-
not
counted
58 60 62 64 66 68-74 76 78 80 82 84
YEAR
Figure 2.— Number of adult sea lampreys lifted in the Holyoke fish lifts each year, 1958-84.
478
1984 there should be increased returns of adults at
Holyoke. The return of sea lampreys at Holyoke in
1984 was not a record return, but this could be due
to the high discharge caused by the 50-yr flood that
occurred in early June 1984, when most sea lam-
preys are lifted. If the sea lamprey population in-
creases, the wound frequencies should increase on
host species of marine and anadromous fish.
Sex Ratio
Sex ratios for both years were skewed from 1:1
in favor of males, but the ratio was only significant
in 1982: in 1981, 56% were males (ratio: 1.3:1; x2
= 3.4, P > 0.05; in 1982, 62% were males (ratio:
1.6:1; x2 = H.6, P < 0.005, Table 1). Sex ratios also
changed during the spawning migration with the
proportion of males increasing late in the run. The
percent of males in the early and late periods were
55 and 59% in 1981 and 59 and 67% in 1982. The
increase in the proportion of males was not signifi-
cantly different from a 1:1 ratio in 1981, but the in-
crease was significant in 1982 (x2 = 7.6:P < 0.01).
Applegate (1950) found that males in landlocked sea
lamprey populations increased to about 75% in the
late part of the run. The reason for this phenomenon
is unknown.
Males are the most abundant sex in stable popula-
tions of sea-run and landlocked sea lampreys.
Beamish et al. (1979) reported 55% males (ratio:
1.36:1) in nearly mature adults in the St. John River
in 1974-77 (Table 1). Davis (1967), who collected
anadromous sea lampreys for 5 yr from Barrows
Stream, ME, reported a male:female ratio of 1.9:1;
however, the sample size was very small (N = 66).
Potter et al. (1974) found an excess of males in land-
Table 1. — Mean total length and weight (SE in parenthesis), and
percent males in sea lampreys sampled at Holyoke Dam, Connec-
ticut River, compared with samples collected from the Mactaquac
Dam, St. John River.
Dam &
N
Mean length
(cm)
Mean length
(cm)
Male Female
year
Male
Female
male
Holyoke
1981
464
71.3
(2.8)
71.5
(2.9)
—
—
56
1982
404
71.4
71.1
1794
2806
62
(2.7)
(3.6)
(8.2)
(12.01)
Mactaquac3
1974-77
341
72.4
72.9
868
885
55
(4.7)
(5.1)
(18.1)
(18.3)
'249 males were weighed.
2155 females were weighted.
3Data from Beamish et al. (1979); ± 95% confidence limits in parenthesis.
locked sea lamprey (ratio: 1.26:1). The sex ratio in
stable populations (where males are more abundant
than females) is different from the ratio in popula-
tions from the upper Great Lakes, where an excess
of females is typical of populations being eradicated
or controlled (Smith 1971). Sex ratios in sea lam-
preys also vary with cycles of abundance (Wigley
1959; Smith 1971), and temperature and nutrition
may differentially affect growth and survival of male
and female ammocoetes (Hardisty 1954).
Total Length and Weight
In 1981, 464 sea lampreys (0.9% of the number
lifted) were measured for total length; in 1982 the
number examined was 404 (1.5% of the number
lifted). There was no significant difference between
the mean length of males and females during either
year or for both years (Student's t-test: P > 0.05,
Table 1). Length of females and males ranged from
60 to 85 cm in both years.
The similarity in mean total length of adults in the
consecutive spawning runs of 1981-82 suggests
relative stability of the sea lamprey population. This
differs greatly from the unstable sea lamprey
populations in the Great Lakes where body length
decreased from 1950's to 1960's— changes related
to decreases in food supply and changes in the en-
vironment (Smith 1971).
The mean weight of females was not significant-
ly different from the mean weight of males (Stu-
dent's t-test: P > 0.05, Table 1). We determined the
length-weight relationship by using the regression
equations: log w = -3.42 ± (2.21) (log 1), (r2 =
0.75, P < 0.01) for females and log w = -3.11 ±
(2.10) (log 1), (r2 = 0.76, P < 0.01) for males. There
was no significant difference between the slopes of
the regression lines, consequently we combined
males and females (N = 404). Using the equation
y = b + mx or weight = b + (slope) (length), a highly
significant correlation (r2 = 0.76, P < 0.01) was
found for the regression equation: weight = 521.9
+ (0.23890) (length). The length-weight relationship
is linear, rather than sigmoid, as it is in most fishes.
Because the body is attenuate, the weight of sea lam-
preys does not increase as rapidly with length as it
does in most other fishes. This relationship is less
evident in females, possibly because of the additional
weight of their eggs.
Generally, in landlocked populations, females are
slightly heavier than males because of their high
fecundity (Applegate 1950). We also found this was
true. Although the sea lampreys at Holyoke Dam
were similar in length to those in the St. John River,
479
the average weight of Connecticut River fish was
considerably less (Table 1). The difference in average
weight between sea lampreys in the two populations
is not due to the difference in location of upstream
sampling sites, but possibly to differences in
energetic requirements, food supplies, or some
aspect of the environment during the oceanic
parasitic phase. A difference in weight between
populations has previously been found in landlocked
sea lampreys in the Great Lakes (Smith 1971).
Acknowledgments
This project was supported by Federal Aid Pro-
ject AFS-4-R-21 and D-J Project 5-29328 to the
Massachusetts Division of Fisheries and Wildlife and
the Massachusetts Cooperative Fishery Research
Unit. We thank P. Eschmeyer for a valuable review
of the manuscript.
Literature Cited
Applegate, V. C.
1950. Natural history of the sea lamprey, Petromyzon
marinus, in Michigan. U.S. Fish Wildl. Serv., Spec. Sci.
Rep.-Fish. 55, 237 p.
Beamish, F. W. H.
1980. Biology of the North American anadromous sea lam-
prey, Petromyzon marinus. Can. J. Fish. Aquat. Sci. 37:
1924-1943.
Beamish, F. W. H., and I. C. Potter.
1975. The biology of the anadromous sea lamprey (Petro-
myzon marinus) in New Brunswick. J. Zool. (Lond.) 177:
57-72.
Beamish, F. W. H., I. C. Potter, and E. Thomas.
1979. Proximate composition of the adult anadromous sea
lamprey, Petromyzon marinus, in relation to feeding, migra-
tion and reproduction. J. Anim. Ecol. 48:1-19.
BlGELOW, H. B., AND W. C. SCHROEDER.
1953. Fishes of the Gulf of Maine. U.S. Fish Wildl. Serv.,
Fish. Bull. 53:1-577.
Davis, R. M.
1967. Parasitism by newly-transformed anadromous sea lam-
preys on landlocked salmon and other fishes in a coastal
Maine lake. Trans. Am. Fish. Soc. 96:11-16.
Hardisty, M. W.
1954. Sex ratio in spawning populations of Lampetra
planeri. Nature (Lond.) 173:874-875.
Moffitt, C. M., B. Kynard, and S. G. Rideout.
1982. Fish passage facilities and anadromous fish restoration
in the Connecticut River basin. Fisheries (Bethesda) 7(6):
2-11.
Potter, I. C, F. W. H. Beamish, and B. G. H. Johnson.
1974. Sex ratios and lengths of adult sea lampreys (Petro-
myzon marinus) from a Lake Ontario tributary. J. Fish.
Res. Board Can. 31:122-124.
Ricker, W. E.
1975. Computation and interpretation of biological statistics
offish populations. Fish. Res. Board Can., Bull. 191:1-382.
Smith, B. R.
1971. Sea lampreys in the Great Lakes of North America.
In M. W. Hardisty and I. C. Potter (editors), The biology of
lampreys, Vol. 1, p. 207-247. Acad. Press, Lond.
Whitworth, W. R., P. L. Berrien, and W. T. Keller.
1976. Freshwater fishes of Connecticut. State Geol. Nat.
Hist. Serv. Conn., Dep. Environ. Prot., Bull. 101, 134 p.
WlGLEY, R. L.
1959. Life history of the sea lamprey of Cayuga Lake, New
York. U.S. Fish Wildl. Serv., Fish. Bull. 59:560-617.
Kathleen Stier
Boyd Kynard
Massachusetts Cooperative Fishery Research Unit
204 Holdworth Hall
University of Massachusetts
Amherst, MA 01003
AN IMPROVED
OTTER SURFACE SAMPLER
Field trials using a neuston sampler described by
Sameoto and Jaroszynski (1969) revealed serious
sampling problems associated with coastal waters
of British Columbia. Due to extensive freshwater
runoff in the vicinity of large rivers, sampling con-
ditions including choppy surface waters of lowered
salinity and vertically depressed distributions of
near-surface larval and juvenile fishes. Under such
conditions, the S-J sampler behaved erratically,
throwing considerable spray, and, when adjusted to
increase depth of tow, the body and control surfaces
deformed at speeds in excess of 5 knots. The modifi-
cations described here reflect our objectives of im-
proving performance, increasing durability, and
ease of handling, without increasing costs other than
those incurred by adding a flowmeter to provide
quantitative catches. The complete unit is depicted
in Figure 1.
Detailed Description
Sampler Box
Constructed of 1/8" marine aluminum, this alu-
minum is folded into a body with one welded seam
(Fig. 2). The leading edges are reinforced with 1/4"
aluminum for attaching the bridles and depressor.
The square mouth opening was sized to accomo-
date 0.25 m2 bongo nets having a circumference
of 185 cm. Body dimensions are 46 x 46 x 60
cm.
480
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
PERSPECTIVE - NEUSTON SAMPLER
swivel
Figure 1.— Neuston sampler with net cod-end attached.
Net Attachment
We replaced the grommet and bolt-through net
fastening system of the S-J sampler with an alu-
minum channel clamp (Fig. 2). Net slippage is pre-
vented by sewing a 1/4" rope into the net collar.
Stainless steel bolts remain permanently attached
to the sampler body so that, to mount or replace the
net, it is merely slid over the box and the channel
placed over the bolts and secured. One man can
replace the net in 5 min.
Lateral Wings
Individual fins bolt directly to the sides of the body
and are made of 1/8" aluminum with the inside edge
bent at 90° for an attachment face (Fig. 3). The
outer edge is bent downward 15° to stiffen it and
to reduce side slippage under tow. The wings
pivot on a bolt anteriorly and are adjusted through
a series of holes in the sampler body (Figs. 1,
2).
Depressor
Bolted directly to the body and adjusted as for the
wings (Figs. 1, 2), the depressor is made from 1/4"
marine aluminum bent at right angles on either end
for attachment (Fig. 3). It serves also as the lower
towing point and stiffens the body.
Tow Points
The sampler is adjusted in relation to the towing
vessel by a stainless steel turnbuckle on the upper
bridle (roll aspect), and by selecting the lower tow
point (depressor) and upper tow point (leading top
corner of the body) from a series of holes (Figs. 1,
2, 3). The tow point fastening is a threaded U-
bolt, fastened on both sides of the sampler frame
(Fig. 3).
Flotation
A streamlined float constructed of fiberglassed,
polyurethane foam which bolts to the upper face of
the body (Figs. 1, 2). At neutral buoyancy the
sampler floats with the mouth opening just below
the water surface. As with the S-J sampler, vertical
positioning under tow is the balanced outcome of
downward depressor force and lift from the lateral
fins. These adjustments are made to maintain an
8-10 cm headspace of air in the sampler while under
tow.
481
towing
points
0
towing
points
tow
direction
51cm -•
p— 47 cm - — h
/
PLAN VIEW FLOAT
6.3mm holes
10 cm centres
float bolts to
top of box
63mm x 25mm
stainless bolts
SIDE ELEVATION
6.3 x 25mm
stainless bolt
1.2 x 3cm
alum, channel
net collar with
rope sewn in
6.3mm rope
stainless nut
I5cm
47 cm
51 cm
NET ATTACHMENT DETAIL
L.SIDE ELEVATION FLOAT
to accept standard 1/4 m2
(184 cm circum) plankton net
EF
46cm
-46cm
B-
15x5 x 0.5cm
reinforcing pads
welded both
sides
9.5mm x 25mm
stainless bolt
5cm — ►
wing
depressor
^
32mm marine alum,
folded a welded at
one corner.
9.5mm x 38mm
stainless bolt
0 6.3mm holes
19mm o.c.
09.5 mm
holes
61cm
2.5cm
06.3mm
holes
BOX - FRONT ELEVATION
R=IOcm-
BOX- L.SIDE ELEVATION
Figure 2.— Scale drawings of the sampler body and float, and net attachment detail.
Flowmeter
A General Oceanics meter is attached inside the
body by means of a hinged strut which folds forward
to facilitate reading the meter (Figs. 1, 3). The meter
is free-pivoting in the horizontal plane and offset 17
cm from the center of the mouth opening.
Evaluation
This modified version of the otter neuston sampler
has been used extensively since 1981, offshore to
Station Papa (Mason et al. 1983) and in inside waters
under all weather conditions, including a full gale.
It performs best when towed into or across the wave
direction at 4-6 knots. At higher speeds, disturbance
due to backsplash from the fins and bridal may
cancel out potential advantage of further increase
in tow speed. Sampling efficiency is deemed to be
relatively high when using a 500 pjm mesh net at
night. Catches of juvenile fishes in the Strait of
Georgia are quantitatively comparable with those
482
51cm
5cm
15cm I—
09.5mm
holes
10cm
-—5cm
50cm
L WING -SIDE ELEVATION
strut
bend at 15°
from horiz.
-30°
WING -FRONT ELEVATION
strut 2.5cm wide 7
x 3.2mm thick /
weld
bend
h— 10cm
f— 10cm
45cm
45.75cm
heat
bene
90*
,'
6.3mm marine alum.
RHOcm-
2.5cm
~*l\
5cm -J
0 9.5mm holes
4cm o.c.
0 6.3mm holes
^_ 19mm o.c.
L.WING PLAN VIEW
DEPRESSOR- FRONT ELEVATION
SIDE ELEVATION
0 9.5mm threaded
brass rod
lock nut
012mm
alum, pipe
Top half hinge threaded
to accept brass rod
Hole cut in lower half of
hinge and in box to
accomodate lock nut.
0 6.3mm holes
6.3 mm
U bolt
DETAIL OF TOW POINTS
J
Leading edge,
bottom of sampler
stainless flathead
bolts c/w nuts
tow bridle
attaches here
FLOWMETER ATTACHMENT DETAIL
Figure 3.— Scale drawings of the depressor and wings, and tow point and flowmeter details.
made with a large volume, two-boat surface trawl
as employed by Barraclough et al. (1966). We found
no significant difference (student's £-test) between
mean total catch (12.9 and 12.1 fish/100 m3) for
nine taxa common to both gears in eight pairs of
tows made locally in the Strait of Georgia, British
Columbia, during March-April. Among the fish sam-
pled by this gear in offshore and shelf waters are
juvenile Pacific salmon to 14 cm, Pacific saury to
25 cm, juvenile sablefish, rockfish, greenlings, and
squid, in addition to the routine catches of ichthyo-
plankton and general zooplankton.
483
Literature Cited
Baraclough, W. E.
1967. Number, size and food of larval and juvenile fish caught
with a two-boat surface trawl in the Strait of Georgia, April
25-29, 1966. Fish. Res. Board Can., Biol. Stn. Nanaimo,
B.C., Manuscr. Rep. Ser. 922, 54 p.
Mason, J. C, R. J. Beamish, and G. A. McFarlane.
1983. Sexual maturity, fecundity, spawning, and early life
history of sablefish (Anoplopoma fimbria) off the Pacific
coast of Canada. Can. J. Fish. Aquat. Sci. 40:2126-2134.
Sameoto, D. D., and L. 0. Jaroszynski.
1969. Otter surface sampler: a new neuston net. J. Fish.
Res. Board Can. 26:2240-2244.
J. C. Mason
A. C. Phillips
Pacific Biological Station
Fisheries Research Branch
Department of Fisheries and Oceans
Nanaimo, British Columbia V9R 5K6, Canada
MORPHOLOGICAL EVIDENCE FOR
STARVATION AND PREY SIZE SELECTION
OF SEA-CAUGHT LARVAL SABLEFISH,
ANOPLOPOMA FIMBRIA
One of the major causes of larval mortality is star-
vation, this being related to the patchiness of food
resources (Hunter 1981). While starvation has been
induced under laboratory conditions [e.g., herring,
Clupea harengus, and plaice, Pleuronectes platessa
(Ehrlich et al. 1976); northern anchovy, Engraulis
mordax (O'Connell 1976); jack mackerel, Trachurus
symmetricus (Theilacker 1978, 1981)], starved lar-
vae have rarely been observed in nature (northern
anchovy, O'Connell 1980; jack mackerel, Theilacker
1986). Various methods have been used to charac-
terize starvation in fish larvae, including condition
factor (Blaxter 1971), chemical analyses (Ehrlich
1974), histological analyses (Umeda and Ochiai 1975;
O'Connell 1976, 1980; Theilacker 1978, 1986), and
morphological analyses (Shelbourne 1957; Nakai et
al. 1969; Ehrlich etal. 1976; Theilacker 1978, 1981,
1986). While histological and chemical analyses are
based on qualitative changes in tissues that result
from starvation, their methodologies require special
preservation techniques, negating their application
to samples preserved without these techniques in
mind. To characterize starvation in samples that
have not been specially preserved, measures of mor-
phology and/or condition factor are more appropri-
ately applied. In the present study, in the absence
of special preservation techniques, the occurrence
of starvation in sea-caught larval sablefish, Anoplo-
poma fimbria, was examined using morphological
measures.
The sablefish inhabits the continental shelf of the
North Pacific Ocean and is the subject of an inten-
sifying fishery off the west coast of North America,
yet little is known about the early life history of the
species. Recent evidence obtained off Canada sug-
gests that sablefish spawn in water deeper than 300
m, with spawning activity peaking in February.
Eggs (1.8-2.2 mm in diameter) descend while devel-
oping, and hatching probably occurs at depths in ex-
cess of 400 m (Mason et al. 1983). Although size at
hatching and the size at first feeding have not been
clearly defined, Mason et al. (1983) reported collect-
ing recently hatched larvae of 5-6 mm. After hatch-
ing, larvae ascend to surface waters and become
neustonic (Kendall and Clark 19821). Juveniles ap-
parently remain in shallow water until they mature.
Beyond reports of distribution (Kendall and Clark
fn. 1; Clark 19842) and descriptive work (e.g., Koba-
yashi 1957; Ahlstrom and Stevens 1976), studies of
larval and early juvenile sablefish have concentrated
on aging and growth (Boehlert and Yoklavich 1985;
Shenker and Olla in press).
Our aim in the present study was to detect the
possible occurrence of starvation in larval sablefish
collected off Washington and Oregon during April
and May 1980 (Kendall and Clark fn. 1), using
selected morphological measurements to determine
variability in larval condition. Further, to elucidate
the possible relationship between larval condition
and feeding requirements, prey size-selection and
diet were analyzed.
Methods
Sablefish larvae were collected by using a 0.5 m
neuston net (Sameoto and Jaroszynski 1969) with
0.505 mm mesh, towed for 10 min from the RV
Tikhookaenskiy , during the first cooperative U.S.-
U.S.S.R. ichthyoplankton survey off the Washing-
ton and Oregon coast in 1980 (Kendall and Clark
fn. 1). Larvae from stations 20, 24, 25, 34, 38, 50,
Kendall, A. W., 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, Seattle, WA
98112.
2Clark, J. B. 1984. Ichthyoplankton off Washington, Oregon
and Northern California, May-June 1981. Processed Rep. 84-11,
46 p. Northwest and Alaska Fisheries Center, National Marine
Fisheries Service, NOAA, Seattle, WA 98112.
484
FISHERY BULLETIN: VOL. 84, NO. 2, 1986.
54, 70, and 71 (Fig. 1), collected between 22 April
and 4 May 1980, formed the basis for this study. All
larvae were preserved in 10% Formalin3 at sea.
After sorting, larvae were switched into 5% For-
malin, where they remained until their examination
in 1983.
The following body measurements were recorded:
standard length (SL), head length (HL), eye
diameter (ED), body depth at pectoral (BD.P), and
body depth at anus (BD.A) (after Theilacker 1981).
Standard length was measured to the nearest 0.1
mm. All other measurements were made to the
nearest 0.05 mm using an ocular micrometer.
Because body proportions change dramatically with
size of larvae, it was necessary to restrict any com-
parisons to samples which were not statistically dif-
ferent in terms of the distribution of SL values. Also,
to minimize ambiguities attributable to slight dif-
ferences in size, comparisons of body measurements
were made using a ratio of the body measurement
to SL (e.g., HL/SL) as well as the absolute measure-
ment (mm). Because a number of larvae were dam-
aged prior to the time measurements were made
(e.g., eyes were missing, the gut was separated from
6Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
the body) the sample size (n) varied within a station.
To classify larval condition, statistical comparisons
of the body measurements were made using the
Mann- Whitney test (Zar 1974), a nonparamotric
rank procedure.
Food particle-size selection was examined by
measuring the widths of prey items ingested by 84
larvae from stations 24, 34, 50, 70, and 71. Soft-
bodied prey items were not measured due to the dif-
ficulty in accurately assessing their effective width.
All measurements were made using an ocular
micrometer at 40 x. Prey widths were originally
plotted for five size classes of larvae: 8.2-12.5,
12.6-16.5, 16.6-20.5, 20.6-24.5, and 24.6-28.5 mm
SL. The prey-size selection curve of larvae 12.6-16.5
mm closely approximated the curve of larvae
16.6-20.5 mm, and so these size classes were com-
bined. Similarly, the curves of larvae 20.6-24.5 mm
and 24.6-28.5 mm were essentially superimposed
one upon the other, and as a result these size classes
were also combined. This yielded three functional
sablefish size classes for particle-size analysis:
8.2-12.5, 12.6-20.5, and 20.6-28.5 mm SL.
The incidence of empty guts was recorded, and
diet was analyzed in terms of numerical percent
composition and frequency of occurrence of copepod
nauplii.
I30°W
-48°N
Figure 1.— Map of the Washington and Oregon coast where lar-
val sablefish were collected in 1980.
Results
Morphological Measurements
Out of a total of 56 larvae collected at station 25,
48% (27 larvae) appeared emaciated, in marked con-
trast to larvae collected at all other stations. This
emaciated condition, which we interpreted as evi-
dence of starvation, was present in 82% of the lar-
vae <12.5 mm SL (27 out of 32) collected at this sta-
tion but was absent in fish larger than 12.5 mm SL.
To test whether this interpretation, which was based
on a gross visual examination of these larvae, was
statistically verifiable, the morphology of the ema-
ciated larvae from station 25 was compared with lar-
vae of the same size from stations 20, 24, 34, 38,
50, 54, 70, and 71. The size range, 8.2-12.5 mm SL,
was selected as the broadest range over which the
distributions of SL values of these two groups were
equivalent, and excluded the two smallest larvae col-
lected at station 25 from the comparisons. Signifi-
cant differences were observed in seven of eight
body measurements, indicating that distinct dif-
ferences were present in the larvae from station 25
when compared with larvae of similar size from all
other stations (Table 1).
485
Table 1 .—A comparison of median values of body measurements of Anoplopoma fim-
bria larvae from station 25 with larvae from stations 20, 24, 34, 38, 50, 54, 70, and
71. The size range was 8.2-12.5 mm SL.
Stations 20, 24,
34, 38, 50, 54,
Station 25
70, and 71
P1
Standard length, SL (mm)
10.0
10.25
>0.20
95% Confidence Interval, C.I.
(9.2-10.4)
(10.0-10.5)
n2 =
25
118
Head length, HL (mm)
1.5
2.1
<0.001
95% C.I.
(1.4-1.8)
(2.0-2.1)
HL/SL
0.165
0.200
<0.001
95% C.I.
(0.147-0.177)
(0.194-0.206)
n =
25
114
Eye diameter, ED (mm)
0.7
0.85
<0.001
95% C.I.
(0.6-0.7)
(0.8-0.9)
ED/SL
0.069
0.082
<0.001
95% C.I.
(0.066-0.073)
(0.081-0.084)
n =
23
113
Body depth at pectoral, BD.P (mm)
1.0
1.3
<0.001
95% C.I.
(0.9-1.15)
(1.3-1.3)
BD.P/SL
0.109
0.128
<0.001
95% C.I.
(0.098-0.118)
(0.125-0.131)
n »
13
100
Body depth at anus, BD.A (mm)
1.0
1.2
<0.005
95% C.I.
(0.7-1.2)
(1.15-1.25)
BD.A/SL
0.104
0.116
>0.10
95% C.I.
(0.082-0.139)
(0.112-0.118)
n »
11
84
1P = probability that body measurements of station 25 larvae were equivalent with larvae from
stations 20, 24, 34, 38, 50, 54, 70, and 71, as determined by the Mann-Whitney test.
2The sample size was not constant within each group because some larvae were damaged prior
to the time measurements were made (e.g., some had lost eyes, the gut was separated from the body).
Analysis of Gut Contents
Examination of the gut contents of larvae <12.5
mm SL provided further evidence as to the starved
condition of the larvae at station 25. At this station
75% of the larvae (24 out of 32) had no food in their
guts, and 9% (3 larvae) had ingested 2 or fewer prey
items. In addition to being empty, the guts of lar-
vae collected at station 25 were shrunken, which is
reflective of poor feeding conditions (Nakai et al.
1969). At all other stations the incidence of empty
guts for larvae <12.5 mm SL was <1%, as was the
incidence of larvae ingesting 2 or fewer prey
items.
Circumstantial evidence as to the cause of star-
vation comes from food analyses. It was apparent
that while sablefish larvae selected increasingly
larger prey as they grew larger, the minimum size
of prey eaten did not increase appreciably. By ex-
amining the widths of all prey items ingested by
larvae of different lengths (Fig. 2), three general
patterns emerged: 1) Larvae 8.2-12.5 mm SL prin-
cipally ingested the narrowest prey (0.01-0.10 mm
in width), 2) larvae 12.6-20.5 mm SL ingested
slightly larger prey (0.11-0.20 mm in width), and
3) sablefish 20.6-28.5 mm SL primarily ingested the
largest prey (0.21-0.30 mm in width), although they
also ingested a broad range of prey sizes.
Copepod nauplii were the dominant small prey,
and were all <0.20 mm wide. They accounted for
88.3% of the diet (by number) of small larvae (<12.5
mm). Based on prey-size selection alone (Fig. 2), it
appears that copepod nauplii may have also contrib-
uted substantially to the diet of larvae 12.6-20.5 mm
SL, but not to the diet of fish 20.6-28.5 mm SL.
Dietary analysis confirmed this, with nauplii com-
prising 26.9% of the diet of larvae 12.6-20.5 mm,
but merely 1.4% of the diet offish 20.6-28.5 mm SL.
Considering the relative importance of copepod
nauplii in the diet of larvae 12.6-20.5 mm SL and
the fact that this size class continued to ingest
nauplii although capable of ingesting larger prey,
the frequency of occurrence of copepod nauplii in
the guts of these larvae was examined at each sta-
tion as inferential evidence of the abundance or
availability of copepod nauplii (Table 2). At station
25 only 27% of larvae 12.6-20.5 mm SL ingested
nauplii compared with 60-100% at all other stations;
the low frequency of occurrence of nauplii in guts
of these larvae at station 25 was obtained even
though no guts were empty. These data indicate that
copepod nauplii may not have been abundant or
486
bT
o
50
\
•
A
^•-^8.2 -12.5 mm SL
° — ° 12.6-20.5 mm SL
o
t \
• •20.6-28.5 mm SL
t 40
CO
o
Q_
O 30
O
- i
1
1
~ 1
'V
A
\ \
\ \
\
o
PERCENT
o o
1
-1
1 1
> /
/ \
\ \
•
\
•
\
\\
\\
i
V~-
\ _
T-mQ,
0<
8 A i
i
0
.01-
0.1 1-
0.21-
0.31-
0.41-
0.51- 0.61- 0.71- 0.81-
0.91
0
.10
0.20
0.30
0.40
0.50
0.60 0.70 0.80 0.90
1.00
PREY WIDTH (mm)
Figure 2.— The size of prey selected by larval sablefish, plotted for three size classes of larvae: 8.2-12.5 mm
SL (n = 43), 12.6-20.5 mm SL (n = 25), and 20.6-28.5 mm SL (n = 16).
Table 2. — Frequency of occurrence of copepod nauplii found in the guts of larval sable-
fish, by size class and station.
Station number
Size class
20
24
25
34 38 50
54
70
71
<12.5 mm
12.6-20.5 mm
38/38
1 00%
6/10
60%
6/6
100%
2/2
100%
!7/32
22%
4/15
27%
9/9 32/32 6/6
100% 100% 100%
8/8 11/11 1/1
100% 100% 100%
15/16
94%
3/3
100%
10/10
100%
10/11
91%
11/12
92%
2/3
67%
1This includes 24 larvae <12.5 mm SL with empty guts.
readily available at station 25, with the high in-
cidence of starvation at this station suggesting a
cause-and-effect relationship between these two
factors.
Discussion
There is no definitive way of discerning whether
the sablefish larvae that we categorized as starv-
ing had starved to the "point of no return". To
ascertain whether sea-caught larvae have starved
beyond recovery requires rearing larvae from eggs
in the laboratory under different feeding regimes,
and using these as standards of comparison for sea-
caught specimens. Unfortunately, this has been done
in only a few cases. For example, O'Connell (1976)
established histological criteria for starvation under
laboratory conditions for the northern anchovy.
These criteria were then employed to identify starv-
ing larvae collected in the Southern California Bight
(O'Connell 1980). The proportion of starving larvae
was estimated to be 8%, for larvae <7.5 mm SL,
with this representing 40% of the daily rate of mor-
tality. In a more recent and comprehensive study,
Theilacker (1986) utilized both histological and mor-
phological criteria (Theilacker 1978, 1981) to ex-
amine starvation of sea-caught first-feeding jack
mackerel in the Southern California Bight. She
determined that starvation varied with habitat. In
the open ocean, the number of larvae <3.5 mm dying
487
of starvation per day was 57-70%, whereas only
6-12% of the first-feeding larvae collected near
islands and banks were starving.
Until techniques are developed for rearing sable-
fish from eggs, we are limited to utilizing com-
parisons of sea-caught larvae to infer the importance
of starvation in the early life history of this species.
While starving larvae were observed at only one sta-
tion, our finding confirms that sablefish larvae do
encounter suboptimal environmental conditions in
the sea. However, neither the transience nor geo-
graphic extent of this phenomenon can be assessed
in the absence of an intensive sampling scheme
designed specifically to answer these questions.
Although definitive plankton composition data are
lacking, the occurrence of starving larvae at station
25 appears to reflect a paucity of copepod nauplii.
While appropriate prey concentrations (Laurence
1974; Lasker 1975; Houde 1978), particle size
(Lasker 1975; Hunter 1981), and prey species com-
position (Lasker 1975; Scura and Jerde 1977) all
relate to the survival and growth of marine fish lar-
vae, not all larvae are able to maintain associations
with suitable prey patches. Lasker (1975) empha-
sized the transient nature of optimal feeding condi-
tions in the sea, noting that northern anchovy lar-
vae which had been associated with a good feeding
patch (a bloom of Gymnodinium splendens that per-
sisted for 18 d) would probably die of starvation
after a wind storm broke up the bloom. Patchiness
of food resources has also been suggested by the
station-to-station variability in growth rates of
northern anchovy (as determined from daily incre-
ments of otoliths) (Methot and Kramer 1979).
Similarly, after monitoring larval development in
both good and bad plankton patches, Shelbourne
(1957) reported that a scarcity of appropriate food
resulted in a deterioration of the physical condition
of plaice larvae.
Where morphological measurements of larvae are
concerned, changes in body measurements which
result from handling and preservation techniques
must be considered. Net abrasion results in mech-
anical damage to the larvae (Blaxter 1971) as well
as shrinkage (Blaxter 1971; Theilacker 1980), with
the amount of shrinkage depending on whether
death preceded fixation (Blaxter 1971), and the ex-
tent of handling (Theilacker 1980). The type of fix-
ative used (Theilacker 1980), its concentration,
salinity, and temperature (Hay 1982) also affect the
degree of shrinkage. In the present case, shrinkage
most likely occurred during the 3 yr these larvae
were held in Formalin. However, absolute lengths
may not be critical to evaluating the significance of
our findings, and the differences that were seen be-
tween stations could not have resulted simply from
differences in shrinkage. This was clear from the
qualitative differences in gut appearance seen
between stations (i.e., shrunken and empty guts ver-
sus guts filled to distention). Further, since the
sablefish larvae we examined were all caught and
preserved during the same cruise, we assumed that
whatever shrinkage that may have resulted from
handling and preservation techniques is constant
throughout the samples.
Larval fishes are limited in the prey that they con-
sume by their ability to capture and process it. As
they grow, larvae become very successful predators,
caused in part by an increase in mouth size. As a
result, the size of prey selected increases as devel-
opment proceeds. Prey width was used to examine
prey-size selection because prey width appears to
be the critical dimension for the successful inges-
tion of oblong prey by larval fishes (Blaxter 1965;
Arthur 1976; Hunter 1981). For sablefish, definitive
shifts in the size of prey consumed occurred at about
12.5 and 20.5 mm SL. The diet of the larger larvae
was more diverse than the diet of small larvae. This
expansion of the range of prey selected is not un-
common (e.g., Hunter 1981) and is adaptive inas-
much as it enables larvae to ingest suboptimal prey
items at times when optimal or preferred prey are
not available. Smaller fish appear limited in the size
of prey they can exploit. This limitation, combined
with larvae <12.5 mm SL being associated with an
unsuitable prey patch at station 25, may have been
responsible for the high incidence of empty guts and
starvation.
Acknowledgments
We wish to thank Kevin Bailey, George Boehlert,
and two anonymous reviewers for their comments
on drafts of this manuscript. Thanks also to Michael
Davis and Steve Ferraro for their advice on statis-
tical analyses, and Art Kendall for valuable discus-
sions and continual encouragement.
This work was supported by the Northwest and
Alaska Fisheries Center, National Marine Fisheries
Service, NOAA Contract No. 83-ABC-00045.
Literature Cited
Ahlstrom, E. H., and E. Stevens.
1976. Report of neuston (surface) collections made on an ex-
tended CalCOFI cruise during May 1972. Calif. Coop.
Oceanic Fish. Invest. Rep. 18:167-180.
Arthur, D. K.
1976. Food and feeding of larvae of three fishes occurring
488
in the California Current, Sardinops sagax, Engraulis mor-
dax, and Trachurus symmetricus. Fish. Bull., U.S. 74:
517-530.
Blaxter, J. H. S.
1965. The feeding of herring larvae and their ecology in rela-
tion to feeding. Calif. Coop. Oceanic Fish. Invest. Rep. 10:
79-88.
1971. Feeding and condition of clyde herring larvae. Rapp.
P.-v. Reun. Cons. int. Explor. Mer 160:128-136.
BOEHLERT, G. W., AND M. M. YOKLAVICH.
1985. Larval and juvenile growth of sablefish, Anoplopoma
fimbria, as determined from otolith increments. Fish. Bull.,
U.S. 83:475-481.
Ehrlich, K. F.
1974. Chemical changes during growth and starvation of her-
ring larvae. In J. H. S. Blaxter (editor), The early life
history of fish, p. 301-323. Springer- Verlag, Berlin.
Ehrlich, K. F., J. H. S. Blaxter, and R. Pemberton.
1976. Morphological and histological changes during the
growth and starvation of herring and plaice larvae. Mar.
Biol. (Berl.) 35:105-118.
Hay, D. E.
1982. Fixation shrinkage of herring larvae: effects of salin-
ity, formalin concentration, and other factors. Can. J. Fish.
Aquat. Sci. 39:1138-1143.
Houde, E. D.
1978. Critical food concentrations for larvae of three species
of subtropical marine fishes. Bull. Mar. Sci. 28:395-
411.
Hunter, J. R.
1981. Feeding ecology and predation of marine fish larvae.
In R. Lasker (editor), Marine fish larvae: morphology,
ecology, and relation to fisheries, p. 33-77. Sea Grant Pro-
gram, Univ. Wash. Press, Seattle.
KOBAYASHI, K.
1957. Larvae and youngs of the sablefish, Anoplopoma fim-
bria (Pallas), from the sea near the Aleutian Islands. [In
Jpn., Engl, abstr.] Bull. Jpn. Soc. Sci. Fish. 23:376-382.
Lasker, R.
1975. Field criteria for survival of anchovy larvae: The rela-
tion between inshore chlorophyll maximum layers and suc-
cessful first feeding. Fish. Bull., U.S. 73:453-462.
Laurence, G. C.
1974. Growth and survival of haddock Melanogrammus aegle-
finus larvae in relation to planktonic prey concentration. J.
Fjsh. Res. Board Can. 31:1415-1419.
Mason, J. C, R. J. Beamish, and G. A. McFarlane.
1983. Sexual maturity, fecundity, spawning, and early life
history of sablefish (Anoplopoma fimbria) off the Pacific
coast of Canada. Can. J. Fish. Aquat. Sci. 40:2126-
2134.
Methot, R. D., Jr., and D. Kramer.
1979. Growth of northern anchovy, Engraulis mordax, lar-
vae in the sea. Fish. Bull., U.S. 77:413-423.
Nakai, Z., M. Kosaka, M. Ogura, G. Hayashida, and H. Shimo-
zono.
1969. Feeding habit, and depth of body and diameter of
digestive tract of shirasu, in relation with nutritious condi-
tion. [In Jpn., Engl, abstr.] J. Coll. Mar. Sci. Technol.,
Tokai Univ. 3:23-34.
O'Connell, C. P.
1976. Histological criteria for diagnosing the starving con-
dition in early post yolk sac larvae of the northern anchovy,
Engraulis mordax Girard. J. Exp. Mar. Biol. Ecol. 25:
285-312.
1980. Percentage of starving northern anchovy, Engraulis
mordax, larvae in the sea as estimated by histological
methods. Fish. Bull., U.S. 78:475-489.
Sameoto, D. D., and L. O. Jaroszynski.
1969. Otter surface sampler: a new neuston net. J. Fish.
Res. Board Can. 26:2240-2244.
Scura, E. D., and C. W. Jerde.
1977. Various species of phytoplankton as food for larval
northern anchovy, Engraulis mordax, and relative nutri-
tional value of the dinoflagellates Gymnodinium splendens
and Gonyaulax polyedra. Fish. Bull., U.S. 75:577-583.
Shelbourne, J. E.
1957. The feeding and condition of plaice larvae in good and
bad plankton patches. J. Mar. Biol. Assoc. U.K. 36:539-552.
Shenker, J. M., and B. L. Olla.
In press. Laboratory feeding and growth of early juvenile
sablefish, Anoplopoma fimbria. Can. J. Fish. Aquat. Sci.
Theilacker, G. H.
1978. Effect of starvation on the histological and morpho-
logical characteristics of jack mackerel, Trachurus sym-
metricus, larvae. Fish. Bull., U.S. 76:403-414.
1980. Changes in body measurements of larval northern an-
chovy, Engraulis mordax, and other fishes due to handling
and preservation. Fish. Bull., U.S. 78:685-692.
1981. Effect of feeding history and egg size on the morphol-
ogy of jack mackerel, Trachurus symmetricus, larvae.
Rapp. P.-v. Reun. Cons. int. Explor. Mer 178:432-440.
1986. Starvation-induced mortality of young sea-caught jack
mackerel, Trachurus symmetricus, determined with
histological and morphological methods. Fish. Bull., U.S.
84:1-17.
Umeda, S., and A. Ochiai.
1975. On the histological structure and function of digestive
organs of the fed and starved larvae of the yellowtail, Seriola
quinqueradiata. [In Jpn., Engl, abstr.] Jpn. J. Ichthyol.
21:213-219.
Zar, J. H.
1974. Biostatistical analysis. Prentice-Hall, Englewood
Cliffs, NJ, 620 p.
Jill J. Grover
College of Oceanography
Oregon State University
Hatfield Marine Science Center
Newport, OR 97365
Bori L. Olla
Cooperative Institute for Marine Resources Studies
Northwest and Alaska Fisheries Center
National Marine Fisheries Service, NOAA
Hatfield Marine Science Center
Newport, OR 97365
489
NOTICES
NOAA Technical Reports NMFS published during last 6 months of 1985
Technical Report NMFS
31. Shark catches from selected fisheries off the U.S. east coast. July 1985,
iii + 22 p.
Analysis of various sources of pelagic shark catches in the Northwest
and Western Central Atlantic Ocean and Gulf of Mexico with com-
ments of other large pelagics. By Emory D. Anderson, p. 1-14, 3
figs., 17 tables.
Estimated catches of large sharks by U.S. recreational fishermen in
the Atlantic and Gulf of Mexico. By John G. Casey and John J. Hoey
p. 15-19, 5 tables.
The incidental capture of sharks in the Atlantic United States Fishery
Conservation Zone reported by the Japanese tuna longline fleet. By
W. N. Witzell, p. 21-22, 3 tables.
32 . Nutrient distributions for Georges Bank and adjacent waters in 1979. By
A. F. J. Draxler, A. Matte, R. Waldhauer, and J. E. O'Reilly.
July 1985, iii + 34 p., 32 figs., 2 tables.
33. Marine flora and fauna of the Northeastern United States. Echinoder-
mata: Echinoidea. By D. Keith Serafy and F. Julian Fell. September
1985, iii + 25 p., 42 figs.
34. Additions to a revision of the shark genus Carcharhinus: synonymy of
Aprionodon and Hypoprion, and description of a new species of Car-
charhinus (Carcharhinidae). By J. A. F. Garrick. November 1985, iii
+ 26 p., 14 figs., 4 tables.
35. Synoptic review of the literature on the Southern Oyster Drill Thais
haemastomafloridana. By Philip A. Butler. November 1985, iii + 9 p.
36. An egg production method for estimating spawning biomass of pelagic
fish: application to the northern anchovy, Engraulis mordax. Reuben
Lasker (editor). December 1985, iii + 99 p.
Introduction: an egg production method for anchovy biomass assess-
ment. By Reuben Lasker, p. 1-3, 1 fig.
Biomass model for the egg production method. By Keith Parker, p.
5-6.
Parameter estimation for an egg production method of northern an-
chovy biomass assessment. By Susan Picquelle and Gary Stauffer,
p. 7-15, 8 figs., 6 tables.
Sea survey design and analysis for an egg production method of an-
chovy biomass assessment. By Paul E. Smith and Roger P. Hewitt,
p. 17-26, 4 figs., 8 tables.
The CalCOFI vertical egg tow (CalVET) net. By Paul E. Smith,
William Flerx, and Roger P. Hewitt, p. 27-32, 5 figs., 1 table.
Procedures for sorting, staging, and ageing eggs. By Gary Stauffer
and Susan Picquelle, p. 33-35.
Staging anchovy eggs. By H. Geoffrey Moser and Elbert H. Ahlstrom,
p. 37-41, 2 figs.
A model for temperature-dependent northern anchovy egg develop-
ment and an automated procedure for the assignment of age to staged
eggs. By Nancy C. H. Lo, p. 43-50, 2 figs., 6 tables.
A protocol for designing a sea survey for anchovy biomass assess-
ment. By Robert P. Hewitt, p. 51-53.
Sampling requirements for the adult fish survey. By Susan Picquelle,
p. 55-57, 1 fig.
Spawning frequency of Peruvian anchovies taken with a purse seine.
By Jurgen Alheit, p. 59-61, 1 table.
Preservation of northern anchovy in formaldehyde solution. By J. Roe
Hunter, p. 63-65, 1 fig., 1 table.
490
Batch fecundity in multiple spawning fishes. By J. Roe Hunter, Nancy
C. H. Lo, and Roderick J. H. Leong, p. 67-77, 6 figs., 5 tables.
Measurement of spawning frequency in multiple spawning fishes. By
J. Roe Hunter and Beverly J. Macewicz, p. 79-94, 7 figs., 1 table.
Comparison between egg production method and larval census method
for fish biomass assessment. By Roger P. Hewitt, p. 95-99, 2 figs.,
1 table.
Some NOAA publications are available by purchase from the Superintendent of Documents, U.S.
Government Printing Office, Washington, DC 20402.
491
> 4 S3 - $6
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LO, NANCY C. H. Modeling life-stag itaneous mortality rates, an
application to northern anchovy, Engt • eggs and larvae 395
SEN, A. R. Methodological problem? ommercial rockfish landings . . . 409
POLOVINA, JEFFREY J. A varial v version of the Leslie model with
application to an intensive fishi; i a multispecies stock 423
MATSUURA, YASUNOBU, and TAKUMI YONEDA. Early development
of the lophid anglerfish, Lophv; ophysus 429
SQUIRES, DALE. Ex-vessel pric in the New England fishing industry .. 437
LEBER, KENNETH M., and I I ( & GREENING. Community studies in seagrass
meadows: A comparison of t or sampling macroinvertebrates and
fishes 443
Notes
OXENFORD, HAZEL A. AYNE HUNTE. A preliminary investigation of the
stock structure of the dolphin, Coryphaena hippurus, in the western central
Atlantic 451
FORWARD, RICHARD B., JR., BLANCA ROJAS de MENDIOLA, and RICHARD T.
BARBER. Effects of temperature on swimming speed of the dinoflagellate Gym-
nodinium splendens 460
GRAHAM, JEFFREY B., RICHARD H. ROSENBLATT, and DARCY L. GIBSON.
Morphology and possible swimming mode of a yellowfin tuna, Thunnus aWacares, lack-
ing one pectoral fin 463
RATTY, F. J., Y. C. SONG, and R. M. LAURS. Chromosomal analysis of albacore, Thun-
nus alalunga, and yellowfin, Thunnus albacares, and skipjack, Katsuwonus pelamis,
tuna 469
STIER, KATHLEEN, and BOYD KYNARD. Abundance, size, and sex ratio of adult
sea-run sea lamprey, Petromyzon marinus, in the Connecticut River 476
MASON, J. C, and A. C. PHILLIPS. An improved otter surface sampler 480
GROVER, JILL J., and BORI L. OLLA. Morphological evidence for starvation and
prey size selection of sea-caught larval sablefish, Anoplopoma fimbria 484
Notices 490
• GPO 593-096
MBL WHOI LIBRARY
UH nwB G
J?
^TO'ca
C
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—__--_-_-__-«-_-_-—-——_
Vol. 84, No. 3
July 1986
PRINCE, ERIC D., DENNIS W. LEE, CHARLES A. WILSON, and JOHN M. DEAN.
Longevity and age validation of a tag-recaptured Atlantic sailfish, Istiopfwrus platypterus,
using dorsal spines and otoliths 493
PARRISH, RICHARD H, DONNA L. MALLICOATE, and RICHARD A. KLINGBEIL.
Age dependent fecundity, number of spawnings per year, sex ratio, and maturation stages
in northern anchovy, Engraulis mordax 503
PENNINGTON, MICHAEL. Some statistical techniques for estimating abundance indices
from trawl surveys 519
REILLY, STEPHEN B., and JAY BARLOW. Rates of increase in dolphin population
size 527
ATKINSON, C. ALLEN. Discrete-time difference model for simulating interacting fish
population dynamics 535
PARSONS, D. G., and G. E. TUCKER. Fecundity of northern shrimp, Pandcdus borealis,
(Crustacea, Decapoda) in areas of the Northwest Atlantic 549
WAHLEN, BRUCE E. Incidental dolphin mortality in the eastern tropical Pacific tuna
fishery, 1973 through 1978 559
SOMERTON, DAVID A, and ROBERT S. OTTO. Distribution and reproductive biology
of the golden king crab, Lithodes aequispina, in the eastern Bering Sea 571
POWER, JAMES H. A model of the drift of northern anchovy, Engraidis mordax, larvae
in the California Current 585
JOHNSON, PHYLLIS T Parasites of benthic amphipods: dinoflagellates (Duboscquodinida:
Syndinidae) 605
YANG, M. S., and P. A LIVINGSTON. Food habits and diet overlap of two congeneric
species, Antheresthes stomias and Atheresthes evermanni, in the eastern Bering
Sea 615
SHEPARD, ANDREW N., ROGER B. THEROUX, RICHARD A. COOPER, and JOSEPH
R. UZMANN. Ecology of Ceriantharia (Coelenterata, Anthozoa) of the northwest Atlantic
from Cape Hatteras to Nova Scotia 625
POTTHOFF, THOMAS, SHARON KELLEY, and JOAQUIN C. JAVECH. Cartilage and
bone development in scombroid fishes 647
REIS, ENIR GIRONDI. Age and growth of the marine catfish, Netuma barba (Siluri-
formes, Ariidae), in the estuary of the Patos Lagoon (Brasil) 679
DANDONNEAU, YVES. Monitoring the sea surface chlorophyll concentration in the
tropical Pacific: consequences of the 1982-83 El Nino 687
(Continued on back cover)
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NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION
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NATIONAL MARINE FISHERIES SERVICE
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Fishery Bulletin
The Fishery Bulletin carries original research reports and technical notes on investigations in fishery science, engineering, and economics.
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National Marine Fisheries Service, NOAA
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National Marine Fisheries Service National Marine Fisheries Service
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Fishery Bulletin
CONTENTS
Vol. 84, No. 3 July 1986
PRINCE, ERIC D., DENNIS W. LEE, CHARLES A. WILSON, and JOHN M. DEAN.
Longevity and age validation of a tag-recaptured Atlantic sailfish, Istiophorus platypterus,
using dorsal spines and otoliths 493
PARRISH, RICHARD H., DONNA L. MALLICOATE, and RICHARD A. KLINGBEIL.
Age dependent fecundity, number of spawnings per year, sex ratio, and maturation stages
in northern anchovy, Engraulis mordax 503
PENNINGTON, MICHAEL. Some statistical techniques for estimating abundance indices
from trawl surveys 519
REILLY, STEPHEN B., and JAY BARLOW. Rates of increase in dolphin population
size 527
ATKINSON, C. ALLEN. Discrete-time difference model for simulating interacting fish
population dynamics 535
PARSONS, D G., and G E. TUCKER. Fecundity of northern shrimp, Pandalus borealis,
(Crustacea, Decapoda) in areas of the Northwest Atlantic 549
WAHLEN, BRUCE E. Incidental dolphin mortality in the eastern tropical Pacific tuna
fishery, 1973 through 1978 559
SOMERTON, DAVID A., and ROBERT S. OTTO. Distribution and reproductive biology
of the golden king crab, Lithodes aequispina, in the eastern Bering Sea 571
POWER, JAMES H. A model of the drift of northern anchovy, Engraulis mordax, larvae
in the California Current 585
JOHNSON, PHYLLIS T Parasites of benthic amphipods: dinoflagellates (Duboscquodinida:
Syndinidae) 605
YANG, M. S., and P. A. LIVINGSTON. Food habits and diet overlap of two congeneric
species, Antheresthes stomias and Atheresthes evermanni, in the eastern Bering
Sea 615
SHEPARD, ANDREW N, ROGER B. THEROUX, RICHARD A. COOPER, and JOSEPH
R. UZMANN. Ecology of Ceriantharia (Coelenterata, Anthozoa) of the northwest Atlantic
from Cape Hatteras to Nova Scotia 625
POTTHOFF, THOMAS, SHARON KELLEY, and JOAQUIN C. JAVECH. Cartilage and
bone development in scombroid fishes 647
REIS, ENIR GIRONDI. Age and growth of the marine catfish, Netuma barba (Siluri-
formes, Ariidae), in the estuary of the Patos Lagoon (Brasil) 679
DANDONNEAU, YVES. Monitoring the sea surface chlorophyll concentration in the
tropical Pacific: consequences of the 1982-83 El Nino 687
I M«rtn« BMogteat Uboraton
(Continued on next page)
Seattle, Washington
1986
For sale by the Superintendent of Documents, U.S. Government Printing Office, W
DC 20402— Subscription price per year: $21.00 domestic and $26.25 foreign. Cost per single
issue: $6.50 domestic and $8.15 foreign.
OCT 6 1986
Woods Hole. Mass.
Contents— Continued
ROGERS, S. GORDON, HIRAM T. LANGSTON, and TIMOTHY E. TARGETT. Ana-
tomical trauma to sponge-coral reef fishes captured by trawling and angling .... 697
QUAST, JAY C. Annual production of eviscerated body weight, fat, and gonads by
Pacific herring, Clupea harengus pallasi, near Auke Bay, southeastern Alaska . . . 705
WENNER, CHARLES A., WILLIAM A. ROUMILLAT, and C. WAYNE WALTZ. Con-
tributions to the life history of Black sea bass, Centropristis striata, off the south-
eastern United States 723
Notes
LENARZ, WILLIAM H., and TINA WYLLIE ECHEVERRIA. Comparison of visceral
fat and gonadal fat volumes of yellowtail rockfish, Sebastes flavidus, during a normal
year and a year of El Nino conditions 743
SORENSEN, PETER W, MARCO L. BIANCHINI, and HOWARD E. WINN. Diel
foraging activity of American eels, Anguilla rostrata (Lesueur), in a Rhode Island
estuary 746
KILLAM, KRISTIE, and GLENN PARSONS. First record of the longfin mako, Isurus
paucus, in the Gulf of Mexico 748
STIER, KATHLEEN, and BOYD KYNARD Movement of sea-run sea lampreys, Petro-
myzon marinus, during the spawning migration in the Connecticut River 749
HOGANS, W E., and P. C. F. HURLEY. Variations in the morphology of Fistulicola
plicatus Rudolphi (1802) (Cestoda:Pseudophyllidea) from the swordfish, Xiphias gladius
L., in the Northwest Atlantic Ocean 754
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 ap-
proves, recommends or endorses any proprietary product or proprietary material
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ly the advertised product to be used or purchased because of this NMFS publication.
LONGEVITY AND AGE VALIDATION OF A TAG-RECAPTURED
ATLANTIC SAILFISH, ISTIOPHORUS PLATYPTERUS,
USING DORSAL SPINES AND OTOLITHS
Eric D. Prince,1 Dennis W. Lee,1 Charles A. Wilson,2
and John M. Dean3
ABSTRACT
A tagged female Atlantic sailfish, Istiophorus platypterus, of 24.6 kg (54 lb) was recaptured on 14 January
1984, after being at large for 10 yr and 10 mo (4,025 d). Approximate age based on tagging records
ranged from at least 13 to 15 + yr. Maximum estimated longevity of this species was therefore revised
upwards from previously reported >7 yr to at least 13-15+ yr. Estimates of age based on sections of
dorsal spine numbers 3-6 ranged from 2 to 8 yr and substantially underestimated the range in age known
from tagging records (13-15 + yr). This discrepancy was due to enlargement of the porous, vascularized
core of spine sections which obscured zonations associated with early growth history. Thus, dorsal spines
do not appear to be useful in ageing older sailfish (i.e., >5 yr). Age estimates from sagittae (otoliths)
were 13 yr based on scanning electron microscope counts of external ridges and analysis of internal otolith
microstructure. Otolith age, therefore, agreed with age known from tagging records. The relatively large
size of the sagitta (7.84 mg) also provides additional evidence that the otolith could be from a very old
sailfish. These data strongly suggest that in older, larger sailfish (>5 yr, 22.7 kg), sagittae, rather than
dorsal spines, should be used as the source of age and growth information.
The Atlantic sailfish, Istiophorus platypterus, is one
of the most popular recreational fishes along the
U.S. Atlantic coast, Gulf of Mexico, and Caribbean
Sea. In fact, this species has been described as the
most sought after fish by southeast marine charter
boat anglers, particularly in south Florida (Ellis
1957). Although most landings of Atlantic sailfish
in the southeastern United States are made by
recreational anglers, many are also taken inciden-
tally by domestic and foreign commercial longline
vessels (Lopez et al. 1979). The biological informa-
tion presently used in stock assessments of Atlan-
tic sailfish (Conser 1984) consists of age and growth
data derived exclusively from analysis of dorsal
spines (Jolley 1974, 1977; Hedgepeth and Jolley
1983). However, uncertainties remain concerning
Atlantic sailfish age structure, longevity, choice of
skeletal structure for ageing, and rate of growth
because of inconsistencies reported in the literature.
In addition, the accuracy of age and growth esti-
1 Southeast Fisheries Center Miami Laboratory, National Marine
Fisheries Service, NOAA, 75 Virginia Beach Drive, Miami, FL
33149-1099.
2BeIle W. Baruch Institute for Marine Biology and Coastal
Research, Department of Biology and Marine Science Program,
University of South Carolina, Columbia, SC 29208; present ad-
dress: Coastal Ecology and Fisheries Institute, Louisiana State
University, Baton Rouge, LA 70803-7503.
3Belle W. Baruch Institute for Marine Biology and Coastal
Research, Department of Biology and Marine Science Program,
University of South Carolina, Columbia, SC 29208.
mates from skeletal structures and length-frequency
analyses have not been validated for all age classes
(de Sylva 1957; Jolley 1974, 1977; Radtke and Dean
1981; Hedgepeth and Jolley 1983).
One problem in using spines as a source of age
and growth information is the tendency of the
vascularized core to obscure zonations associated
with early growth history. The enlargement of the
vascularized core and subsequent reabsorption of
tissues are most severe in the largest and oldest
specimens (causing underestimates of true age) and
have contributed to the lack of detailed information
for older age classes. Several studies have also
reported difficulty in interpreting the double and tri-
ple bands often observed in Atlantic sailfish spines
(Jolley 1977; Hedgepeth and Jolley 1983). These
problems are not unique to sailfish (Casselman 1983;
Compean- Jimenez and Bard 1983) and have resulted
in an unusually large proportion of spine samples
(as much as 76%) being rejected for age and growth
analysis (Jolley 1977). Radtke and Dean (1981)
reviewed this problem and suggested that otoliths
(sagittae) may be a better skeletal structure for age
and growth assessment in sailfish because these
structures do not have the disadvantages associated
with the spinal core. For example, 98% of the oto-
lith samples examined by Radtke and Dean (1981)
were reportedly suitable for age and growth estima-
tion. Even though these preliminary findings were
Manuscript accepted October 1985.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
493
FISHERY BULLETIN: VOL. 84, NO. 3
encouraging, use of otoliths to resolve age and
growth discrepancies for Atlantic sailfish has not
been reported, and no conclusive evidence is avail-
able to validate the accuracy of age estimates for
this species using any method. We present an
analysis of dorsal spines and otoliths obtained from
one tag-recaptured Atlantic sailfish, where age was
very closely approximated from tagging records, to
help resolve the problems associated with ageing
this species.
METHODS
The Cooperative Gamefish Tagging Program of
the Southeast Fisheries Center Miami Laboratory
recovered a tag from a female Atlantic sailfish,
which had been recaptured on 14 January 1984, off
Boynton Beach, FL (Prince and Lee 1984). This fish
was originally tagged and released off the Florida
Keys (Islamorada) on 5 March 1973, at an estimated
weight of 18.2 kg (about 40 lb). When recaptured
it weighed 24.6 kg (54 lb) and had a lower jaw fork
length (LJFL) of 176.5 cm. The sailfish appeared
to have a healthy external appearance when caught
and body proportions and overall morphology were
within the normal range for a specimen of this size.
The entire fish was made available to us by J. T.
Reese Taxidermist, Inc. (Ft. Lauderdale, FL), and
both sagittae and the first six dorsal spines were
sampled for age determination.
Dorsal Spine Analysis
Dorsal spines were collected from the tagged
Atlantic sailfish following the procedures of Prince
and Lee (1982). Past efforts to age sailfish using dor-
sal spines have relied on spine number 4 as the
source of age and growth information (Jolley 1974,
1977; Hedgepeth and Jolley 1983). We collected the
first six anterior dorsal spines to insure that the
number assigned to each spine was accurate for
identification and analysis and to gain information
about possible differences between spines. The first
two anterior dorsal spines of sailfish are greatly
reduced in size compared with spines 3-6 and were
not used to estimate age. In addition, spines pos-
terior to spine number 6 have a smaller diameter
and were not used for age determination. This deci-
sion was based, in part, on a report by Robins4 and
Robins and de Sylva (1963) who believed that the
4Robins, C. R., Professor, Rosenstiel School of Marine and At-
mospheric Sciences, University of Miami, 4600 Rickenbacker
Causeway, Miami, FL 33149, pers. commun. 1982.
posterior dorsal spines of billfish do not grow
throughout their entire lifetime and recommended
that only anterior spines be used for age and growth
studies.
Dorsal spines 3-6 were cleansed of tissue, labeled
with a collection number, and preserved in isopropyl
alcohol (98%). The methods of sectioning dorsal
spines given by Hedgepeth and Jolley (1983) and
Prince et al. (1984) were used in this study. Dorsal
spine number 4 was sectioned by M. Y. Hedgepeth
at the laboratory of the Florida Department of
Natural Resources (FDNR), West Palm Beach, FL,
to ensure that processing of this spine was identical
with methods previously reported. We sectioned
spines 3, 5, and 6 using a Buehler ISOMET5 saw
and a 10.16 cm diameter diamond wafer blade. At
least 2 or 3 sections (0.44-0.46 mm thick) were taken
from each spine. Additional sections were taken
from spine number 4 after it had been processed by
FDNR personnel. All spine sections were placed into
labeled vials with isopropyl alcohol (98%) for storage
and extraction of oil. A single section was selected
and allowed to air dry before microscopic examina-
tion.
Dorsal spine sections were examined initially
using a compound stereoscope (6.0 x) with trans-
mitted light in order to assess that portion of the
section not affected by the vascularized core. Mea-
surements (in millimeters, mm) of the solid bone
area in the distal portion of the right lobe of each
section were taken along a straight-line counting
path from the focus to the outside margin of the
structure.
We assigned an age to each spine by counting only
concentric translucent bands that were continuous
around the circumference of the entire section. In
transmitted light, the zonations consisted of a dark
opaque zone followed by a light translucent zone.
D. W. Lee made three repeated counts of translu-
cent zones using a compound stereoscope at 12.0 to
25.0 x magnification.
Otolith Analysis
The general methods of Radtke and Dean (1981)
and Wilson and Dean (1983) were used to extract
and prepare the sagittae for examination by scan-
ning electron microscopy (SEM) and light micro-
scopy. The sagittae were removed from the tagged
Atlantic sailfish, cleaned with sodium hypochloride
solution, and rinsed in xylene and then 95% ethanol.
5Reference to trade names and products does not imply endorse-
ment by the National Marine Fisheries Service.
494
PRINCE ET AL.: LONGEVITY AND AGE OF ATLANTIC SAILFISH
The weight of one air-dried otolith was measured
to 0.001 mg (±5%) using a Perkin Elmer AD2Z
ultra-microbalance. The sagitta was attached to an
aluminum stub, coated with gold, and examined by
SEM at 15.0-1500 x to observe the surface mor-
phology. External ridges on the rostral lobe of
sailfish sagittae, first described by Radtke and Dean
(1981), was one of the features used in this study
for age estimation.
Following the methods of Haake et al. (1982) and
Wilson and Dean (1983), the other member of the
pair of sagittae was embedded in epoxy resin, and
a section was made in the transverse plane by polish-
ing both sides to 0.5 mm thickness with 600 grit
sandpaper and 0.3 ^m alumina polish. The internal
structure of the sectioned sagitta was examined with
an Olympus BH2 compound microscope at 4.0 to
1200 x to aid overall orientation and understanding
of the growth of the structure and to interpret the
external ridges used for age estimation.
imum longevity of this species by a considerable
margin. Although Jolley (1977) speculated that sail-
fish may live as long as 9 or 10 yr because the one
age 8 individual was not the largest specimen in his
sample, his estimated ages did not exceed 8 yr. In
addition, the maximum estimated age reported in
other recent studies was >7 yr (Radtke and Dean
1981; Hedgepeth and Jolley 1983). An Atlantic sail-
fish of estimated age 7 or 8 from the above sources
corresponds to an average size of about 25 kg (55
lb). Since our records indicate the age of the tag-
recaptured 24.6 kg (54 lb) sailfish was 13-15+ yr,
it appears that maximum longevity of Atlantic sail-
fish could be considerably older, perhaps over 20 yr,
because numerous specimens exceeding 45.5 kg (100
lb) have been caught during the last decade (Beards-
ley 1980). This reasoning assumes that sailfish have
indeterminate growth throughout their entire life-
time and that their size is proportional to age. It also
appears from tagging data that Atlantic sailfish may
RESULTS AND DISCUSSION
Our tagging records indicate that the tagged
Atlantic sailfish recaptured on 14 January 1984, was
at-large for 10 yr and 10 mo or 4,025 d. An experi-
enced charter boat captain estimated its size when
tagged to be 18.2 kg (40 lb). Bias in overestimating
the size of billfish during tagging has been a com-
mon problem since the inception of the Cooperative
Gamefish Tagging Program in 1954 (Prince 1984).
However, we feel that such an error would probably
not exceed ± 4.6 kg (10 lb) in a fish of this size, par-
ticularly when the experience of the captain making
the estimate is considered. The estimated age of a
sailfish of about 18.2 kg (40 lb) would be 2-4 yr based
on dorsal spine analysis (Jolley 1974, 1977; Hedge-
peth and Jolley 1983) and 3-5 yr based on otolith
analysis (Radtke and Dean 1981). Therefore, the ap-
proximate range in age of this sailfish based on tag-
ging information is 13-15+ yr. We feel these are
conservative figures based on the available informa-
tion and it is highly unlikely that this fish could be
younger than 13 yr.
Maximum longevity of Atlantic sailfish was first
inferred by de Sylva (1957) to be at least 3 or 4 yr
based on length-frequency analysis (Fig. 1). A modal
group beyond 4 yr was indicated in his analysis but
year class designation was not discussed. Since
1957, estimated longevity of Atlantic sailfish has
been revised upwards (Fig. 1) to ^7 yr. Our tagging
records indicate, however, that the oldest Atlantic
sailfish aged by dorsal spine analysis (Jolley 1977;
estimated age 8) probably underestimates the max-
14 r
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STUDIES
1 deSylva (1957)
2 Jolley (1974)
3 Jolley (1977)
4 Radtke ond Deon (1981)
5 Hedgepeth ond Jolley (1983)
6 Prince et al. (This paper)
13-15+
9-10
3-4
>7
957 974 1977 1981 1983 984
(1) (2) (3) (4) (5) (6)
YEAR (STUDY)
Figure 1.— Estimates of maximum longevity (yr) for Atlantic
sailfish from six different studies, 1957-84.
495
FISHERY BULLETIN: VOL. 84, NO. 3
grow very slowly after sexual maturity (sexual
maturity for female Atlantic sailfish reported at
13-18 kg, Jolley 1977). For example, tagging records
indicate that this fish, which was tagged at 18.2 kg,
gained only about 6.4 (14 lb) while being at-large
almost 1 1 yr. Our analysis of spines and otoliths sup-
port these findings.
Dorsal Spines
Examination of sections from dorsal spines 3-6
(Fig. 2) indicated that the vascularized core com-
prised an extensive area in all sections. The solid
bone area where zonations were not disrupted
varied in size and comprised 14, 19, 30, and 37%
of the right lobe of spine sections 3, 4, 5, and 6,
respectively (Table 1). The vascularized core severe-
ly restricted the zonation counts because increments
associated with early growth history were totally
disrupted and could not be enumerated. Counts of
zonations on the four spine sections ranged from 2
to 8 (Table 1). This suggests that spine number 4,
which had been used in past studies to assign ages,
may not necessarily be the best choice for ageing
sailfish, particularly for the larger, older specimens.
For example, spines 5 and 6 both had a higher per-
centage of solid bone, and counts of zonations in
these spines were proportionately higher than in
spines 3 and 4 (Fig. 2, Table 1). However, all spines
substantially underestimated the age of this sailfish,
where approximate age (13-15+ yr) was known
from tagging records. Hedgepeth6 reports that spine
number 4 would not have been included in the data
sets of previous published studies because of the ex-
tensive size of the vascularized core area. We con-
clude from these data that dorsal spine sections are
probably only useful for ageing sailfish from > 1 to
6Hedgepeth, M. Y., Fisheries Biologist, Florida Department of
Natural Resources, 727 Belvedere Rd., West Palm Beach, FL
33405, pers. commun. 1984.
Table 1 .—Mean count of zonations (3 repetitions) and percentage
solid bone in the distal portion of the right lobe of sections taken
from dorsal spines 3-6 of Atlantic sailfish (see text and Fig. 2).
Measurements and counts were taken along a straight line count-
ing path bisecting the spine laterally from the focus to the edge
of each section.
Dorsal
Mean
Solid
Solid bone
Total
spine
count
bone
measurement
measurement
number
(range)
(0/0)
(mm)
(mm)
3
2.0
14
1.89
13.52
4
3.7(3-4)
19
3.55
18.76
5
5.0
30
4.90
16.56
6
7.3(7-8)
37
6.08
16.39
5 yr. Although there may be some bias associated
with ageing these young sailfish because of the
vascularized core, this bias is probably minimal.
However, for sailfish older than estimated age 5 and
about >22.7 kg (50 lb), the bias substantially under-
estimates age and this bias increases with an in-
crease in size and age of the fish. In addition, spines
have not been shown to be useful in ageing sailfish
<l-yr-old (Jolley 1974, 1977).
Otoliths
Sagittae from the tagged Atlantic sailfish had ex-
ternal and internal morphologies that were charac-
teristic of sailfish reported by Radtke and Dean
(1981), as well as other istiophorids (Radtke et al.
1982; Wilson and Dean 1983; Radtke 1983). For ex-
ample, major features of these sagittae include a
rostrum and antirostrum separated by a deep sulcus
(Fig. 3). The external ventral and lateral surfaces
of the rostrum consist of a series of ridges that are
perpendicular to the axis of growth (Fig. 4). Radtke
and Dean (1981) suggested that the number of
rostral ridges can be used to estimate age of Atlan-
tic sailfish. To make an accurate count of external
ridges for age estimation, it is necessary to under-
stand the internal and external otolith growth pat-
tern so that the location and number of the first few
rostral ridges can be firmly established. These ini-
tial ridges are often covered by excess calcium car-
bonate (Wilson 1984), particularly in older speci-
mens, and are not always visible on the external
features of the lateral surface (Fig. 4).
The growth of the rostrum occurs in two direc-
tions (Figs. 3, 4). During early stages, incremental
growth of the rostral lobe occurs in the ventral direc-
tion out to a bend where growth shifts to a more
medioventral and then to a medial direction (Fig.
3). This same pattern of otolith growth has been
reported for blue marlin, Makaira nigricans, and
white marlin, Tetrapturus albidus (Wilson 1984).
However, it is difficult to illustrate a complex three-
dimensional otolith on a two-dimensional photo-
graph. Therefore, Figures 3 and 4 should be ex-
amined consecutively to obtain a proper orientation
of the structure.
Although rostal ridges on the external lateral sur-
face (Fig. 4) are not distinct because of the excess
calcium carbonate, after the change in the axis of
growth, the ridges on the ventral surface (ridges
3-10) can be counted easily (Fig. 4). Several lines of
evidence points towards the first two growth zones
occurring within the boundaries of the lateral sur-
face. For example, a distinct internal translucent
496
PRINCE ET AL.: LONGEVITY AND AGE OF ATLANTIC SAILFISH
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ANTIROSTRUM
FISHERY BULLETIN: VOL. 84, NO. 3
Figure 3.— Transverse section of the sagitta from
the tag-recaptured Atlantic sailfish at-large for 10
yr, 10 mo. Major features of the sagitta are labeled
and the approximate location and number of the
first 10 external ridges are shown on the rostrum.
Directional growth of the rostrum is indicated by
white letters and arrows.
ROSTRUM
LU
O
<
Li-
ar
CO
— i
<
CC
2
>
05 mm
LATERAL SURFACE
498
PRINCE ET AL.: LONGEVITY AND AGE OF ATLANTIC SAILFISH
' S **? ' urn
■T'^W
VENTRAL
SURFACE
10
9
8
^
f
4 -TT+-T-
• T^~>* LATERAL
Ik '*■''. X -SURFACE
5W >
t
FIRST 2 RIDGED
COVERED BY/
CaCOj^fvER-
BURDEN ^
/
CORE
NSID
Figure 4.— Lateral and ventral view of the sagitta rostrum from the tag- recaptured Atlantic sailfish showing the overall pattern of
otolith growth and the approximate location and number of the first 10 external ridges.
499
FISHERY BULLETIN: VOL. 84, NO. 3
zone exists between the boundary of many of the
external ridges shown in Figure 3. This zone extends
from the surface to deep within the internal struc-
ture of the rostrum (Fig. 3). The distinct change in
optical density of the first of these prominent zones
marks what we believe is the boundary between the
1st and 2d ridges and suggests that the first major
growth zone is located between the core and the
bend (Fig. 3). Further, using the SEM we counted
150-200 finely spaced increments between the core
and the first prominent translucent zone. This count
also supports our interpretation of the location of
the first annual zone if these increments are as-
sumed to form daily, the fish was born sometime
in late spring or early summer (as reported by
Beardsley et al. 1975), and the annual zonations are
being formed in the winter. Jolley (1977) reported
that annual zones in Atlantic sailfish spines tend to
be formed in late fall or winter and he also spec-
ulated that sailfish may form the first annuli on
spines prior to a full year's growth. The location of
the second translucent zone, based on similar evi-
dence, appears to be at the beginning of the bend
(Fig. 3). The width of the first two major growth
zones (^0.5 mm) are considerably larger than the
zones beyond the end. Wide spacing of year marks
during early growth have been observed in many
fishes when growth rates are most rapid (Dean et
al. 1983). Therefore, these data support our conten-
tion that at least two ridges should be accounted for
as occurring within the boundaries of the lateral
surface.
Rostral ridges 3 through 10 were easily distin-
guished and counted on the sagitta's ventral surface
within the same plane of focus (Fig. 5, bottom).
After the 10th ridge, however, the rostrum changes
direction slightly (Fig. 3), and it was necessary to
refocus to observe ridges 11 through 13 (Fig. 5, top).
We feel that potential sources of error in our counts
of rostral ridges would have most likely occurred
at the beginning and end of the counting path. In
addition, we feel that if errors were made at these
locations, they would have increased the count.
Therefore, otolith age of the tagged Atlantic sailfish
was estimated to be 13 yr. However, it should be
recognized that potential errors in this estimate
could have resulted if one or two ridges were un-
accounted for on the lateral surface or on the tip
of the rostrum on the ventral surface. Otolith age
under these circumstances should be presented con-
servatively as ranging from 13 to 15+ yr.
The weight of one sagitta from the tagged Atlan-
tic sailfish (7.84 mg) was extremely heavy for an
istiophorid of comparable size. For example, it was
1.24 mg heavier than the sagitta from a 29.6 kg (65
lb) sailfish caught in 1985 off Miami and was 1.18
mg heavier than the largest sagitta from Pacific blue
marlin reported by Radtke (1983). In addition, the
tagged sailfish sagitta was in the upper range in
weight (0.51-8.16 mg) of more than 500 blue and
white marlin sagittae examined by Wilson (1984).
Since the relationship between the size of otoliths
and the age of fishes has been shown to be positive-
ly correlated for some teleosts (Somerton 1985), we
feel that the relatively large size of this sagitta pro-
vides additional indirect evidence that this structure
could be from a very old sailfish.
CONCLUSIONS
Our tagging records indicate that estimates of
maximum longevity for Atlantic sailfish should be
revised upwards to at least 13-15+ yr, and that
sailfish of this age can grow at a very slow rate
(about 0.59 kg/yr during its time at large). Dorsal
spines do not appear to be an accurate source of age
and growth information for older, larger sailfish (>5
yr, ^22.7 kg or 50 lb), while sagittae do provide more
accurate estimates of age for these older age groups.
Since current stock assessments of Atlantic sailfish
(Conser 1984) rely exclusively on dorsal spine ageing
data as input, these assessments offer little insight
into the more mature segments of the population.
If skeletal structures from the larger, older fish are
systematically rejected for ageing analyses, an
underestimate of age and longevity and an
overestimate of growth rate can occur (Nammack
et al. 1985). Therefore, future assessments should
be revised using otolith ageing methods to clarify
that portion of the age structure that can not be
reliably appraised using dorsal spines.
ACKNOWLEDGMENTS
We thank J. T. Reese Taxidermist, Inc., Ron Har-
rison (angler), and Captain Bud Carr for providing
us with biological samples and other information
from the tagged Atlantic sailfish. Personnel from
the Florida Department of Natural Resources in
West Palm Beach, FL, sectioned and analyzed dor-
sal spine number 4. Dana Dunkleberger (University
of South Carolina) assisted in preparing scanning
electron micrographs.
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Beardsley, G. L.
1980. Size and possible origin of sailfish, Istiophonts
500
PRINCE ET AL.: LONGEVITY AND AGE OF ATLANTIC SAILFISH
Figure 5.— Scanning electron micrograph of
the ventral view of the sagitta rostrum from
the tag-recaptured Atlantic sailfish. A count of
external ridges 3-10 (bottom) and 10-13 (top)
were used to assign a numeric otolith age of 13
yr. Bar on bottom = 1.0 mm, bar on top = 0.1
mm.
501
FISHERY BULLETIN: VOL. 84, NO. 3
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shop on age determination of oceanic pelagic fishes: tunas,
billfishes and sharks, p. 151-156. U.S. Dep. Commer.,
NOAA Tech. Rep. NMFS-8.
502
AGE DEPENDENT FECUNDITY, NUMBER OF SPAWNINGS PER YEAR,
SEX RATIO, AND MATURATION STAGES IN
NORTHERN ANCHOVY, ENGRAULIS MORDAX
Richard H. Parrish,1 Donna L. Mallicoate,1 and
Richard A. Klingbeil2
ABSTRACT
Maturity stage data from fishery sampling programs and ovarian histological data from research cruises
were used to develop a method for determining the age-specific number of spawnings per year and annual
fecundity of the central stock of northern anchovy, Engraulis mordax.
The sex ratio was found to be size and age dependent in both the fishery and trawl surveys with
females increasingly dominant in the larger and older size and age classes. The overall sex ratio in trawl
surveys was nearly 1:1; the fishery data favored females 1.48:1. The magnitude and duration of maturity
stages were size and age dependent with peak spawning occurring earlier in the season in younger fish.
Maturity stages and histological classes with hydrated eggs showed essentially the same diurnal pattern
for nightly spawning activity indicating that the presence of hydrated eggs could be used as an index
of daily spawning. The daily spawning incidence and total annual fecundity were found to be heavily
age dependent. Females in their first spawning season had an average of 5.3 spawnings, while those
in their fourth had an average of 23.5 spawnings. When combined with the higher batch fecundity of
larger fish this results in 4 + year-old females producing nearly 5 times as many eggs per unit of weight
as 1-year-olds. When the age-specific fecundity and sex ratio in the fishery are combined it is apparent
that the catch of a ton of 4 + year-old northern anchovy reduces the reproductive potential of the stock
7.3 times as much as the catch of a ton of 1-year-olds.
It was concluded that age-specific fecundity in multiple spawning fishes is of greater significance
for management than previously thought. It is also significant that much of the observed variance in
stock-recruitment relationships for multiple-spawning fishes may be due to the fact that spawning biomass
is a poor index of the egg production and reproductive potential of the stock.
Age-specific variation in life history rates is a major
factor in population and management models of ex-
ploited fishes, and variation in reproductive effort
is of great significance in such models. Size and age-
specific batch fecundity estimates have been avail-
able for many species for decades, and for species
which spawn only once per spawning season these
are readily incorporated into models. However it has
been impossible to determine the age-specific repro-
ductive effort of species which spawn many times
during a spawning season because there has been
no way to determine the number of spawnings per
year.
Recent research on the histology of the ovaries
of northern anchovy, Engraulis mordax, and an-
choveta, Engraulis ringens, suggest that they
spawn approximately once a week during peak
spawning months (Hunter and Goldberg 1980;
'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, 245 W. Broadway
Street, Long Beach, CA 90802.
Hunter and Macewicz 1980; Alheit et al. 1983; Alheit
et al. 1984). Hunter and Leong (1981), in their study
of the spawning energetics of the northern anchovy,
found that northern anchovy spawn about 20 times
per year. Hunter and Leong (1981) and Alheit et al.
(1983) suggested that annual fecundity per unit of
parental biomass may be highly variable and depen-
dent upon the nutritional state and size structure
of the stock.
Potentially the recently developed histological
techniques could be utilized to determine age-specific
annual fecundity; however, this would be very ex-
pensive as it would require a very large data set
which would necessarily be stratified by age and
time of year. The objectives of this report are 1) to
demonstrate a method for combining the high
resolution reproductive information from the
histology of the ovaries with inexpensive, lower
resolution reproductive information derived from
resource surveys and fishery sampling programs to
determine the age-specific reproductive potential of
a multiple spawning species, and 2) to evaluate the
gross anatomical maturity stages which have been
Manuscript accepted January 1986.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
503
FISHERY BULLETIN: VOL. 84, NO. 3
utilized in field sampling programs for northern an-
chovy and to use the historical data from these pro-
grams in conjunction with ovarian histological data
to describe age-dependent annual fecundity in the
central stock of northern anchovy.
DATA SOURCES
There are three major sources of biological data
for adult northern anchovy in California: samples
taken from the commercial fishery (Collins and
Spratt 1969), samples taken from midwater trawl
hauls carried out by the Sea Survey Program (Mais
1974), and samples taken primarily by midwater
trawl during egg production cruises (Picquelle and
Hewitt 1983). The first two sources are the result
of long-term research and monitoring programs
carried out by the California Department of Fish and
Game, and the third is the result of research cruises
carried out by the National Marine Fisheries Ser-
vice. The fishery data used in this analysis consist
of biological information for 60,661 northern an-
chovy sampled from the San Pedro purse seine fleet
during the period of 1966-80 and 4,904 northern an-
chovy sampled from the Monterey fleet during
1966-78. All northern anchovy in the fishery samples
were aged and nearly all were assigned maturity
stages. We used a geographically restricted subset
of the 1966-83 sea survey data (lat. 29.5°-34.5°N;
54,457 northern anchovy). Maturity stages were not
recorded for males in the sea survey data and age
determinations were made on only a portion (19,031)
of the fish sampled. In both data sets age determina-
tions were made from otoliths with methods
described by Collins and Spratt (1969). The third
source of data, provided to us by B. Macewicz3, con-
sists of histological information for the gonads of
8,672 females sampled during the months of
February to April from 1977 to 1984. Age deter-
minations were not made and maturity stages were
not taken on these fish.
The gross anatomical maturity stage description
used for northern anchovy is a slightly modified
version of the system developed by Bowers and
Holliday (1961) for herring. The system has seven
maturity stages which are primarily based on the
portion of the body cavity occupied by the gonads
and, in the later stages, by the appearance of trans-
lucent eggs or milt (Table 1). Herring are consider-
ably larger than anchovy, and they are generally not
3B. Macewicz, Southwest Fisheries Center La Jolla Laboratory,
National Marine Fisheries Service, NOAA, 8604 La Jolla Shores
Drive, La Jolla, CA 92038, pers. commun. August 1984.
considered to be multiple spawners; therefore, there
are some difficulties in applying the maturity stages
to anchovy. The most obvious problem is that a con-
siderable proportion of the anchovy sampled had
gonads so small that sex determinations were not
made as they would have required magnification.
There was also a small proportion of fish in which
physical deterioration made sex determination im-
possible. The California anchovy fishery is primar-
ily for reduction to fish meal, and the quality of the
fish was occasionally very poor when the fish were
sampled. Another major difficulty is that it is not
possible to distinguish between anchovy gonads that
are resting (i.e., stage 2) between multiple spawn-
ings in the same season and those resting between
spawning seasons. A comparable problem exists
with spent fish (stage 7).
Table 1 .—The international (Hjort) scale of maturity stages of the
gonad. From Bowers and Holliday (1961).
Stage 1 : Virgin individuals: very small sexual organs close under
vertebral column; ovaries wine-colored, torpedo-shaped,
about 2-3 cm long and 2-3 cm thick, eggs invisible to
naked eye; testes whitish or greyish-brown, knife-
shaped, 2-3 cm long and 2-3 cm broad.
Stage 2: Maturing virgins or recovering spents: ovaries some-
what longer than half the length of ventral cavity, about
1 cm diameter, eggs small but visible to naked eye; milt
whitish, somewhat bloodshot, of same size as ovaries,
but still thin and knife-shaped.
Stage 3: Sexual organs more swollen, occupying about half of
ventral cavity.
Stage 4: Ovaries and testes occupying almost two thirds of ven-
tral cavity; eggs not transparent, milt whitish, swollen.
Stage 5: Sexual organs filling ventral cavity; ovaries with some
large transparent eggs; milt white, not yet running.
Stage 6: Roe and milt running (spawning).
Stage 7: Spents: ovaries slack with residual eggs; testes baggy,
bloodshot.
SEX RATIO
Description of the sex ratio in northern anchovy
was confounded by the presence of fish for which
the sex could not be determined. The relationship
between size and the percentage of these unsexed
fish is similar for both the commercial purse seine
and midwater trawl data. In both data sets, a large
percentage of the fish smaller than 100 mm stand-
ard length (SL) are of unknown sex, about 10% of
the 101-110 mm fish are of unknown sex, and only
a small percentage of the fish larger than 110 mm
are of unknown sex (Table 2). The percentages of
fish with unknown sex at sizes larger than 110 mm
in the purse seine data are somewhat higher than
those in the midwater trawl data. This is probably
due to the occasional occurrences of fish in which
504
PARRISH ET AL.: AGE DEPENDENT FECUNDITY IN NORTHERN ANCHOVY
the condition was too poor to allow sex identifica-
tion. The relationship between age and the percent-
age of unsexed fish is similar to that described for
size (Table 2). It should be noted that both data sets
are biased towards larger and older fish. The age
composition of anchovy in the midwater trawl data
is biased because of the fact that otoliths were often
not taken when trawl hauls were dominated by
young-of-the-year fish (Parrish et al. 1985). The
purse seine data contain a much smaller percentage
of small or young fish than the midwater trawl data.
This is primarily caused by the fact that a 5-in (about
108 mm SL) minimum size limit was in effect for
most of the 1966-80 period.
To evaluate the seasonal cycle of the occurrence
of northern anchovy for which the sex could not be
identified, the monthly percentages of females,
males, and anchovy with unknown sex were deter-
mined by age group for the San Pedro fishery (Fig.
1). In all age groups the minimum percentages of
fish which could not be sexed occurred from about
January to May in association with the spawning
season. Higher percentages occurred both before
and after the spawning season, particularly in the
first potential spawning season. This implies that
a significant percentage of anchovy mature, or at
least partially mature, and then reabsorb their
gonadal tissue to the point that their gonads are so
small that they cannot be sexed without magnifica-
tion. It also implies that a bias due to the unsexed
fish exists. This bias is at a minimum from January
to May and it primarily affects the analyses of fish
in their first potential spawning season.
Klingbeil (1978) found the female:male ratios of
northern anchovy sampled in the Sea Survey Pro-
gram and in the commercial fishery to be 1.03:1 and
1.60:1 respectively. The additional years of infor-
mation from these two sources, in our data sets, pro-
Table 2.— Proportion of northern anchovies with unknown sex and sex ratio by size (A) and
by age (B).
San Pedro anchovy fishery
Sea survey (lat 29.5°-34.5°N)
Length
Unknown
Females
Mean
Unknown
Females
Mean
(mm)
sex
male
SL
Number
sex
male
SL
Number
61- 70
1.000
A
1
0.996
0.00
273
71- 80
0.676
0.71
—
37
0.941
0.94
—
597
81- 90
0.437
0.67
—
252
0.810
0.78
—
1,396
91-100
0.283
0.77
—
2,261
0.500
0.84
—
2,208
101-110
0.114
1.06
—
8,684
0.100
0.82
—
2,882
111-120
0.057
1.30
—
17,186
0.016
0.78
—
4,141
121-130
0.029
1.53
—
19,396
0.007
1.07
—
4,016
131-140
0.014
2.10
—
10,010
0.003
1.43
—
2,439
141-150
0.007
2.90
—
2,354
0.003
2.56
—
772
151-160
0.009
4.43
—
438
0.005
3.09
—
185
161 +
0.024
7.20
—
42
0.000
9.67
—
32
Total
0.057
1.48
—
60,661
B
Annual
0.187
1.02
—
19,031
Age
0
0.202
0.83
104.2
1,862
0.779
0.81
88.7
3,616
1
0.090
1.15
112.8
16,167
0.122
0.88
107.2
4,812
2
0.046
1.49
121.1
20,885
0.022
0.86
119.4
4,733
3
0.036
1.76
126.3
14,174
0.010
1.15
126.4
3,543
4 +
0.022
2.01
134.0
7,573
0.003
1.66
135.0
2,327
Total
0.057
1.48
121.2
60,661
0.187
1.02
113.7
19,031
Age
0
1
February-April
0
2,271
0.093
0.95
106.5
4,646
0.153
0.79
101.0
2
0.027
1.33
116.2
4,279
0.004
0.78
117.3
2,035
3
0.018
1.45
123.3
3,410
0.002
1.04
125.3
1,928
4 +
0.014
1.69
134.4
3,620
0.001
1.55
134.6
1,382
Total
0.041
1.30
119.0
15,955
0.048
0.96
117.6
7,616
Age
August-December
0
0.259
0.77
104.2
1,204
0.831
0.78
88.6
3,216
1
0.083
1.19
117.6
6,411
0.104
0.97
112.2
2,198
2
0.060
1.59
123.1
12,082
0.035
0.91
120.5
2,311
3
0.051
1.92
127.7
7,648
0.021
1.28
128.1
1,255
4 +
0.039
2.33
132.9
2,532
0.007
1.57
135.4
560
Total
0.069
1.58
123.2
29,877
0.316
1.02
109.7
9,540
505
FISHERY BULLETIN: VOL. 84, NO. 3
40
O30
20
10-
- 1 1 1 f 1 1 1 1 1 1 r
JUL RUG SEP OCT NOV DEC JAN FEB MflR RPR HAY JUN
MONTH
Figure 1.— The monthly percentages of northern anchovies with
unknown sex, by age group, in samples from the San Pedro fishery.
duced essentially no change in the sex ratio in the
sea survey data (1.02:1). However, there was a
reduction in the proportion of females in the fishery
data (1.48:1) which was associated with a reduction
in the average age of anchovy in the catch after 1977
(Mais 1981). Sunada and Silva (1980) also found a
female:male sex ratio greater than unity in the
northern Baja California purse seine fishery, 2.15:1
in 1976 and 1.44:1 in 1977. Alheit et al. (1984)
reported a sex ratio of 1.30:1 in purse seine caught
Peruvian anchoveta sampled during their spawning
season. Klingbeil (1978) and Alheit et al. (1984)
reported that during the spawning season there
were unexpectedly large numbers of samples in
which sex ratios were heavily dominated by either
males or females. Alheit et al. (1984) suggested that
"hydrated females segregate, either by depth or
area, from the 'normal' school, taking a high per-
centage of males with them forming 'spawning
schools' dominated by males."
Analysis of the sex ratio by size and age groups
shows that there are increasingly larger proportions
of females in the larger and older groups (Table 2).
This trend is evident in both the fishery and sea
survey data. In the fishery data there are more
males than females identified in the fish smaller than
100 mm SL and in age group 0. The proportion of
females increases until there are more than twice
as many females as males among fish larger than
130 mm and in age group 4 + . There is a similar
trend in the sea survey data; however, females do
not outnumber males until the fish are larger than
120 mm and 3 yr of age. The sex ratio in age group
4+ is 1.66:1. The apparent dominance of females
in the larger size classes may be partially caused by
sex related differences in growth rates; however,
their dominance in the older age classes of both the
purse seine and midwater trawl samples cannot be
explained by differences in growth. We grouped our
data sets into the spawning months (February- April)
and nonspawning months (August-December) in
order to evaluate features which might be caused
by behavioral differences that may occur during the
spawning season. This analysis shows that the over-
all sex ratio in northern anchovy taken by midwater
trawl is close to 1:1 in both nonspawning and spawn-
ing seasons (Table 2B). It also shows that the sex
ratios in younger fish are dominated by males and
those in older fish are dominated by females. The
overall sex ratio in northern anchovy sampled in the
purse seine fishery is heavily dominated by females;
however, the sex ratio is higher in the nonspawn-
ing season (1.58:1) than in the spawning season
(1.30:1). The crossover from male to female domi-
nance of the sex ratio occurs between age group 2
and 3 in the sea survey data and at age 1 in the
fishery data.
MATURITY STAGES IN
NORTHERN ANCHOVY
Seasonal Variation in Maturity Stages
To determine which of the various data sets avail-
able for northern anchovy were best suited for
evaluating maturity stages in the central stock, we
examined the seasonality of three grouped matur-
ity stages of four data subsets. The grouped stages
included immature or resting females (stages 1 and
2); females just beginning to mature (stage 3); and
the highly mature, spawning, and spent females
(stages 4-7). The data consisted of two sets of
samples from the commercial fishery (Monterey and
San Pedro) and the sea survey samples from south-
ern California (lat. 32.5°-34.5°N) and northern Baja
California (29.5°-32.5°N).
The seasonal patterns of the grouped maturity
stages of females sampled in the San Pedro fishery
(Fig. 2A), the sea survey in southern California (Fig.
2B), and the sea survey in northern Baja California
(Fig. 2C) are quite similar. The pattern in the Mon-
terey fishery differs from that in the other data sets
in that spawning is at the highest levels in April and
September (Fig. 2D). It cannot presently be deter-
mined if there are one or two peaks of spawning in
506
PARRISH ET AL.: AGE DEPENDENT FECUNDITY IN NORTHERN ANCHOVY
90
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Figure 2.— The monthly percentages of grouped maturity stages for female northern anchovies sampled in A, San Pedro fishery; B,
Sea survey (lat. 32.5°-34.5°N); C, Sea survey (29.5°-32.5°N); D, Monterey fishery.
the Monterey area due to the lack of data from May
to July. Because of the different seasonal pattern
of the grouped maturity stages in the Monterey
fishery data and because there is more than one
stock in this region (Vrooman et al. 1981), it was
decided to exclude this area from further analysis.
The analyses that follow are based on the combined
San Pedro fishery and southern California-northern
Baja California sea survey data sets (52,352 females
of which 41,930 were aged).
To obtain a first approximation of the magnitude
and duration of maturity stages in the central stock
of northern anchovy, the monthly percentages of
fish with each maturity stage were calculated for
females and for males. The seasonal patterns were
found to be essentially the same for males and
females; however, the males tended to have some-
what larger percentages of fish in the higher matur-
ity stages. Our presentation is limited to informa-
tion on females.
507
FISHERY BULLETIN: VOL. 84, NO. 3
The proportion of females classified as stage 1,
virgin individuals, is at a minimum during the
spawning season, comprising <10% of the females
sampled during February, March, and April. How-
ever, during the summer more than half of the
females were classified as stage 1 (Fig. 3A). Stage
2 females, maturing virgins and recovering spents,
are at a minimum in August (when most females are
classified as stage 1). From September until January
between 40 and 60% of the females are classified
as stage 2. During the spawning season, and just
after, the percentage of stage 2 females dropped
between 30 and 40%. The August to September
decline in the percentage of stage 1 females is
primarily caused by the sharp increase in the pro-
portion of stage 2 females. Thus, the combined per-
centage of stages 1 and 2 females is probably a
reasonable inverse indicator of the seasonality of
spawning. However, during the spawning season an
unknown proportion of those classified as stages 1
and 2 are females that have recently spawned and
are between multiple spawnings.
Stage 3 females (ovary enlarged, occupying about
half of the length of the ventral cavity) have a con-
siderably different pattern. There is a gradual in-
crease from about 5% in August to about 30% in
January. This percentage is maintained until April,
i.e., through the spawning season; it then drops to
about 5% in June. The monthly percentages of the
higher maturity stages (4,5, and 6) clearly delineate
the spawning season as primarily a January-May
event (Fig. 3B). The relatively constant low level of
stage 7 females is unexpected as the maximum pro-
portion of spent fish would be expected to occur just
after the peak of spawning.
Maturity Stage Relationships
with Size and Age
To examine potential relationships between the
size and age of northern anchovy and the duration
and magnitude of maturity stages we calculated the
monthly percentages of grouped maturity stages for
four size classes (81-100, 101-120, 121-140, and
141-160 mm SL) and four age groups (1, 2, 3, and
4 + ). Age group 1 includes fish prior to and after
their first potential spawning season (i.e., young-of-
the-year fish in July through the following June).
Age group 4 + includes fish in their fourth and sub-
sequent spawning seasons. The grouped maturity
stages (1, 2, 3, and 4-7) are the same as those pre-
sented earlier.
Size has a large effect on both the duration and
magnitude of maturity stages in northern anchovy.
With the exception of those sampled from February
to April nearly all of the 81-100 mm SL females were
classified as immature or resting (Fig. 4A). In addi-
tion, the majority of this size anchovy have gonads
too small to determine their sex without magnifica-
tion (Table 2). As the size class increases the per-
centage of stages 1 and 2 decreases; this occurs in
all months; however, the minimum percentage of
90-
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JUL AUG SEP OCT NOV DEC JAN FEB MAR APR MAY JUN
MONTH
Figure 3.— The monthly percentages of individual maturity stages for female northern anchovies. A. Stages 1-3. B. Stages 4-7.
508
PARRISH ET AL.: AGE DEPENDENT FECUNDITY IN NORTHERN ANCHOVY
90
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MONTH
Figure 4.— The monthly percentages of grouped maturity stages
for female northern anchovies, by size group. A. Stages 1 + 2 B.
Stage 3. C. Stages 4-7.
stages 1 + 2 occurs in February to April. The per-
centage of females just beginning to mature (i.e.,
stage 3) has an abrupt peak in February-March in
the smallest size class (Fig. 4B). This peak becomes
increasingly spread out in the larger size classes.
The higher maturity stages (4-7) are most abundant
from February to April in all size classes (Fig. 4C).
The larger size classes have much larger percent-
ages of females in the higher maturity stages than
the smaller size classes, and there is a minor peak
in the percentage of the higher maturity stages dur-
ing the fall in the two largest size classes. Analysis
of the data by age group showed, as would be ex-
pected, that increased age has essentially the same
effect as increased size on the magnitude and dura-
tion of maturation stages.
SPAWNING INCIDENCE AND
FECUNDITY
Studies by Hunter and Goldberg (1980) in Califor-
nia and Alheit et al. (1983) in Peru examined post-
ovulatory follicles to determine the spawning
frequency of female anchovies (i.e., the time inter-
val between spawnings). A second method would be
to determine the percentage of females with
509
FISHERY BULLETIN: VOL. 84, NO. 3
hydrated eggs. Hunter and Macewicz (1980) showed
that northern anchovy begin hydrating eggs at about
0600 in the morning and by sunset about 14% of the
females have hydrated eggs. They felt that the best
indicator of the time of spawning was the occurrence
of both hydrated eggs and new postovulatory
follicles. This occurred in a low percentage of their
samples indicating that spawning was completed
rapidly; the time of maximum spawning occurred
between 2100 and 0200 with a peak between 2200
and 2300. Hunter and Macewicz (1980) divided the
nightly pattern of spawning in anchovy into three
periods: "early spawning period (1800 to 2100 hours),
some spawning occurs but the ovaries of most
reproductively active females are in the hydrated
stage; maximum spawning (2100-0200 hours), most
females spawn (females with hydrated eggs decline
to 0 and females with new postovulatory follicles
reach the maximum number for the night); and post-
spawning (0200-0600 hours), little or no spawning
occurs and females destined to spawn the next night
begin hydration." A considerable amount of new
histological data is now available as a result of a
series of egg production biomass surveys for north-
ern anchovy. B. Macewicz (fn. 3) has analyzed the
histology of the ovaries of 8,672 anchovy sampled
in these surveys, and our analysis of this new infor-
mation verifies the temporal patterns which Hunter
and Macewicz (1980) described from a much smaller
sample (Fig. 5).
Comparison of Maturity Stages and
Histology Classes
The histological data show that during the early
evening the percentage of females with hydrated
eggs could be an indicator of the percentage of
females spawning per day (i.a, the spawning in-
cidence). To use the extensive maturity stage data
available for northern anchovy it is necessary to
determine the relationships between the histology
of the gonads and the maturity stages used in the
California Department of Fish and Game's sampling
programs. To date histological and field maturity
stage data have not been taken on the same individ-
uals; therefore, analysis is limited to comparisons of
the two data sets. In the following comparisons the
sea survey and histology data sets were limited to
samples taken during the period 1977-84 and dur-
ing the principal spawning season (i.a, February-
April). Since nearly all of the trawls were taken at
night, the data were limited to those taken from 1800
to 0500 h. The midwater trawl hauls were normally
15 min in duration, and about 30% of the fish in the
JO
en
o
in
si
is
10-
5-
UJ
d
20
15-
£ 10-
5 -
HYDRATED
EGGS (H)
t r
DAY 0
P0STGVULAT0RY
FOLLICLES (POF)
I I -1 '
1800 2000 2200 2400 200 400
TIME OF NIGHT
Figure 5— The percentages of female northern anchovies with
ovaries in three histological classes, by time of night.
histological data set and 30% in the maturity stage
data sets were taken in the same trawl hauls during
cooperative cruises.
The histological data are divided into six classes
(B. Macewicz fn. 3):
1. Ovaries with hydrated eggs and no day-0 post-
ovulatory follicles.
2. Ovaries with hydrated eggs and day-0 postovul-
atory follicles.
3. Ovaries with day-0 postovulatory follicles and no
hydrated eggs.
4. Ovaries with day-1 postovulatory follicles.
5. Mature ovaries with no hydrated eggs, no day-0
nor day-1 postovulatory follicles.
6. Immature ovaries, few or no yolked oocytes, no
atresia present in the ovary other than late-stage
corpora atretica.
Northern anchovy, spawning on the night they were
sampled (day 0), include the first three classes; those
that spawned on the night before they were sampled
(day 1) are class four.
A comparison of the percentages of hydrated
females in the sea survey data (i.e, stages 5 + 6) with
that in the histological data (i.e, classes 1 + 2) shows
that they have essentially the same pattern from the
onset of spawning in the early evening until spawn-
510
PARRISH ET AL.: AGE DEPENDENT FECUNDITY IN NORTHERN ANCHOVY
ing is completed in the early morning (Fig. 6). This
implies that in the early evening maturity stages 5
+ 6 can be used to estimate the spawning incidence;
however, within a few hours after sunset the per-
centage of females with hydrated eggs (i.e., stages
5 + 6) rapidly becomes an underestimate of the in-
cidence of spawning due to the completion of spawn-
ing. If only the females (n = 2,161) sampled between
the hours of 1800 and 2000 are considered, then the
percentage in maturity stages 5 + 6 (15.3%) is quite
close to the percentage of day-0 females calculated
for the total histology data set (15.9%).
The variation throughout the night of the percent-
ages of the other maturity stages is also of interest
as it offers some insight into the meaning of maturity
stages in anchovy. Hunter and Macewicz (1980)
showed that spawning primarily occurs between the
hours of 1800 and 0200. In the sea survey data the
percentage of stages 5 + 6 falls from 15.3 to 1.6%
over this time period (Fig. 7). The expected matur-
ity stage that should increase over this time period
is stage 7 (i.e., spents: ovaries slack with residual
eggs). This, however, is not the case The percentage
of stage-7 females has very little variation over the
1900-0200 period; going from 2% at 1900 to 3.6%
at 0200. This suggests that residual eggs occur in
only a small percentage of anchovy and that stage
7 cannot be used to determine if an anchovy has
spawned within 24 h. This is consistent with Stauf-
fer and Picquelle's (1980) observation that field-
spawned northern anchovy were found to release
nearly 100% of their hydrated eggs. The percentages
of the other maturity stages show considerable varia-
tion from 1900 to 0200 h. Stages in which the ovary
is small (i.e., 1 + 2) occur in about 37% of the females
in the early evening. This increases rapidly after
2300 and by 0200 these stages comprise about 46%
of the females. Stages 3 + 4, in which the ovaries
occupy from one half to two thirds of the ventral
cavity, occur in about 46% of females in the early
evening. This rises to a peak of about 54% at 2300-
2400 and then declines to about 49% at 0200.
Our interpretation of the patterns exhibited by the
sea survey data is that the percentage of females at
stages 5 + 6 in the early evening (i.e., 15.3%) is a
valid estimate of the percentage of sampled females
with hydrated eggs. However, as the night progresses
the percentage of stages 5 + 6 declines. At the peak
of spawning, just before midnight, many females ap-
pear to be misidentified as stages 3 + 4. This could
occur if they had spawned part of their eggs before
they were captured and if the person making the
maturity stage determinations used the size of the
ovary, rather than the presence of hydrated eggs, to
determine the maturity stage After midnight an
increasing percentage of spawning females have
CO
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s
10-
5-
20-
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F 15
en
£ 10
HYDRATED EGGS
STAGES 5+6
1 I 1 1 1 1 1 1 — T
1800 2000 2200 2400 200
TIME OF NIGHT
400
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■*• 20-
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cs
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i i i i i i i i i i i
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20-
STAGES 5+6
10-
•v.
STAGE 7 \ ^
i ■ i i i i-i ■ ■ ■ •
1800 2000 2200 2400 200
TIME OF NIGHT
400
Figure 6.— The percentages of female northern anchovies with
hydrated eggs and with maturity stages 5 + 6, by time of night.
Figure 7.— The percentages of grouped maturity stages for female
northern anchovies by time of night. (Two hour moving average.)
511
FISHERY BULLETIN: VOL. 84, NO. 3
apparently spawned all of their hydrated eggs and
they are then classified as stage 1 or 2. The mean-
ing of stage 7 in female anchovy remains a mystery.
The seasonal and diurnal patterns described above
indicate that, with the exception of stages defined
by the presence of hydrated eggs, gross anatomical
maturity stages have little utility other than describ-
ing the seasonality of spawning. However, field iden-
tifications of the presence of hydrated eggs, if they
are calibrated with histological data and if the diur-
nal pattern of hydration is known, can potentially
be used to determine spawning incidence.
Several authors have pointed out that females with
hydrated eggs and actively spawning females were
more numerous than females with day-1 postovula-
tory follicles, and have suggested that hydrated and
actively spawning females may be more susceptible
to capture due to behavioral or physiological factors
(Hunter and Goldberg 1980; Stauffer and Picquelle
1980; Alheit et al. 1984). Previous workers have
therefore used the percentage of day-1 females as
the index of the daily spawning incidence The over-
all percentages of day-0 and day-1 females in the
histology data set (8,672 females) used in our
analyses are 15.9 and 11.5%. Alheit et al. (1983)
found the overall percentages of day-1 and day-2
Peruvian anchoveta females to be 17.26 and 14.81%.
Hunter and Goldberg (1980), and subsequent
workers on the northern anchovy, took their samples
at night whereas Alheit et al. (1983) took their Peru-
vian anchoveta samples primarily during the day.
Therefore the definition of day-1 is somewhat dif-
ferent in studies of the two species. In our analysis
both day-0 and day-1 females appear to be more
susceptible to capture by midwater trawl in the early
evening than later at night. The percentages of both
decline as the night progresses; however, the decline
is more extreme in the day-0 females (Fig. 8).
The use of maturity stages 5 + 6 could result in
several sources of bias that would tend to produce
overestimates of the spawning incidence of northern
anchovy. If females with hydrated eggs are more
susceptible to capture, there will be a tendency to
produce biased estimates. However, this bias would
not be expected to be size or age dependent, nor
would it be expected to vary during the spawning
season. The same bias would be expected to occur
in 1- and 4-yr-old hydrated females and the same bias
would be expected in February and April. Therefore
the use of the percentages of hydrated females or
maturity stages 5 + 6 females may result in over-
estimates of the total spawning incidence or annual
fecundity, but the relative spawning incidence or
relative annual fecundity of the different age groups
would not be biased. A second source of bias is that
an unknown number of females have ovaries so small
that visual determination of sex is impossible with-
out magnification. Therefore, the incidence of spawn-
ing is overestimated because it is calculated by
dividing the number of stages 5 + 6 females by less
than the total number of females. This bias is size
and age dependent, being much more common in
smaller and younger anchovy, but not month depen-
dent. Note that the various studies of the spawning
incidence in northern anchovy and Peruvian an-
choveta have defined the spawning incidence to be
the number of females spawning per day divided by
the number of mature females, i.e., these studies ex-
clude immature females, which are primarily the
smaller and younger fish, from the calculation.
There are also several sources of bias that would
tend to produce underestimates of the spawning in-
cidence The anchovy fishery in southern California
primarily occurs at night during the fall months and
during the daylight hours in the spring. A period of
low availability to the commercial fishery is asso-
ciated with the spawning season. Mais (1974) asso-
ciated this phenomenon with variation in schooling
behavior and showed that acoustic surveys detect
relatively few "commercial-sized" anchovy schools
during the spawning season. If low availability to the
commercial fishery is associated with spawning ac-
t 1 — i 1 1 1 1 1 1 1 r
1800 2000 2200 2400 200 400
TIME OF NIGHT
Figure 8.— The percentages of day-0 and day-1 female northern
anchovies by time of night.
512
PARRISH ET AL.: AGE DEPENDENT FECUNDITY IN NORTHERN ANCHOVY
tivity, it is probable that the fishery undersamples
the active spawners. In addition, a proportion of the
commercial catches occur during the time of day
when the females do not have hydrated eggs. The
fishery data will therefore tend to underestimate the
spawning incidenca The total sea survey data will
also produce an underestimate as it includes samples
taken throughout the night.
The combined fishery-sea survey data used in our
analyses will therefore provide only an index of the
daily spawning incidenca To evaluate the potential
net bias of this index we calculated the percentage
of females with maturity stages 5 + 6, in the com-
bined fishery-sea survey data, and the percentage
of females with day-1 postovulatory follicles, in the
histological data. To make the data comparable we
used the period 1977-84 and the months February-
April. The percentage of females with maturity
stages 5 + 6 and the percentage of females with
day-1 postovulatory follicles was 10.9 and 11.5%. Use
of the maturity stage data will therefore slightly
underestimate the daily spawning incidence (i.a,
10.9/11.5 = 0.948).
Size Dependent Batch Fecundity
Annual fecundity in the northern anchovy is
dependent upon the batch fecundity and the number
of spawnings per year. Batch fecundity is size depen-
dent and the best average estimate over six seasons
(Hunter et al. 1985) is given below. Note that Hunter
et al. found significant variation (ANOVA) among
years.
batch fecundity = -1,104 + 614 (WT)
where WT = female wet weight, minus ovaries, in
grams. During the spawning season ovary free
weight of northern anchovy is equal to 95% of the
total wet weight (Hunter and Leong 1981). Batch
fecundity, with the above relationships, for a typical
1-yr-old (12 g) and a typical 4-yr-old (24 g) are 5,896
eggs and 12,895 eggs. On a per unit weight basis
the 24 g fish would produce only 9.4% more eggs
than the 12 g fish. Age-dependent variations in
batch fecundity are therefore of only minor signifi-
cance in the relationship between spawning biomass
and annual fecundity. There is the possibility that
batch fecundity could vary over the spawning
season, and since we have shown an age-dependent
seasonality in the spawning incidence of northern
anchovy, this could potentially contribute to age-
dependent differences in annual fecundity. Hunter
and Leong (1981), however, found average batch
fecundity to be essentially the same in samples taken
in January-February and in March- April.
Size-Dependent Histology
Classes
Hunter and Macewicz (1980) found no relationship
between size and the percentage of mature female
northern anchovy with day-1 postovulatory follicles.
Later work by Picquelle and Hewitt (1984) showed
that weight and spawning incidence were highly cor-
related in the northern portion of the central stocks
range. They stated that this implied that the larger
females spawned more frequently or that the
smaller females had a much shorter spawning
season. We analyzed the larger histology data set
now available and found that the percentages of
females with hydrated oocytes or with day-1 post-
ovulatory follicles, as well as the percentage of
females with maturity stages 5 + 6, were depen-
dent upon the size of the females (Fig. 9).
CO
E 40-
u.
o
tn 20-
HISTOfJGY
MATURITY
— -^— /STAGES
ca
*\
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HYDRATE)
1
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PERCENTflGE
ca en
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STAGES 5+6
5 -
. r ,
1 i
80
81-
100
101-
120
121-
140
141-
160
LENGTH SLCMN;
Figure 9.— The percentages of female northern anchovies with
hydrated eggs, with maturity stages 5 + 6, and day-1 histological
classes by size group.
Age-Dependent Spawning Incidence
and Annual Fecundity
To assess age-dependent, annual fecundity in the
central stock of northern anchovy we calculated the
513
FISHERY BULLETIN: VOL. 84, NO. 3
number of spawnings and the fecundity on a
monthly basis for age groups 1, 2, 3, and 4 + .
Average monthly wet weight by age was taken from
Mallicoate and Parrish (1981). The number of
spawnings per month was calculated from the num-
ber of days per month and the index of daily spawn-
ing (i.e., the proportion of stages 5 + 6). Note that
the bias due to the unknown sex problem discussed
earlier would tend to cause an overestimation of the
daily spawning incidence: particularly in females in
their first spawning season. Also note that the in-
dex of daily spawning underestimates the spawn-
ing incidence by about 5%.
Our analysis shows that there are large, age-
dependent variations in the proportions of female
northern anchovy spawning as the spawning season
progresses (Fig. 10). From July until January all age
groups have a very low daily spawning index. Inten-
sive spawning commences in February and all age
groups have roughly the same spawning index
(9-12%). In March the spawning index of age group
1 declines to about 2%; it increases slightly in April
and declines to about 1% in May. In age group 2 the
spawning index increases to 13% in March and then
declines to about 2% by May. Age groups 3 and 4 +
have peak spawning indices in March (25 and 27%),
considerable spawning in April (10 and 17%) and
lesser amounts in May (3 and 6%) and June (3 and
6%).
Older females have a much larger number of
spawnings per spawning season than younger
~i 1 1 1 r
JUL RUG SEP OCT NOV DEC JflN FEB MflR RPR MAY JUN
MONTH
Figure 10.— The monthly percentages of female northern
anchovies with maturity stages 5 + 6, by age group.
females (Table 3). In their first spawning season
females have an average of 5.3 spawnings. In their
second spawning season this rises to 11.9 and in
their third and fourth plus seasons the number of
spawnings rises to 19.2 and 23.5. The increase in
the number of spawnings associated with increas-
ing age appears to be primarily due to the increase
in the length of the spawning season that occurs in
older fish. The average number of spawnings per
season for all females sampled was 15.1. This is less
than the estimate that Hunter and Leong (1981)
developed from the energetics of female northern
anchovy (i.e., 20 spawnings per year). Their calcula-
tions indicated that mature female northern anchovy
spawned on the average 15 times between February
and September; their calculation of the number of
spawnings from October to January (5) was esti-
mated indirectly from the relative monthly larval
abundance in 1953-60. Our estimate of the number
of spawnings from February to September (14.3) is
very close to the Hunter and Leong (1981) estimate
which was based on a smaller histology data set.
However, our estimate of the number of spawnings
from October to January is only 0.8 and is much less
than their indirect estimate based on the relative
seasonal larval abundance for the 1953-60 period.
The central stock of northern anchovy was at a much
smaller population size in 1953-60 than it was in
1966-84 (MacCall 1980) and northern fish, with a
seasonal spawning pattern similar to that occurring
in the Monterey data, may have comprised a larger
proportion of the anchovy population off California
during the 1953-60 period than at present thus in-
flating Hunter and Leong' s estimate for the
October-January period.
Our analysis indicates that annual fecundity in the
central stock of northern anchovy is heavily age
dependent; the average 4 + yr-old female produces
nearly 10 times as many eggs as a 1-yr-old female
(Table 3). Our calculations show that central stock,
female anchovy produce 2,803, 6,550, 11,434, and
13,861 eggs/g of body weight per spawning season
in their 1st, 2d, 3d, and 4th plus spawning seasons.
Females 4 yr of age and older produce nearly 5 times
as many eggs per unit of weight as 1-yr-olds.
DISCUSSION
Over the last decade it has become apparent that
recruitment failure is the major threat to many of
the world's largest fisheries. In addition, variation
in recruitment is a significant causal factor in the
interyear variation of the annual catches of many
fisheries. Stocks of small pelagic fishes appear to
514
PARRISH ET AL.: AGE DEPENDENT FECUNDITY IN NORTHERN ANCHOVY
Table 3.— Proportion of maturity stages 5 + 6, number of spawnings and fecundity of female northern anchovies sampled in the Sea
Survey Program (lat. 29.5°-34.5°N) and San Pedro fishery.
July1 Aug.1 Sept. Oct. Nov. Dec.
Jan.
Feb.
Mar.
Apr. May June Total2 Eggs/g3
Prop. 5 + 6
Spawnings
Wt. (g)
No. eggs
Prop 5 + 6
Spawnings
Wt. (g)
No. eggs
Prop. 5 + 6
Spawnings
Wt. (g)
No. eggs
Prop. 5 + 6
Spawnings
Wt. (g)
No. eggs
Prop. 5 + 6
Spawnings
0.000
0.000
0.000
0.000
0.002 0.000
0.062 0.000
15.5 15.5
492 0
0.022 0.024
0.682 0.744
18.3 18.3
6,527 7,120
0.021 0.016
0.651 0.496
20.1 20.1
6,914 5,268
0.017
0.527
0.021
0.651
0.000
0.000
11.2
0
0.005
0.150
17.4
1,357
0.005
0.150
19.1
1,506
0.004
0.120
20.9
1,330
0.008
0.240
0.005
0.155
11.1
832
0.007
0.217
16.8
1,887
0.010
0.310
19.3
3,148
0.013
0.403
21.8
4,680
First spawning season
0.000 0.000 0.005 0.087 0.023
0.000 0.000 0.155 2.436 0.713
12.0 11.0 11.4 11.6 12.8
0 0 860 13,793 4,536
Second spawning season
0.001 0.001 0.015 0.110 0.132
0.030 0.031 0.465 3.080 4.092
17.2 16.3 16.2 15.6 16.5
268 261 8,881 24,626 34,866
Third spawning season
0.002 0.002 0.008 0.124 0.251
0.060 0.062 0.248 3.472 7.781
19.2 19.3 19.1 18.0 20.7
606 630 2,489 33,836 85,360
Fourth-plus spawning seasons
0.003 0.003 0.008 0.115 0.271
0.090 0.093 0.248 3.220 8.401
22.3 22.2 23.6 23.3 26.6
1,071 1,102 2,952 37,390 110,293
All spawning seasons combined
0.011 0.002 0.002 0.010 0.107 0.151
0.341 0.060 0.062 0.310 2.996 4.681
0.036 0.011
1 .080 0.341
13.7 15.4
7,438 2,687
0.065 0.021
1.950 0.651
17.7 18.3
17,980 6,230
0.101 0.031
3.030 0.961
22.2 20.9
35,891 10,655
0.166 0.065
4.980 2.015
26.5 25.7
67,123 26,454
0.004
0.120
13.6
819
0.020
0.600
17.5
5,462
0.026
0.780
22.7
9,467
0.056
1.680
25.7
18,136
0.094 0.044 0.012
2.820 1.364 0.360
5.3
32,514 2,803
11.9
102,174 6,550
19.2
205,819 11,434
23.5
322,957 13,861
15.1
'Missing data estimated from adjacent months,
includes 5% correction for spawning incidence bias.
3Total eggs/February weight.
be particularly susceptible to collapse; however, per-
turbations of recruitment is a potential threat to any
fishery in which one or two year classes comprise
the bulk of the landings. The stock-recruitment ap-
proach to understanding or predicting recruitment
has fallen into disfavor, at least in the small pelagic
fishes, because stock size has not proven to be a good
predictor of recruitment. In its pure form (Bever-
ton and Holt 1957; Cushing 1971; Ricker 1975) the
stock-recruitment concept is based on two factors:
1) Parent stock size is a measure of the reproduc-
tive potential of the stock, and 2) there are compen-
satory mechanisms which reduce the number of
recruits per spawner as the size of the parent stock
increases. This compensation occurs through some
mix of reduced fecundity of the parent stock,
reduced growth of the recruiting cohort and in-
creased mortality of the recruiting cohort. Recruit-
ment variations are usually attributed to changes
in environmental conditions, usually unknown, and
the causal mechanisms, also usually unknown, are
thought to occur during the early life history stages.
The present emphasis of recruitment research is on
the growth and mortality of the early life history
stages. Potential variations of stock fecundity as a
factor in recruitment variations has largely been
ignored.
There are now 6 years of egg production estimates
available for the central stock of northern anchovy
(Bindman 1985). The mean spawning incidence for
these years is 0.124 and the spawning incidence
varied from 0.094 in the El Nino year of 1983 to
0.160 in 1984. This implies that the central stock
produced 70% more eggs, per unit of spawning
biomass, in 1984 than in 1983. Santander (1980)
showed that the Peruvian anchoveta had both re-
duced spawning and an alteration of the seasonal-
ity of spawning during the 1972 El Nino. The results
presented here, which show that fecundity is strong-
ly age dependent, suggest that the reduction in age
composition caused by heavy exploitation will great-
ly reduce the average fecundity per unit of biomass
and also result in a reduction in the length of the
spawning season. It appears that interyear varia-
tions in the age composition of a stock or in en-
vironmental factors associated with energy reserves
or egg production are likely to alter greatly a stock's
reproductive potential. If this is the case in other
species which have multiple spawning, much of the
variance in the stock-recruitment relationships of
these fishes may be due to the fact that spawning
biomass is a poor index of the reproductive poten-
tial of the stock.
To date information concerning age-specific
reproductive potential has not been available for
multiple spawning fishes because of the difficulty
515
FISHERY BULLETIN: VOL. 84, NO. 3
of determining the number of spawnings per year.
The pioneering work by Hunter and Goldberg (1980)
and later studies based on this work clearly demon-
strate that, at least for many clupeids, the spawn-
ing incidence or spawning frequency can be deter-
mined with properly designed histological studies.
Unfortunately a research program designed to
determine age-specific reproductive potential would
be very expensive as it would require a field sam-
pling progam extending over the whole spawning
season, in many cases the entire year; and it would
require histological analysis and aging of a large
number of females, both quite labor intensive.
It appears that the only way it may be possible
to determine age-specific reproductive potential for
many fishes is to use the approach developed here
which combines two methodologies: histological
assessment of ovaries because it unambiguously and
accurately measure spawning rate and a traditional
fishery sampling program which utilizes an inexpen-
sive rapid index of reproductive condition, such as
the maturity stage system or a gonado-somatic
index, in which thousands of specimens can be
processed. Whichever anatomical grading system is
used, its principal purpose would be to determine
the percentage of hydrated females. Most of the
maturity stages (i.e., 1-4, 7) in the system used for
northern anchovy are only of value in describing the
seasonality of spawning. The only stages (i.e., 5 and
6) which can be used to determine the number of
spawnings are those in which the eggs are hydrated,
and they can be directly used as an index in north-
ern anchovy because it is known that the duration
of hydrated eggs in the ovary is <24 h. The tradi-
tional fishery sampling program may, as in the case
for northern anchovy, already be available. If this
is the case the principal work will be to calibrate
properly the maturity stage or gonado-somatic in-
dex with the histological analysis. For this approach
to work the fishery must, of course, take hydrated
females.
CONCLUSIONS
It is important for those managing fisheries which
are susceptible to recruitment overfishing to realize
that the alteration in the age structure of a stock
that occurs under heavy exploitation may have
greater effects on the total fecundity and seasonality
of spawning than previously recognized. Manage-
ment strategies which decrease the exploitation of
older, more fecund females could increase yields and
also provide increased protection against recruit-
ment overfishing. In northern anchovy there is the
additional factor that the sex ratio in the fishery is
age dependent (i.e., the female:male ratio for 1-yr-
old anchovy in the San Pedro fishery is 0.83:1,
whereas that for 4+ yr-olds is 2.01:1). When this
factor is multiplied by the difference in the fecun-
dity of the two age groups, it is apparent that the
catch of a ton of 4 + yr-old northern anchovy reduces
the reproductive potential of the stock 7.3 times as
much as the catch of a ton of 1 -yr-old fish.
ACKNOWLEDGMENTS
We gratefully acknowledge John Hunter and
Beverly Macewicz for allowing us to use their exten-
sive data on the histology of the ovaries of northern
anchovy and Carol Kimbrell for providing us with
the computer files. John Hunter also provided con-
siderable input to the development of the work and
edited the manuscript. We would also like to thank
Eric Knaggs, Eugene Fleming, and John Sunada for
providing us with the anchovy fishery data and Ken-
neth Mais for providing the sea survey anchovy data.
LITERATURE CITED
Alheit, J., B. Alegre, V. H. Alarcon, and B. J. Macewicz.
1983. Batch fecundity and spawning frequency of various an-
chovy (Genus: Engraulis) populations from upwelling areas
and their use for spawning biomass estimates. FAO Fish.
Rep. 291, 3:977-985.
Alheit, J., V. H. Alarcon, and B. J. Macewicz.
1984. Spawning frequency and sex ratio in the Peruvian an-
chovy, Engraulis ringens. CalCOFI Rep. 25:43-52.
Beverton, R. J. H., and S. J. Holt.
1957. On the dynamics of exploited fish populations. Fish.
Invest. Lond. Ser. 2, 19:1-533.
Bindman, A. G.
1985. The 1985 spawning biomass of the northern anchovy.
U.S. Dep. Commer., NOAA, NMFS, SWFC, Admin. Rep.
LJ-85-21, 21 p.
Bowers, A. B., and F. G. T. Holliday.
1961. Histological changes in the gonad associated with the
reproductive cycle of the herring (Clupea harengus L.).
Mar. Res. Scot. 5, 16 p.
Collins, R. A., and J. D. Spratt.
1969. Age determination of northern anchovies, Engraulis
mordax, from otoliths. Calif. Dep. Fish Game, Fish Bull.
147, p. 39-55.
Cushing, D. H.
1971. The dependence of recruitment on parent stock in dif-
ferent groups of fishes. J. Cons. Perm. Int. Explor. Mer
33:340-362.
Hunter, J. R., and S. R. Goldberg.
1979. 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., N. C. H. Lo, and R. J. H. Leong.
1985. Batch fecundity in multiple spawning fishes. In R.
516
PARRISH ET AL.: AGE DEPENDENT FECUNDITY IN NORTHERN ANCHOVY
Lasker (editor), An egg production method for estimating
spawning biomass of pelagic fish: application to the northern
anchovy, Engraulis mordax, p. 67-77. U.S. Dep. Commer.,
NOAA Tech. Rep. NMFS 36.
Hunter, J. R., and B. J. Macewicz.
1980. Sexual maturity, batch fecundity, spawning frequency,
and temporal pattern of spawning for the northern anchovy,
Engraulis mordax, during the 1979 spawning season.
CalCOFI Rep. 21:139-149.
Klingbeil, R. A.
1978. Sex ratios of the northern anchovy, Engraulis mordax,
off southern California. Calif. Fish Game 64:200-209.
MacCall, A. D.
1980. Population models for the northern anchovy (Engraulis
mordax). Rapp. P. -v. Reun. Cons. Perm. int. Explor. Mer
177:292-306.
Mais, K. F.
1974. Pelagic fish surveys in the California Current. Calif.
Dep. Fish Game, Fish Bull. 162. 79 p.
1981. Age-composition changes in the anchovy, Engraulis
mordax, central population. CalCOFI 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 symmetricus.
CalCOFI Rep. 22:69-81.
Parrish, R. H., D. L. Mallicoate, and K. F. Mais.
1985. Regional variations in the growth and age composition
of northern anchovy, Engraulis mordax. Fish. Bull., U.S.
83:483-496.
Picquelle, S. J., and R. P. Hewitt.
1983. The northern anchovy spawning biomass for the
1982-83 California fishing season. CalCOFI Rep. 24:16-28.
1984. The 1983 spawning biomass of the northern anchovy.
CalCOFI Rep. 25:16-27.
Ricker, W. E.
1975. Computation and interpretation of biological statistics
offish populations. Fish. Res. Board Can. Bull. 191, 382 p.
Santander, H.
1980. Fluctuaciones del desove de anchoveta y algunos fac-
tores relacionados. In IOC Workshop Rep. 28, UNESCO,
Paris, p. 255-274. [Workshop on the effects of environmen-
tal variation on the survival of larval pelagic fishes, Lima,
Peru. 20 April-5 May 1980.]
Stauffer, G. D., and S. J. Picquelle.
1980. Estimates of the 1980 spawning biomass of the cen-
tral subpopulation of northern anchovy. U.S. Dep. Com-
mer., NOAA, NMFS, SWFC, Admin. Rep. LJ-80-09, 24 p.
SUNADA, J. S., AND S. SlLVA.
1980. The fishery for northern anchovy, Engraulis mordax,
off California and Baja California in 1976 and 1977.
CalCOFI 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. Dep. Fish Game 67:39-51.
517
SOME STATISTICAL TECHNIQUES FOR ESTIMATING ABUNDANCE
INDICES FROM TRAWL SURVEYS
Michael Pennington1
ABSTRACT
Methods are presented for estimating an index of relative abundance from trawl survey catch per tow
data. The estimated variance of the index takes into account the within survey variability in catch and
possible yearly changes in catchability. Applying the techniques to a series of surveys for yellowtail
flounder, Limanda ferruginea, off the northeast coast of the United States yields an abundance index
with a variance which is 40% lower than the variance of the original survey index for the current value
and 57% lower for values not near the ends of the survey series.
The average number of fish caught per tow during
a trawl survey is often used as an index of a species's
relative abundance (Grosslein 1969; Clark 1979).
Catch per tow data are usually quite variable
because of the heterogeneous distribution of many
fish stocks (Byrne et al. 1981). A further source of
variability for survey indices of abundance is that
the catchability of a particular species with respect
to the survey trawl may change from year to year
(Byrne et al. 1981; Collie and Sissenwine 1983). As
a result, the observed time series of abundance in-
dices reflects changes in the population, within
survey sampling variability, and varying catchabil-
ity over time.
This paper uses various statistical methods to con-
struct from the catch per tow data an index of abun-
dance which more closely tracks the population than
does the original (average catch per tow) series.
Specifically, since the distribution of catch per tow
data is often highly skewed and contains a propor-
tion of zeros, estimates of the mean catch per tow
for each survey are made based on the A-distribution
(Aitchison and Brown 1957). Next, time series tech-
niques are used to estimate the component of the
series generated by the actual changes in the
population.
The methods are applied to data for yellowtail
flounder, Limanda ferruginea, from a series of
groundfish trawl surveys conducted off the north-
east coast of the United States as part of the
National Marine Fisheries Service's MARMAP pro-
gram. The resulting index of abundance is substan-
tially more precise than the original index.
Northeast Fisheries Center Woods Hole Laboratory, National
Marine Fisheries Service, NOAA, Woods Hole, MA 02543.
STATISTICAL METHODS
Sources of Variability
Let yt denote the observed average catch per tow
for the survey conducted in year t and z\ = E[yt],
the expected value of yt. Since a species catchabil-
ity may change from year to year with respect to
the survey trawl, let z = E[z'\p] denote the expected
value of z given a population level p. Then
y, = zt + et.
The error term, et, can be expressed as
et = (Vt ~ z't) + (z't ~ Zt),
where the first error component is due to the within
survey variability and the second is due to changes
in catchability.
In order to construct an index of abundance, it is
necessary to assume a functional relationship be-
tween zt and pt. A reasonable assumption made in
practice (and in this paper) is that
zt = apt.
If the relationship is not linear, then the unadjusted
catch per tow index will be a biased measure of
relative abundance.
Estimating the Mean Catch per Tow
The distribution of marine survey data often can
be described by what is called a A-distribution (Ait-
chison and Brown 1957). That is, the data contain
Manuscript accepted October 1985.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
519
FISHERY BULLETIN: VOL. 84, NO. 3
a proportion of zeros and the nonzero values are
distributed lognormally. The minimum variance un-
biased estimates of the mean, c, and its variance,
var(c), for the A-distribution are given by (Penning-
ton 1983),
c =
and
var(c) =
ra
n
n'
0,
exp(^) Gm(s2/2), ra > 1,
ra = 1,
ra = 0,
(1)
f ™ exp(2^)
= <*<**> •■feff
x Gr
Im - 2
m - 1
, m > 1,
ra = 1,
(2)
EFFICIENCY OF x
Figure 1.— The efficiency of x and s2 (the sample mean and
variance, respectively) for the A-distribution with 50% zeros.
o,
ra = 0,
where n is the number of tows, m is the number of
nonzero values, y and s2 are the sample mean and
variance respectively of the nonzero logf values, x1
is the single (untransformed) nonzero value when
ra = 1, and
GJx) = 1 +
+ I
ra
1
ra
x
(m - l)2-?-1 x>
j=2 jyO (ra + 1) (ra + 3). . .(ra + 2j> - 3) j\ '
The series defining Gm{x) is a function of x [e.g., #
= s2/2 in Equation (1)] and ra which is easily
evaluated for particular values of x and ra using a
computer.
Figure 1, which is an extension of a graph in Ait-
chison and Brown (1957, p. 98), shows the large sam-
ple efficiency of the ordinary sample statistics as
compared with their most efficient estimates for the
A-distribution with 50% zeros. Estimates of a2, the
variance of the nonzero loge values, are often be-
tween 1 and 2 for trawl surveys. Thus (Fig. 1) the
sample mean is a fairly efficient estimator of the
mean for trawl surveys, but the sample variance is
highly inefficient. Though for larger values of o2,
which, for example, are common for egg surveys
(Pennington and Berrien 1984), the sample mean is
also very inefficient. It does not follow that the
variance of c is necessarily small, but it is smaller,
and as o2 increases, much smaller than the variance
of the sample mean. However, it should be noted
that if the sample variance is used to estimate the
variance of the sample mean for moderate sample
sizes because of the inefficiency of the sample
variance, the estimated variance of c will often be
greater than the estimated variance of the sample
mean.
Estimating the Index of Abundance
As an index of abundance, the series of yearly
catch per tow estimates, yh (based, e.g., on the A-
distribution theory if appropriate) has two draw-
backs. First, its estimated variance when derived
from the within survey variance can be an under-
estimate since catchability may vary from year to
year. The second and more serious deficiency is that
the index for a particular year is based only on that
year's survey which disregards relevant information
contained in the surveys for other years.
520
PENNINGTON: TECHNIQUES FOR ESTIMATING ABUNDANCE
One method to construct an abundance index
based on the entire survey series is briefly as follows
(more details can be found in Pennington (1985)).
Suppose the population (or zt) can be represented
by the autoregressive integrated moving average
process (Box and Jenkins 1976, Chap. 4)
0(5) zt = 0(5) at.
where the at's are independently identically distrib-
uted {iid) and normally distributed (N) with mean
zero and variance o2 [iid N(0, o2)]. If yt = zt + et,
and the et's are assumed iid N(0, o2), then yt will
follow the model
0(5) yt = r,(B) ct,
(3)
Suppose the factors causing the change in popula-
tion from year t - 1 to year t (such as recruitment,
fishing mortality, natural mortality, and migrations)
produce at's which are approximately iid N{0, o2).
If the measurement errors are multiplicative, then
In yt = In zt + et.
(8)
Assuming the e/s are iid N(0, o2) and independent
of the a/s, then it follows as above that yt can be
represented by the model
(1 - 5) In yt = (1 - 05) ct.
(9)
where the ct's are iid N(0, of)
For model (9) [generated by Equations (7) and (8)]
where the ct's are iid N(0, o2). Now if model (3)
and the ratio of/of are known, then the maximum and
likelihood estimate of zt is given by
0 = o*M
2/„2
(10)
(1 - 0)2 = olio
&t = Vt ~ -z(Ct - nj ct+1
- TIo C
2 W + 2 ~ ) • • • »
nT_t cT), (4)
where T denotes the last year of the series, the ct's
are the estimated residuals generated by model (3),
and the n values are calculated using the identity
0(5) = (1 - nxB - n252 - . . .) r]{B). (5)
The variance of zt is given approximately by
varfo) = o
^ „2
1 - (n§ + 4
2 \ °e:
(6)
where rc0 = 1.
The model for yt [Equation (3)] is usually ob-
tained in practice by fitting a model to the observed
series using procedures described in Box and
Jenkins (1976). If catchability is constant over time,
the within survey sampling variance provides an
estimate of oez. But if catchability varies, another
approach is necessary.
Toward this end, consider the expression
"t-i
or
(1 - 5) In zt = at.
(7)
Therefore, assuming the above approximations to
the population dynamics, fitting model (9) to the
observed survey series provides an estimate, 0, of
o^lol and an estimate of o2. The it-weights for the
model are from Equation (5) given by
= (1 - 0) 0<
i > 1.
(11)
It may be noted that if model (9) is valid and catch-
ability is constant over time then the estimate of o2
given by 0 d2 [from Equation (10)] would approx-
imately equal the estimate of o2 based on the within
survey sampling variance.
AN APPLICATION
The Northeast Fisheries Center conducts an
extensive groundfish trawl survey as part of its
MARMAP program two times a year: in the fall
since 1963 and in the spring since 1968 (Grosslein
1969). The survey region is divided into sampling
strata based on geographic boundaries and depth
contours (Fig. 2). For each survey, trawl stations
are chosen randomly within each stratum. One of
the objectives of the surveys is to provide indices
of abundance for the many species of commercial
value in the region.
Yellowtail flounder is an important New England
fishery resource whose population has fluctuated
considerably over the survey period (Clark et al.
1984). Commercial catch statistics exist for yellow-
tail flounder, but age data suitable for a VPA (Vir-
tual Population Analysis) are unavailable. Major
521
FISHERY BULLETIN: VOL. 84, NO. 3
CD
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3
PL,
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OS
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CD
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o
522
PENNINGTON: TECHNIQUES FOR ESTIMATING ABUNDANCE
yellowtail flounder fisheries are off southern New
England (strata 5, 6, 8, 9) and on Georges Bank
(strata 13-21). The two stocks are fairly distinct but
with some intermixing (Clark et al. 1984).
The nonzero catch per tow survey data for yellow-
tail flounder are approximately lognormally distrib-
uted within a stratum. Therefore, the estimators
based on the A-distribution [Equations (1) and (2)]
were used to estimate the mean catch per tow and
its variance in each stratum. The regional estimates
for southern New England and Georges Bank were
then calculated in the usual manner for each survey
(see, e.g., Pennington and Brown 1981).
Model (9) was fit to each series (spring 1968-84
and fall 1963-84 in both regions) and the model's
adequacy checked (Box and Jenkins 1976, Chap. 8).
Table 1 contains summary statistics and parameter
Table 1.— Summary statistics and parameter estimates for the
yellowtail flounder survey series. The first three sample autocorre-
lations (rv r2, and r3) are for the first differenced logged series.
No. of
Survey years
'1
r2
r3
0
SE(fl)
oi
Southern New En
gland
Spring 17
-0.23
0.12
-0.18
0.21
0.28
0.57
Fall 22
-0.26
0.07
-0.31
0.40
0.22
0.71
Georges Bank
Spring 17
-0.32
0.00
-0.09
0.61
0.23
0.36
Fall 22
-0.30
-0.06
0.18
0.36
0.23
0.33
Average
-0.28
0.03
-0.10
0.40
^.12
0.50
'Assuming the estimates of 8 are independent.
estimates for the four series. Since the series are
relatively short, the averages of the areal and
seasonal estimates are used as the final estimates
of 0 and o2c (last line in Table 1).
Abundance indices for the two regions and
seasons were calculated by applying to each series
Equation (4) with 6 = 0.4, the rc-weights given by
Equation (11), and the ct's (for each series) gener-
ated by model (9). An estimate of 6] equal to 0.20
and of o\ equal to 0.18 were obtained from Equa-
tion (10). The estimated variance of the index equals,
from Equation (6), 0.12 for the current value and
declines to 0.09 for values not near the series' end
points. This compares with a variance of 0.20 ( =
of) for the original index. Figures 3 (log scale) and
4 (linear scale) show plots of the estimated index and
the observed catch per tow series for the fall sur-
veys off southern New England.
DISCUSSION
The major advantage of estimating an index of
abundance from the entire survey series is that it
can produce an index with a variance considerably
smaller than the variance of the observed series. But
the application also demonstrates that estimates of
the accuracy of an index based only on the within
survey sampling variance can be misleading. For ex-
ample, the 1972 survey value for yellowtail flounder
off southern New England is considered an anom-
o 1 — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i
1963 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84
YEAR
Figure 3.— Logged average catch per tow and the estimated index of abundance for southern New England
yellowtail flounder.
523
FISHERY BULLETIN: VOL. 84, NO. 3
5
o
80-1
70
60-
o 50
a.
.e
o
T3 40
0)
ro 30
>
<
20
10
Survey catch perjow _
Survey index o( abundance
N /
"1963 64 6 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84
YEAR
Figure 4.— Average catch per tow and the estimated index of abundance for southern New England
yellowtail flounder.
aly (Collie and Sissenwine 1983). It does appear
anomalous if comparisons are made using 0.11, the
estimated variance based on the within survey
variance, but not if the estimate of 0.20 (= of) is
considered (Fig. 3).
Assessing the accuracy of an index of abundance
for marine stocks is difficult since the true levels
are never known with certainty. But they can be
compared with other indicators of abundance. The
methods were applied to the haddock stock on
Georges Bank (Pennington 1985) for which a VPA
exists. It was found that model (7) adequately
describes the dynamics of the VPA series, and the
survey series follows model (9). The resulting index
of abundance is quite similar to the VPA estimates.
Collie and Sissenwine (1983) give a method for
estimating the relative abundance of a fish stock
using survey data and commercial catch statistics.
They observe that their method produces estimates
which compare favorably with VPA estimates.
Figure 5 shows plots of Collie and Sissenwine's
estimate of the relative abundance of southern New
England yellowtail flounder and the index based
only on the survey data.
Finally, it should be noted that the purpose of the
modeling stage in the estimation procedure is not
necessarily to develop a realistic model for the
population, but to describe the important stochastic
properties of the series. As the observed series
becomes longer, more precise estimates can be
made. For shorter series, given the large variabil-
ity inherent in marine trawl surveys, a preliminary
estimate of between 0.3 and 0.4 for the smoothing
parameter 6 appears to be an appropriate initial
value to use for estimating an abundance index un-
til more information becomes available.
LITERATURE CITED
AlTCHISON, J., AND J. A. C. BROWN.
1957. The lognormal distribution. Cambridge Univ. Press,
Lond., 176 p.
Box, G. E. P., and G. M. Jenkins.
1976. Time series analysis: forecasting and control. Rev. ed.
Holden-Day, San Franc, 575 p.
Byrne, C. J., T. R. Azarovitz, and M. P. Sissenwine.
1981 . Factors affecting variability of research trawl surveys.
Can. Spec. Publ. Aquat. Sci. 58:238-273.
Clark, S. H.
1979. Application of bottom trawl survey data to fish stock
assessment. Fisheries 4:9-15.
Clark, S. H., M. M. McBride, and B. Wells.
1984. Yellowtail flounder assessment update. U.S. Dep.
Commer., NOAA, Natl. Mar. Fish. Serv., Woods Hole Lab.
Ref. Doc. No. 84-39, 29 p.
Collie, J. S., and M. P. Sissenwine.
1983. Estimating population size from relative abundance
data measured with error. Can. J. Fish. Aquat. Sci. 40:
1871-1879.
Grosslein, M. D.
1969. Groundfish survey program of BCF Woods Hole.
Comm. Fish. Rev. 31(8-9):22-30.
Pennington, M.
1983. Efficient estimators of abundance, for fish and plank-
ton surveys. Biometrics 39:281-286.
1985. Estimating the relative abundance of fish from a series
524
PENNINGTON: TECHNIQUES FOR ESTIMATING ABUNDANCE
80-1
YEAR
Figure 5.— Survey index of abundance (solid line) and Collie and Sissenwine's index (broken line) for
southern New England yellowtail flounder.
of trawl surveys. Biometrics 41:197-202.
Pennington, M., and P. Berrien.
1984. Measuring the precision of estimates of total egg pro-
duction based on plankton surveys. J. Plankton. Res. 6:
869-879.
Pennington, M., and B. E. Brown.
1981 . Abundance estimators based on statified random trawl
surveys. Can. Spec. Publ. Aquat. Sci. 58:149-153.
525
RATES OF INCREASE IN DOLPHIN POPULATION SIZE
Stephen B. Reilly and Jay Barlow1
ABSTRACT
Annual finite rates of increase in dolphin population size were estimated to vary up to a maximum of
1.09, using simulation, based on ranges in vital rates. Vital rate ranges were defined from values reported
in the literature where possible, otherwise by making assumptions about biological or logical limits. Given
information on current values, or limits, of one or more vital rate, one can use the figures presented
to determine ranges of possible rates of increase in population size. The highest rates estimated here
(up to 1 .09) are probably unrealistic, because of the unlikely combinations of high fecundity and low mor-
tality needed to achieve them.
Rates of increase in population size are important
in determining management strategies for fish and
wildlife subject to exploitation. A common manage-
ment approach for setting incidental mortality or
harvest quotas is to use a stock-production model
(Schaeffer 1957; Allen 1976) with an assumed max-
imum rate of increase. For dolphins and other ceta-
ceans, rates of increase have proven extremely dif-
ficult to measure directly. Nonetheless, estimates
of this parameter are sometimes necessary, e.g., in
setting incidental mortality quotas for dolphin
populations involved in the eastern tropical Pacific
purse seine fishery for yellowfin tuna (Smith 1983).
In such situations, even a range, when rigorously
defined, can contribute substantially to delineating
the management options.
In this paper we define a range of reasonable
values of rate of increase (hereafter also referred
to as ROI) in dolphin population size, given what is
known or can be inferred about their age-specific
survival and fecundity distributions, or "vital rates".
We estimate rates of increase using population pro-
jection matrices for various parameter combina-
tions. We also suggest how the resulting ranges in
ROI can be further narrowed, given specific infor-
mation for an individual population.
There are many slightly different definitions for
rate of increase, but all share the commonsense no-
tion of change in population size over time. Caughley
(1977) reiterated the distinction between exponen-
tial and finite rates: finite rates, here symbolized A,
are related to exponential rates, here symbolized r,
by the simple conversion A = er. (We use the term
Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038.
"finite rates of increase" for A following Birch 1948.)
Further, within exponential rates Caughley distin-
guished among "intrinsic" (rm), "survival-fecun-
dity" (rs) and "observed" (r), rates.
In this paper we compute a series of rs values,
resulting from ranges of survival-fecundity distribu-
tions. The highest value of rs resulting from the
range of vital rates considered is our best estimate
of dolphin rm, or "r-max".
We define the ranges in vital rates based on the
literature for dolphins where possible. Otherwise,
we rely on information for other large mammals and
what appear to be logical or biological limits.
There are two previous studies of a similar nature
for delphinids. As part of a general review of life
history analysis of large mammals, Goodman (1981)
examined the relationships among rate of increase,
juvenile and adult survival rates. He looked at single
values for calving interval and age at first reproduc-
tion across ranges of survival rates. We take a
broader look at these relationships, examining
ranges for all four parameters.
Polacheck (1984) examined interparameter rela-
tionships for eastern tropical Pacific (ETP) dolphins,
Stenella spp., given specific vital rate estimates
available as of 1981, showing the values were not
consistent with a positive population growth rate.
Since then, revised estimates have become available
for some relevant parameters, and this specific case
has been reanalyzed, with similar general conclu-
sions.
The only reported dolphin rates of increase are
for Stenella coeruleoalba. For the year 1974, Kasuya
(1976) estimated a rate of 0.024 for the population
off Japan. This value was computed in a complex
manner, based on an observed fishing mortality,
assumed natural mortality, and estimated popula-
Manuscript accepted October 1985.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
527
FISHERY BULLETIN: VOL. 84, NO. 3
tion size, calving interval and sex ratio. Assuming
that calving interval was density dependent, Kasuya
(1976) estimated a maximum annual rate of increase
of 0.044 for this population of 5. coeruleoalba.
METHODS
The Model
Population growth rates are estimated here using
the familiar Leslie matrix model (Leslie 1945). A
simplified parameterization is used for which sur-
vival rates and fecundities remain constant over
many age classes. Four parameters are required: 1)
calving interval for reproductively mature females,
2) average age at first birth for females, 3) annual
adult (noncalf) survival rate, and 4) annual calf sur-
vival rate. This degree of detail corresponds to the
practical limitations in collecting data on wild
dolphin stocks.
The model is constructed with the assumption that
age class 1 corresponds to newly born calves (i.e.,
censuses occur immediately after the calving sea-
son). In fact, the model is not dependent on discrete
calving seasons, but this assumption helps in con-
ceptualizing some elements of the model. The fecun-
dities (elements of the first row of the Leslie matrix)
represent the number of female calves born in one
year per female of a given age class in the previous
year. Fecundities for mature age classes are esti-
mated as the annual pregnancy rate (the inverse of
calving interval) multiplied by the adult survival rate
(the probability that a [pregnant] female will sur-
vive to the calving season) multiplied by 0.5 (the frac-
tion of female offspring). The annual pregnancy rate
is estimated as the percent of sexually mature
females which are pregnant, divided by the gesta-
tion period (in years).
The choice of only two different survival rates for
all life stages was made because of data limitations
for dolphins. Perhaps a more biologically reasonable
assumption would be that dolphins have a U-shaped
mortality curve which is characteristic of mammals
in general (Spinage 1972; Caughley 1977; Siler 1979;
Smith and Polacheck 1981). Barlow2 incorporated
this typical mammalian survivorship curve in models
of growth for spotted dolphins, Stenella attenuata.
Our choice of a separate survival rate for calves was
based on the common observation of higher mortal-
ity in juvenile mammals (Caughley 1977; Siler 1979).
For convenience, juvenile mortality factors are com-
pressed into the first year's survival rates. This
simplification is justified because population growth
rates do not depend on the age at which juvenile
mortality actually occurs. We recognize that juvenile
mortality factors probably extend past the first year
of life, but insufficient data exist to justify including
this in our model. Higher mortality in old age was
not incorporated in our model, but maximum age
was limited to 50 yr. The survival rate at age 50 was
thus zero.
We calculate population growth rates for a range
of the four vital rate parameters mentioned above.
Finite population growth rates, A, that are associ-
ated with these parameter values were calculated
by solving Lotka's characteristic equation, using
Newton's method. The explicit form of Lotka's equa-
tion used is
50
1 = Z A~*l
x=l
x ™>x
2Barlow, Jay. 1986. Biological limits on current growth rate
of a spotted dolphin population (Stenella attenuata). Unpubl.
manuscr. Southwest Fisheries Center La Jolla Laboratory, Na-
tional Marine Fisheries Service, NOAA, 8604 La Jolla Shores
Drive, La Jolla, CA 92038.
where lx is the survivorship from birth to age class
x and mx is the fecundity of age class x.
Below, we define the ranges used for the four
population parameters and describe how they were
selected.
Survival Rates
Ranges in Noncalf Survival Rates
Few estimates of adult survival rates for dolphins
are available in the literature, primarily because ade-
quate data are difficult to collect. Kasuya (1976) pre-
sented annual survival rate estimates of 0.925 and
0.882 for exploited populations of Stenella attenuata
and S. coeruleoalba, respectively; however, his
method (log-linear regression) is biased (Barlow
1982), and he did not adjust for the effect of popula-
tion growth on age structure. A range of 0.85 to 0.97
was chosen for survival rates in this study. Values
<0.85 do not allow population growth for the ranges
of other parameters appropriate here, hence these
values were not considered. Values higher than 0.97
result in more than 22% of the population being over
50 yr old. This is inconsistent with estimates of
longevity for delphinids based on tooth layer counts
[58 yr in S. coeruleoalba (Sacher 1980), 38 yr in
S. attenuata (Hohn and Myrick3)], hence values
3Hohn, A. A., and A. C. Myrick, Jr. 1986. Age distribution
of the kill of spotted dolphins in the eastern tropical Pacific.
528
REILLY and BARLOW: INCREASE IN DOLPHIN POPULATION
>0.97 are untenable as mean per-capita survival
rates.
Ranges in Calf Survival Rate
Again little information is available on calf sur-
vival for dolphins. Kasuya (1976) estimated a juven-
ile survival rate that was higher than that of adults,
based on a balance equation. His methods assume
that populations are neither growing nor declining,
and he did not show that this assumption was met.
Also his juvenile period included all sexually im-
mature age classes. The overwhelming body of
evidence from terrestrial mammals is that very early
juvenile mortality is higher than adult mortality
(Spinage 1972; Caughley 1977; Siler 1979). Even
human populations had a first year survival rate of
<0.88 prior to modern antibiotics (Fruehling 1982,
data for U.S. circa 1900). An upper limit on calf sur-
vival rates was generated by assuming a calf is ab-
solutely dependent on its mother for 1 yr. A calf has
the same risk of dying as an adult, plus the addi-
tional risk of dying of starvation if its mother dies
before completing 1 yr of lactation. The upper limit
on calf survival would thus equal the square of the
adult survival rate. The lower limit on calf survival
rates was chosen as 0.50, a value that seems typical
of pinnipeds (Smith and Polacheck 1981) and long-
lived terrestrial mammals (Spinage 1972).
Fecundity-Related Rates
Ranges in Calving Interval
Observed calving intervals for dolphins general-
ly range from 2 to 4 yr (Perrin and Reilly 1984); con-
sequently, we have used this range in our computa-
tions. Intervals reported for killer whales (which are
also delphinids, but not "dolphins") are considerably
longer, up to 8 yr (e.g., Jonsgard and Lyshoel
1970).
The literature includes reports of calving inter-
vals <2 yr for dolphins. These reports do not appear
to be valid. Reevaluation of data for three of these
reports4 indicates that sampling was biased to-
ward pregnant females (Perrin and Reilly 1984), a
result of what may be a general tendency for
Unpubl. manuscr. Southwest Fisheries Center La Jolla Labora-
tory, National Marine Fisheries Service, NOAA, 8604 La Jolla
Shores Drive, La Jolla, CA 92038.
4Three reported cases of dolphin calving intervals <2 yr, later
found to be biased due to age and sex segregation, are Black Sea
Delphinus delphis and Tursiops truncatus (KJeinenberg 1956) and
Western Pacific Stenella coeruleoalba (Miyazaki and Nishiwaki
1978).
dolphins to segregate by age/sex groupings5.
The remaining reports of calving intervals <2 yr
are from very small sample sizes.6 Gestation periods
for dolphins are at minimum 10 mo, and intraspecific
variation is small. Reported lactation periods range
from 1 yr to over 2 yr (Perrin and Reilly 1984). Sum-
ming these two periods gives another indication that
dolphin calving intervals are not likely to be <2 yr.
An exception to the 2-yr minimum calving inter-
val would possibly be in a population experiencing
very high calf mortality, causing premature cessa-
tion of lactation, and allowing females the opportun-
ity to begin a new calving cycle (assuming there was
no seasonality to breeding which could require a
resting period before the next breeding season). To
include consideration of this case we would need to
devise an arbitrary function relating low calf sur-
vival to short calving intervals. The net result would
again be low rates of increase. To avoid such com-
plications we have simply used 2 yr as the minimum
average calving interval.
Ranges in Age at First Birth
The available data suggest a range in age at at-
tainment of sexual maturity of 6 to 12 yr for dolphins
(Perrin and Reilly 1984). Early reports of Black Sea
common dolphins, Delphinus delphis, attaining sex-
ual maturity at an average of 3 yr (Kleinenberg 1956)
are almost certainly due to faulty age determina-
tion7. Because of the recent findings for S. attenuata
from the ETP (Myrick et al. 1986), we considered
the ages at first birth up to 15 yr. In our formula-
tion of the Leslie model, if females mature and first
conceive at an average age of 10 yr, the first nonzero
fecundity would be in age class 11 (Table 1).
6Hohn, A. A., and M. D. Scott. 1983. Segregation by age in
schools of spotted dolphins in the eastern tropical Pacific. Fifth
Biennial Conf. Biol. Mar. Mammals, Abstr., p. 47.
6Henderson, J. R., W. F. Perrin, and R. B. Miller. 1980. Rate
of gross annual reproduction in dolphin populations (Stenella spp.
and Delphinus delphis) in the eastern tropical Pacific, 1973-78.
Southwest Fisheries Center, La Jolla, California, Admin. Rep.
LJ-80-02, 51 p.
7Myrick, A. C. Jr., Southwest Fisheries Center La Jolla Labor-
atory, National Marine Fisheries Service, NOAA, 8604 La Jolla
Shores Drive, La Jolla, CA 92038, pers. commun. June 1984.
Table 1 . — Parameters used and values included in the computa-
tion of rates of increase in dolphin population size.
Parameter
Values
Calving interval
Age at first birth
Calf survival rate
Noncalf survival rate (Sa)
2 yr 3 yr 4 yr
7 yr 9 yr 11 yr 13 yr 15 yr
0.50 0.52 0.54 . . . (Sa)2
0.850 0.855 0.860 0.865 . . . 0.970
529
FISHERY BULLETIN: VOL. 84, NO. 3
RESULTS
Figures 1 through 5 give finite rates of increase
(displayed as (A - 1) • 100) for the above ranges of
age at first birth, calving interval, and calf and non-
calf survival. The lower left corner of each panel is
blank because we did not consider cases where calf
survival exceeded the square of noncalf survival, for
the reason discussed in Methods.
The maximum finite rates of increase which would
result from the parameter ranges included here are
1.08 to 1.09. Rates as low as 0.89, i.e., decreaseof
11%/yr. also resulted from the parameter ranges
used.
Within the ranges of parameters examined here,
rate of increase is most sensitive to calving inter-
val and noncalf survival rate, followed by age at first
birth, and is relatively insensitive to changes in calf
survival rate. This is an expected result following
the reports by Eberhardt and Siniff (1977) and Good-
man (1981). An increase in calving interval of 1 yr
results in a decrease in ROI of about 0.02, holding
other parameters constant. For example, the max-
imum ROI for a 9 yr age at first birth is about 1.07
with a 2 yr calving interval. This ROI drops to 1.05
with a 3 yr calving interval. A decrease of 0.01 in
noncalf survival rate results in a 0.01 decrease in
ROI, while a 0.10 decrease in calf survival rate
decreases ROI by <0.01. Age at first birth appears
to be nonlinearly related to ROI over the ranges ex-
amined here. An increase in this age from 7 to 9 yr
results in a 0.02 decrease in ROI, while an increase
c
o
o
Q.
O
<D
-t->
CO
DC
"cO
>
>
CO
CO
o
Figures 1-5.— Contours of percent rate of increase in dolphin population size ((A - 1) • 100), as a function
0.50
0.60
0.96
0.85
0.90
0.95 0.97
0.95 0.97
0.96
0.85 0.90 0.95 0.97
Noncalf Survival Rate (proportion)
c
O
"+-
i_
o
a
o
i_
Q.
(D
-t->
CO
DC
"co
>
">
i_
CO
M—
CO
O
0.95 0.97
0.96
0.85
0.90
0.95 0.97
0.85 0.90 0.95 0.97
Noncalf Survival Rate (proportion)
Figure 1.— First reproduction of dolphin age class 7 yr: a) 2-yr
calving interval (upper panel); b) 3-yr calving interval (middle
panel); c) 4-yr calving interval (lower panel).
Figure 2.— First reproduction of dolphin age class 9 yr: a) 2-yr
calving interval (upper panel); b) 3-yr calving interval (middle
panel); c) 4-yr calving interval (lower panel).
530
REILLY and BARLOW: INCREASE IN DOLPHIN POPULATION
from 11 to 13 yr causes only a 0.01 decrease in
ROI.
DISCUSSION
The ranges of rate of increase estimated here are
potentially useful in bracketing possible ROIs for
delphinids in general. For any particular population
it should be possible to further narrow the range of
likely values of ROI, given available estimates for
vital rates. For example, Tursiops truncatus from
the northeast coast of Florida reportedly attain sex-
ual maturity at 12 yr on the average (Sergeant et
al. 1973) and have a 12-mo gestation period (Essa-
pian 1963), giving an estimated age at first birth of
13 yr. Knowledge of this single parameter can nar-
row consideration to Figure 4. Here the estimated
range in ROI is up to a maximum of 1.05, for the
extreme case of an average calving interval of 2 yr,
and noncalf survival >0.96. Additional knowledge
of, say, minimal calving interval for Tursiops could
further narrow consideration to one of the three
panels of Figure 4, and establish minimal survival
rates for positive growth rates, or the maximum rate
of increase possible, given the above constraints on
age at first birth and calving interval.
We assume that the ranges defined here also en-
compass the limits within which vital rates for any
one dolphin species might change in response to
changes in population density. This obviously entails
making simplistic assumptions about density depen-
dence in vital rates, and therefore in rate of increase.
of calf and noncalf survival rates, for the following combinations of calving interval and age at first reproduction:
c
O
O
Q.
O
CD
■♦-•
CO
DC
"cO
>
>
CO
"co
O
0.95 0.97 •■£
0.95 0.97
0.85 0.90 0.95 0.97
Noncalf Survival Rate (proportion)
Figure 3.— First reproduction of dolphin age class 11 yr: a) 2-yr
calving interval (upper panel); b) 3-yr calving interval (middle
panel); c) 4-yr calving interval (lower panel).
C
o
o
a
o
CD
CO
DC
"c0
>
■>
Z5
CO
"cO
O
0.95 0.97
0.96
0.85
0.90
0.95 0.97
0.85 0.90 0.95 0.97
Noncalf Survival Rate (proportion)
Figure 4.— First reproduction of dolphin age class 13 yr: a) 2-yr
calving interval (upper panel); b) 3-yr calving interval (middle
panel); c) 4-yr calving interval (lower panel).
531
FISHERY BULLETIN: VOL. 84, NO. 3
These assumptions are implicit in the concept of
r-max.
There is no evidence that the highest rates of in-
crease calculated here can be achieved by any real
dolphin population. Trade offs may exist between
survival and reproduction. Because of this, some of
the parameter combinations examined here are
probably unlikely, especially combinations of the ex-
treme values, i.e., those producing the highest rates
of increase.
Although our figures also present minimum values
based on parameter combinations we used, we do
not believe that these will be useful in setting lower
bounds on finite rates of increase. Catastrophic
events can always lead to rapid extirpation of a
population. In fact, it is clear that dolphins (and
other animals with similar life histories) can
c
o
'■*-•
o
Q.
O
0
CO
DC
"cO
>
>
CO
CO
O
0.95 0.97
0.95 0.97
0.85 0.90 0.95 0.97
Noncalf Survival Rate (proportion)
Figure 5.— First reproduction of dolphin age class 15 yr: a) 2-yr
calving interval (upper panel); b) 3-yr calving interval (middle
panel); c) 4-yr calving interval (lower panel).
decrease in number much faster than they can
increase.
ACKNOWLEDGMENTS
This study benefited greatly from reviews by J.
Breiwick, D. Chapman, D. DeMaster, D. Goodman,
J. Hedgepeth, F. Hester, G. Sakagawa, D. Siniff,
T. Smith, and an anonymous reviewer. We sincere-
ly thank these people for their contributions.
LITERATURE CITED
Allen, K. R.
1976. A more flexible model for baleen whale populations.
Rep. Int. Whaling Comm. 26: App. Report and Papers of
the Scientific Committee, p. 247-263.
Barlow, J.
1982. Methods and applications in estimating mortality and
other vital rates. Ph.D. Thesis, Univ. California, San Diego,
177 p.
Birch, L. C.
1948. The intrinsic rate of natural increase of an insect
population. J. Anim. Ecol. 17:15-26.
Caughley, G.
1977. Analysis of vertebrate populations. Wiley-Inter-
science, N.Y., 234 p.
Eberhardt, L. L., and D. B. Siniff.
1977. Population dynamics and marine mammal management
policies. J. Fish. Res. Board Can. 34:183-190.
Essapian, F. S.
1963. Observations on abnormalities of parturition in captive
bottlenosed dolphins, Tursiops truncatus, and concurrent
behavior of other porpoises. J. Mammal. 44:405-414.
Fruehling, J. A. (editor).
1982. Sourcebook on death and dying. Marquis Prof. Publ.,
Chicago, 788 p.
Goodman, D.
1981. Life history analysis of large mammals. In C. W.
Fowler and T. D. Smith (editors), Dynamics of large mam-
mal populations, p. 415-436. Wiley, N.Y.
JONSGARD, A., AND P. B. LYSHOEL.
1970. A contribution to the knowledge of the biology of the
killer whale Orcinus orca (L.). Nytt. Mag. Zool. (Oslo)
18:41-48.
Kasuya, T.
1976. Reconsideration of life history parameters of the
spotted and striped dolphins based on cemental layers. Sci.
Rep. Whales Res. Inst. Tokyo 28:73-106.
Kleinenberg, S. E.
1956. Miekopitauishchenie Chernogo i Azovskogo Morei
(Mammals of the Black Sea and Sea of Azov). Akad. Nauk.,
Moscow, 288 p. (Fish. Mar. Serv., Quebec, 1978, Transl.
ser. 4319, 428 p.)
Leslie, P. H.
1945. On the use of matrices in certain population mathe-
matics. Biometrika 33:183-212.
MlYAZAKI, N., AND M. NlSHIWAKI.
1978. School structure of the striped dolphin off the Pacific
coast of Japan. Sci. Rep. Whales Res. Inst., Tokyo 30:
65-115.
532
REILLY and BARLOW: INCREASE IN DOLPHIN POPULATION
Myrick, A. C. Jr., A. A. Hohn, J. Barlow, and P. A. Sloan.
1986. Reproductive biology of female spotted dolphins,
Stenella attenuata, from the eastern tropical Pacific. Fish.
Bull., U.S. 84:247-259.
Perrin, W. F., and S. B. Reilly.
1984. Reproductive parameters of dolphins and small whales
of the family delphinidae. In W. F. Perrin, D. P. DeMaster,
and R. L. Brownell, Jr. (editors), Cetacean reproduction, p.
181-185. Rep. Int. Whaling Comm. Spec. Issue 6.
Sacher, G. A.
1980. The constitutional basis for longevity in the Cetacea:
Do the whales and the terrestrial mammals obey the same
laws? In W. F. Perrin and A. C. Myrick, Jr. (editors), Age
determination of toothed whales and sirenians, 229 p. Rep.
Int. Whaling Comm., Spec. Issue 3.
Schaefer, M. B.
1957. Some aspects of the dynamics of populations important
to the management of commercial marine fisheries. Inter-
Am. Trop. Tuna Comm. Bull. 1:27-56.
Sergeant, D. E., D. K. Caldwell, and M. C. Caldwell.
1973. Age, growth and maturity of bottlenosed dolphins (Tur-
siops truncatus) from northeast Florida. J. Fish. Res.
Board Can. 30:1009-1011.
Siler, W.
1979. A competing-risk model for animal mortality. Ecology
60:750-757.
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.
Smith, T., and T. Polacheck.
1981. Reexamination of the life table for northern fur seals
with implications about population regulatory mechanisms.
In C. W. Fowler and T. D. Smith (editors), Dynamics of large
mammal populations. Wiley, N.Y.
Spinage, C. A.
1972. African ungulate life tables. Ecology 53:645-652.
533
DISCRETE-TIME DIFFERENCE MODEL FOR
SIMULATING INTERACTING FISH POPULATION DYNAMICS
C. Allen Atkinson1
ABSTRACT
The dynamics of interacting fish populations are modeled using a coupled set of discrete-time difference
equations. The basic equations describe predator-prey and competitive relationships analagous to the
first-order expressions used in standard differential equation models. Population births and aging are
represented using a modified Leslie matrix. A spatial representation is also incorporated and consists
of a number of separate compartments, each containing interacting population groups which can be inter-
changed between compartments during a given time period. The potential applicability of the discrete-
time formulation is demonstrated via a simulation of the multispecies fish populations within the Califor-
nia Current during the sardine population collapse of 1930-60.
Numerous mathematical models of interacting multi-
species fish populations are found in the literature
(Riffenburgh 1969; Saila and Parrish 1972; May et
al. 1979; Steele 1979). Depending on the nature of
a particular ecosystem and the desired resolution
level for its components and processes, these models
can become extremely complex (Parrish 1975;
Anderson and Ursin 1977; Laevastu and Favorite
1978). The major limitation in practical fisheries ap-
plications is the lack of sufficient field data to ade-
quately estimate many of the model parameters,
particularly the population interaction terms in com-
plex multispecies models (Goodall 1972).
The two objectives in the present multispecies
model development are 1) to establish a general
mathematical form applicable to a variety of prac-
tical fisheries problems and 2) to provide an efficient
computational tool for simulating complex multi-
species systems. The latter feature has implications
for dealing with the problem of model parameter
uncertainty via specialized Monte Carlo and non-
linear programming procedures as discussed by
Atkinson (1985).
The proposed formulation consists of a unique set
of discrete-time difference equations that describe
first-order dynamic processes affecting some ar-
bitrary number of interacting fish populations at one
or more trophic levels. The discrete equations are
particularly well suited for computer implementa-
tion. There are no requirements for sophisticated
integration routines (e.g., Runge-Kutta, Adams-
Moulton), and the equations have inherent numerical
'System Science Applications, Inc., 121 Via Pasqual, Redondo
Beach, CA 90277.
Manuscript accepted January 1986.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
stability. Difference equations are also compatible
with fisheries data sets (e.g., eggs and larvae sur-
veys) which are usually sampled seasonally.
The essential biological processes represented in
the model are spawning, growth, mortalities, age
class structure, nonuniform spatial distributions,
and migrations. Certain of these features, such as
spawning, sexual maturation, and migrations, are
often most conveniently described in a discrete form
as assumed in the model. Seasonal time steps are
natural increments for consideration as the values
of appropriate model parameters can then be easily
changed to relate seasonal fish behavior.
The mathematical details of the discrete-time
difference model are developed below. The special
problem of estimating model parameters in practical
applications is also briefly discussed. The dynamics
of the California Current fish populations are then
modeled and simulation runs performed correspond-
ing to the period of the sardine collapse in 1930-60.
Comparisons are made between the simulation
results and the actual (estimated) population
responses.
DEVELOPMENT OF THE DISCRETE-TIME
DIFFERENCE EQUATIONS
The dominant first-order ecological processes af-
fecting fish populations are modeled by discrete-time
difference equations. For convenience in the mathe-
matical development, these processes are assumed
to occur in the following sequence during a given
time period: 1) individual growth and mortalities;
2) spatial redistributions of the surviving members;
and 3) births and age class changes of the surviving,
535
FISHERY BULLETIN: VOL. 84, NO. 3
redistributed populations. Consistent with the first-
order nature of the formulas, certain simplifications
are expected to be incorporated in the ecological
representation including implicit modeling of lower
trophic levels (e.g., phytoplankton and zooplankton)
and functional groupings of less important species
as competitors, predators, and prey.
Growth and Mortalities
First-order differential equations of the following
general form are typically used to describe the
growth and mortalities of a population P, under
competitive and predator-prey influences with itself
and other populations:
d t
(rt - u%P - v,P + WjP)Pi
(1)
where r, = survival/growth parameter
P = population vector
= \P\ > " 2 t • • • t "it • ■ • ) Pn)
u{ = competition coefficient vector
— {tin , u,{
2) ■
U;
uin)
Vi =
W: =
predation coefficient vector
prey coefficient vector.
The coefficient vectors ut , v{ , and wx contain ap-
propriate zeros such that only the active interactions
between populations are defined. (Note that vector
multiplication is implied by the forms such as u^P.)
The competition terms correspond to the standard
Gause model, while the predator-prey terms corres-
pond to the simple Lotka-Volterra model (Pielou
1977). The population variables P{ can be expressed
in units of either numbers of individuals or total
biomass, with the coefficients defined accordingly.
Assuming a small time step (At) relative to the
characteristic time of the system (1/r), a discrete-
time approximation is found directly by integrating
Equation (1) to give
Pt(M) = er>M
-u PM
-v P&t
0w, PM
■Pr(0) (2)
These exponential terms form the basis of the dif-
ference model. However, some modification and in-
terpretation of terms is required in order to describe
a general form appropriate over a range of popula-
tion levels.
The most obvious inadequacy of Equation (2) is
the positive exponential prey term, ew<PM, which
gets increasingly larger as prey increases without
ever reaching a saturation condition. A more ap-
propriate form is the predator feeding model given
by Ivlev (1961):
F = Fmax (1 - e-V)
(3)
where F is the predator feeding ration and i, is an
associated prey coefficient, assuming that this form
can also be used to describe the predator's growth/
survival as a function of prey density.
The proposed difference equation for expressing
population growth and mortalities during a At time
step is
Pi(t + 1) = St e~°.p e-W (1 - Rt e-^)Pt(t) (4)
where St = maximum survival/growth rate per
time period
at = discrete form of competition coeffi-
cient vector
Pi = discrete form of predation coefficient
vector
Rt = starvation mortality factor
Yi = discrete form of prey coefficient
vector.
The terms in this generalized form need further
discussion and interpretation.
The maximum survival/growth rate factor, S, ac-
counts for population births (if single age class),
growth (if biomass units), and certain mortalities
such as fishing, disease, and old age. It also accounts
for predatory deaths caused by populations not ex-
plicitly included in the ecosystem model. It does not
account for predation, competition, and prey avail-
ability effects associated with the modeled popula-
tions, which are explicitly stated by the other terms
of Equation (4). Maximum survival/growth is defined
under ideal conditions when competition and pre-
dation influences are negligible and there is an abun-
dant supply of prey.
The a competition coefficient is the exponential
equivalent to the Gause term in Equation (1) and
represents a basic damping factor inhibiting popula-
tion expansion. Self-competition generally relates
to the essential environmental resources such as
food supply and habitat space. Additional intra-
population effects can come into play at the extreme
ranges of population densities to complicate this in-
terpretation, such as decreased fecundity caused by
crowding (Parrish 1975) and decreased birth rates
at very low densities (May 1973). Competition be-
tween population groups involves considerations of
niche overlap relative to the common resources for
which they compete (May 1973). Active competition
536
ATKINSON: FISH POPULATION DYNAMICS
interference effects may also be involved (Levine
1976; Vance 1978). Since my model deals only with
first-order effects, the components of the coefficient
vector a are defined as constants and assumed to
be related to the dominant competitive mechanisms
acting over the range of population densities ex-
pected in the simulation.
The ft predation coefficient in Equation (4) corres-
ponds to the Lotka-Volterra term in the differen-
tial equation and implies unlimited attack capacity
per predator (May 1973). Relative values of these
vector components reflect the comparative attack
rates of the different predators in the model. The
effective ft coefficients perhaps should be reduced
when there are relatively few predators compared
with the size of population P{ because of saturated
feeding. However, predation is probably a second-
ary factor under these conditions as competitive
limitations will tend to dominate. Based on first-
order arguments, constant ft components are as-
sumed to apply over a reasonable range of predator
densities. Leslie and Grower (1960) make a similar
assumption in the prey equation of their two-
component predator-prey model. Their predator
response equation, on the other hand, saturates at
high relative prey levels as in the present model.
The prey form, represented in Equation (4),
reflects Ivlev's form (Equation (3)) and implies some
upper bound survival/growth rate under abundant
prey conditions. The present form also incorporates
a starvation mortality parameter, R, that describes
a worst case condition without prey. This param-
eter would typically equal one unless the M time step
is short or an alternative food source not explicitly
included in the modeling is available to sustain the
population.
Component magnitudes of the prey coefficient
vector, y, relate differences in the relative efficien-
cy with which alternative prey are captured and
utilized for predator growth and/or survival. At
similar prey densities, a predator may utilize dif-
ferent capture methods and feed at higher or lower
rates depending on the size and behavioral charac-
teristics of a particular prey (Parsons and Takahashi
1973). Note, however, from the form of the expon-
ential prey term in Equation (4), that any one suffi-
ciently abundant prey population can satisfy the
predator feeding requirement.
Finally, in comparing the present development
with traditional fishery models, note that Equation
(4) can be directly related to the single species
recruitment models of Ricker (1958) and Beverton
and Holt (1957) if the time step is defined as the
maturation time between spawning and recruit-
ment. Also, a comparable fishing term can be broken
out of the survival/growth parameter as follows:
S =
SfS0
(5)
where Sf is the fishing survival rate and S0 incor-
porates the remaining survival/growth effects. A
corresponding fishing mortality rate, /, can be
defined and related to fishing effort, Ej, as in the
Beverton and Holt (1957) model:
/ =
■\nSf
M
efEf
(6)
where E* is the fishing efficiency and Af is the fish-
ing area. The general compatability with traditional
fishery models is stressed.
Spatial Redistributions
A simplified picture of fish stock migratory pat-
terns during a typical life cycle is illustrated in
Figure 1. Adult fish move from the feeding grounds
to the spawning grounds and return; larval fish drift
from the spawning to the nursery ground; and
recruits join the adult stock on the feeding grounds.
The seasonal timing of these events is quite regular
as are the spatial regions to which the stock return
during the cycle (Cushing 1975).
Large-scale spatial patterns will be represented
in the model by a number of "boxes" or compart-
ments, each with a defined size and each contain-
FEEDING
GROUND
SPAWNING
AREA
NURSERY
AREA
Figure 1.— Typical fish migratory pattern (from Cushing 1975).
537
FISHERY BULLETIN: VOL. 84, NO. 3
ing segments of the various ecosystem populations.
Population variables will now be uniquely assigned
for each box and expressed in density units, such
as numbers or kilograms per hectare. Spatial re-
distributions are assumed to occur during a given
time period via migration, net drift, or turbulent
dispersion. The resultant redistribution process is
expressed by defining population transfers between
boxes.
Spatial redistribution is applied to the surviving
populations determined from Equation (4) and is
described by
PUt + 1,2)
M
= I
m= 1
grkPf(t + 1,1)
(7)
where
P\(t + 1,2) = density of surviving population i
in compartment k after spatial
redistributions
Pf(t + 1,1) = density of surviving population i
in compartment m before spatial
redistributions
M = total number of spatial compart-
ments
= population i transport coefficient
for the exchange from compart-
ment m to compartment k.
9i
ink
The g coefficient defines the population fraction in-
volved in the exchange with an adjustment to ac-
count for the difference in area or volume between
compartments. If no transit occurs between com-
partments, the value of the respective coefficient
is zero.
Birth and Aging Processes
The larvae and juvenile age classes of fish popula-
tions have markedly different survival rates and
behavioral characteristics than do adult populations.
These differences have potentially important first-
order ecological consequences and are, therefore,
of concern in the present model development.
A modified version of the Leslie matrix as pre-
sented by Lefkovitch (1965) is adopted here. Popula-
tions are grouped by stages which can be of unequal
duration with no restriction to single year classes.
The birth and aging matrix transform for N such
stages is given by
n («+i,s)
P&0 + 1.S)
Pfc(*+lf8)
n^+u)
Oil Ji2 j% ■ JiN
an ba 0 . 0
0 al2 bl3 . 0
0 0 0
P!i (t + 1,2)
Pfc(t+1,2)
P% (t + 1,2)
PL (t+1,2)
(8)
Pl(t +
where
P|- (t + 1,3) = density of population %, age class
j after accounting for births and
aging in compartment k
1,2) = density of population i, age class
j before accounting for births and
aging, but after accounting for
spatial redistributions to compart-
ment k
a{j = fraction of population i, age class
j advancing to age class j + 1
6y = fraction of population i, age class
j remaining in age class j
flj = fecundity function for population
i, age class j in compartment k.
The coefficients a and 6 are functions of the size
of the time step and the division of ages within the
population. Equation (8) also implies a fixed age
distribution within an age class, such as a uniform
distribution.
The fecundity term,/, is a function of the popula-
tion age class, as well as being time and space depen-
dent. Explicit population crowding effects are
neglected here because they would be comingled
with the other density-dependent terms in Equation
(4).
Composite Ecosystem Dynamics
Equations
The above equations are combined and expressed
by the general ecosystem dynamics model given
below. The final surviving, redistributed, and aged
population vector at the end of the time period has
been redefined as P(t +1) = P(t +1,3).
538
ATKINSON: FISH POPULATION DYNAMICS
Nt M
PUt +1) = I I F%JLt) gfn(t) Sfn(t) e-J*V
'Jv ' n = l m=\ J
x g-Wtt) [l _ fl£(f) rr,/"(0]
x Pfi(0 (9)
where m is summed over all spatial compartments
M; n is summed over all population subgroups N{,
and F\jjf) is defined by
A(t);j = l,n>2
bm(t);j ^ l,n = j
ain{t);j ^ 2,n = j -1
0 ; otherwise.
n„ (o =
(10)
The model parameters in Equations (9) and (10)
consist of maximum survival/growth rates (S), star-
vation mortality rates (R), transport terms (g), fecun-
dity factors (/), age class changes (a and b), and
population interaction coefficients (a, ft, and y). Time
dependency is indicated for all parameters except
the interaction terms. Space dependency is assumed
to apply to all but age class changes and interaction
terms. If the parameters are described by probabi-
listic functions, the model becomes a stochastic
representation.
The above difference model represents a com-
prehensive description of coupled fish population
dynamics and is proposed for general application.
The form of Equation (9) is particularly well suited
for computer implementation; it provides an effi-
cient time-step simulation capability without requir-
ing a numerical integration scheme. The model can
be conveniently programmed on a mini-computer
system and used to simulate complex multispecies
population dynamics.
MODEL PARAMETER ESTIMATION IN
PRACTICAL APPLICATIONS
The predictive power of the difference model in
practical applications is obviously dependent on the
knowledge of the ecosystem processes and the abil-
ity to estimate the associated parameters used in
the modeling. This situation is true for any eco-
system model whether it consists of difference
equations, differential equations, or any other for-
mulation. In fact, I (1980) showed that difference
equations representing multispecies populations can
be used to approximate the complex response modes
of differential equations by relating parameters and
choosing suitably small differencing time steps. I
also showed that the difference model suffers from
a similar sensitivity to the parameter estimates; the
problem becomes more severe with increasing eco-
system complexity.
Certain parameters in either difference or dif-
ferential equation models can be roughly estimated
from field and/or laboratory studies. Examples in-
clude fecundity and growth rates of individual fish
which can be observed directly. Population-level
parameters, such as interaction and transport
terms, are more difficult to estimate given the
dynamic, wide-ranging nature of fish behavior. Even
with extensive field sampling and the use of multi-
variate statistical techniques to sort out stochastic
environmental features (Reid and Mackay 1968;
Mobley 1973; Poole 1976), these parameter esti-
mates will typically have a large degree of
uncertainty.
The potential advantage of difference models in
dealing with parameter uncertainty is related to
their computational efficiency. When parameter
uncertainty is represented in a probabilistic frame-
work, Monte Carlo procedures can be applied to
statistically describe population response character-
istics based on large numbers of simulation runs.
Probabilistic descriptions of parameter uncertain-
ty can express both the inherent stochastic nature
of the ecosystem and the parameter estimation er-
ror. One problem is that the stochastic ecosystem
features, which are of primary interest, will typically
be masked in the statistics by the large parameter
estimation errors if realistic values for the latter are
included.
I (1980, in press) used nonlinear programming
(NLP) techniques to treat parameter uncertainty in
dynamics models for a general class of ecosystem
problem. My approach is summarized below; it has
been used for resolving parameter estimates in the
difference model application discussed in the section
that follows.
An NLP problem can be stated in the following
general form:
minimize
M
subject to
g(x) = 0
X0 < X < xm
where x is the variable vector with upper and lower
bounds of x0 and xm, respectively; f(x) is the so-
called objective function; and g{x) is a vector func-
tion of implicit constraints.
539
FISHERY BULLETIN: VOL. 84, NO. 3
The problem scenario for my NLP formulation is
that of predicting the dynamic response of eco-
system populations to a given perturbation. The
response is characterized over some period of in-
terest by the objective function which, depending
on the particular problem, can be equated to average
population numbers, final population levels, worst-
year fishery catch, or some other dynamic feature.
The ecological parameters in the dynamics model
become the variables with bounds corresponding to
the estimated parameter uncertainty range.
Implicit parameter constraints are added to the
formulation based on available population history
data, ecosystem stability observations, or any known
or postulated relationships between parameters. The
historical population data are substituted directly
into the difference equations, or other assumed
dynamics equations. In effect, such constraints force
the response modes of the dynamics model to include
past population observations, albeit ones that oc-
curred under different (known) conditions than
those of interest in the future. Stability observations
also infer conditions on the dynamics equations and,
hence, model parameters. However, there are prac-
tical issues in formulating such conditions. Lyapunov
stability analysis techniques (Brogan 1974), while
applicable to nonlinear system analysis, are not
readily defined for the complex difference equations.
Efficient NLP computational procedures have
been applied by me (1980) to solve the special eco-
system formulation described above. A search takes
place through bounded parameter space for extreme
(minimum and maximum) objective function values
while maintaining the equality of the implicit con-
straints, i.e., the search proceeds on the "constraint
surface" in parameter space. The key to an effec-
tive problem solution is the computational require-
ments of the dynamics model which is used in both
constraint formulation and for evaluating the objec-
tive function at each search step. While the NLP
approach does not give definitive estimates of in-
dividual model parameters, it strongly delimits their
range of values via the interrelationships established
by the implicit constraints (Atkinson 1980).
ECOSYSTEM SIMULATIONS USING
THE DIFFERENTIAL EQUATION MODEL
The discrete-time multispecies dynamics model
given by Equation (9) has been implemented as a
FORTRAN computer program and used to perform
a variety of simulations of theoretical and applied
fisheries scenarios (Atkinson 1980). A case of some
practical interest, the collapse of the sardine popula-
tion within the California Current region, will be
described and used to demonstrate the potential
model utility.
General Description of
the Sardine Population Collapse
off California
The waters of the California Current flow south-
ward along the west coast of North America cover-
ing the general region are illustrated in Figure 2.
While the California Current supports a diverse
group of fish, the sardine fishery was by far the most
important in the early years of this century until the
dramatic collapse of the sardine population in
1930-60. A large increase in fishing effort took place
during this time and apparently caused, or at least
was associated with the sardine population collapse.
The estimated history of the sardine population from
1930 to 1960 as derived by Murphy (1966) is shown
in Figure 3.
Two sets of anchovy population estimates for the
1930-60 time frame are also presented in Figure 3.
Although these data are confused by significant gaps
and strong fluctuations from year to year, there does
appear to be a significant population increase from
levels in the 1940's and early 1950's to that near
the end of the 1950's. Since the anchovy is the chief
competitor of the sardine with similar food require-
ments and overlapping habitat boundaries, the
general indication is that the anchovy replaced the
sardine within the trophic structure (Murphy 1966;
Gulland 1971). Murphy's (1966) 3-yr averaged data
provides the clearest evidence of this increasing
trend. Smith's (1972) yearly estimates show that the
anchovy population actually declined from 1940-41
to 1950 (the next year in which data was available),
before a sharp rise occurred. The significant varia-
tions evident in both anchovy and sardine data are
probably caused by random environmental in-
fluences on recruitment success (Lasker 1978; Par-
rish et al. 1981; Methot 1983).
Soutar and Isaacs (1974) presented some interest-
ing longer term data on the sardine and anchovy
(plus other pelagic fish) as derived from sedimen-
tary scale depositions in anaerobic basins off South-
ern California and Baja California. The deposition
rate, which is averaged by 5-yr periods, provides a
relative picture of the population variations over the
last 150 yr (up to 1970). The data for the 1930-60
time frame indicate similar trends to that above, i.e.,
decreasing sardine levels and increasing anchovy
levels. However, significant sardine and anchovy
540
ATKINSON: FISH POPULATION DYNAMICS
r^T"
% '#
*o^
BRITISH
COLUMBIA
50°
«
WL
i§N
WASH.V^^
45°
— /
OREGON
V
>» AVERAGE YEARLY SARDINE
CATCH (1920- 1950)*
PACIFIC NORTHWEST 44K TONS
\
40°
— \
N.CALIFORNIA
S. CALIFORNIA
= 208KTONS
= 115KTONS
fs
^Y
BAJA CALIFORNIA
/
= 0 TONS**
35°
4 /
\ CALIF.
i
"'•v'\ U* 1 1
\7 \ V
30°
mm SARDINE ^
1 1 DISTRIBUTION
F^Tl FISHING
Hii LOCALITIES
mm
25°
'FROM DATA IN MURPHY (1966)
**BAJA FISHERY NOT SIGNIFICANT
UNTIL AFTER 1950
I
I
i
I
125°
120c
115<
110°
Figure 2.— Map of the California Current region showing sardine distribution and major fishing localities in the period
before 1950 (from Murphy 1966).
541
FISHERY BULLETIN: VOL. 84, NO. 3
4000
z
2 3000
z
o
_j 2000 h
a.
O
a.
1000 -
r
i
ANCHOVY '
™— A
V / «
▲
/
/
f l #
ft /
SARDINES' 1
4\ ^
—
I / \ / *•
\ / V
v A •
\ A*
1
1 1
1920
30
40
YEAR
50
1960
Figure 3.— Estimated adult populations of sardine and anchovy
during the 1930-60 sardine collapse period. The solid line cor-
responds to yearly sardine estimates by Murphy (1966). The dashed
line with triangles corresponds to 3-yr average anchovy esti-
mates also by Murphy; the initial point is a 2-yr estimate with a
data gap until 1951. The circles correspond to yearly anchovy
estimates by Smith (1972); a data gap exists between 1941 and
1950.
variations are also evident in earlier times before
fishing pressure became a significant factor in the
ecosystem. For example, the sardine history showed
extremely low levels in 1865-80 comparable to the
levels after 1940. The earlier anchovy record, while
also having periods of relatively high and low
sedimentation rate, appears to have been at con-
sistently higher levels before 1930-60, even higher
than the recent increase of the late 1950's. Soutar
and Isaacs (1974) stated that relatively unproduc-
tive conditions have apparently existed for the past
30 yr or so and have generally affected fish popula-
tions of the California Current.
Model Formulation
subsystem defined by Riffenburgh (1969) and shown
in Figure 4. While not a comprehensive description
of this ecosystem, I use this representation to
demonstrate the application of the difference model
in a reasonably complex fishery situation. The sar-
dine ecosystem will be simulated during the period
from 1932 to 1952 spanning the years of the major
sardine collapse.
The sardine population is divided into three age
groups: larval-year stages, yearlings, and adults.
The larval year is the most vulnerable period of the
sardines' development during which it goes through
many fundamental changes. The yearlings are the
in-between stage to the sexually mature adult
members of the population, which are defined to be
2-yr-olds and above. Early stages of the sardine feed
on phytoplankton while the adults feed primarily on
zooplankton (Huppert et al. 1980). The adults are
also predators of their own larval stages and those
of the anchovy as indicated in Figure 4.
The anchovy population is divided into two groups,
larvae and adult, which have similar intergroup rela-
tionships and feeding habits to the corresponding
sardine groups. Competitor and predator groups to
the sardine and anchovy are defined as lumped
assemblages, both encompassing a broad range of
diverse fish species; the competitor group also con-
tains many invertebrates. The pelagic fish com-
petitors (e.g., jack mackerel) are assumed to behave
similarly to the sardine and anchovy except that
some of the larger members feed on the sardine
yearling stage (Riffenburgh 1969). The predators
(e.g., hake and baracuda) feed on the adults of the
sardine-anchovy-competitor trophic level and also
have other prey that have been decoupled from the
modeled subsystem. Phytoplankton and zooplankton
groups are modeled implicitly as carrying capacity
terms.
Additional model assumptions are that 1) spatial
features are not critical (i.e., one spatial compart-
ment is used), and 2) seasonal effects can be ignored
(i.e., a yearly time step is defined). These two
assumptions are probably not justifiable in the time
period after 1950 or so, because of the shift of
dominance from the northern sardine subpopulation
to the southern one. Important differences in such
factors as natural survival rates, maturation charac-
teristics, and fishing effort exist for these subpopula-
tions (Murphy 1966).
The waters of the California Current region, with
their chemical and biological constituents, can be
viewed as an ecological system (Sette 1969). The
present model focuses on the sardine and anchovy
Discrete-Time Difference Equations
The difference model representing the seven inter-
acting populations of the sardine ecosystem is pre-
542
ATKINSON: FISH POPULATION DYNAMICS
c
0 SARDINE
LARVAE
(© ANCHOVY
LARVAE
(3) SARDINE
ADULT
(D ANCHOVY
ADULT
(6) COMPETITOR
GROUP
© PREDATOR
GROUP
(ADDITIONAL
FOOD SUPPLY)
)
Figure 4.— Schematic showing interactions between sardine ecosystem groups as modeled by Riffenburg (1969). Competitive
relationships are indicated by the connecting lines with dual arrowheads, while predator-prey relationships are defined by
arrows pointing to the predator.
sented in Table 1. These equations reflect the
general form of Equation (9) for a single spatial com-
partment. Parameters are defined for all processes
other than transport, including competition, pred-
ator-prey, survival/growth, births, and fecundity.
These parameters are assumed to be independent
of the year during the 1932-52 simulation period,
except for 1) the sardine fishing rate, 63(t), and 2)
a sardine larvae survival factor, E^t). The latter
are related to the parameters presented earlier by
63(t) = 1 - Sf3(t)
E,(t) = S.iD/S,
where Sf3 is defined in Equation (5) and S: is the
average (reference) sardine larvae survival rate dur-
ing 1932-52. The time-varying fishing rate and lar-
vae survival factor represent the "drivers" perturb-
ing the ecosystem during the sardine collapse period.
Time-varying representations may also be ap-
Table 1— Difference equations describing biomass dynamics of the sardine ecosystem
populations. Note that age sub-groups are indexed as separate populations to simplify
the nomenclature. Also, all populations in exponentials are assumed to be at time f.
Population 1 -
P,(t + 1)
Population 2 -
P2(t + 1)
Population 3 ■
P3(t +1)
Population 4
P*(t + 1]
Population 5
P5(t +1)
Population 6
P6{t + 1)
Population 7 -
P7(t + 1)
sardine larvae
= f3S3.o[1 - <M0]exp(-a33P3 - a35P5 - 036P6)exp(-/337P7)P3(f)
sardine yearling
= E:(t)S, exp(-auP, - a14P4)exp(-/3l3P3 - /515P5 - p,6P6)P,(t)
sardine adult
= S2exp(-a22P2 - a25P5)exp(-/326P6)P2(f)
+ S30[1 - d3(f)]exp(-a33P3 - a35P5 - a36P6)exp(-/337P7)P3(0
anchovy larvae
= f5S5exp(-a53P3 - a55P5 - a56P6)exp(-/357P7)P5(f)
anchovy adult
= S4exp(-a41P, - a44P4)exp(-/?43P3 - /345P5 - /?46P6)P4(f)
+ S5exp(-o53P3 - a55P5 - a56P6)exp(-/357P7)P5(f)
competitor group
= S6exp(-a63P3 - a65P5 - a66P6)exp(-/?67P7)P6(0
predator group
= S7exp(-a77P7j[1 - ff7exp(-y73P3 - y75P5 - y76P6)]P7(f)
543
FISHERY BULLETIN: VOL. 84, NO. 3
propriate for other population parameters such as
anchovy larvae survival but are ignored here. The
modeling emphasizes those features directly impact-
ing the adult sardine population because it is the only
population for which detailed data are available for
making comparisons.
Initial Conditions:
State of the Ecosystem
The sardine ecosystem will assumed to be in an
approximate equilibrium state prior to 1932, ignor-
ing random population fluctuations. The sardine
population appears to be consistently near virgin
levels for the few years that data are available
before 1932 (Fig. 3), and I speculate that the other
populations are at reasonably consistent levels as
well. There is some justification for overall stabil-
ity at the sardine-anchovy-competitor trophic level
and the predator trophic level, if not for individual
fish species or population groups (Sette 1969; Steele
1979).
Estimates of population biomasses prior to the
1932-52 collapse period were summarized by Atkin-
son (1980) from data given by Murphy (1966) and
Riffenburgh (1969). The biomasses presented below
correspond to the assumed equilibrium state at the
start of a fishing year. A fishing year is defined to
begin in the summer after the main spring spawn-
ing season of the sardine and anchovy.
sardine larvae
Pi
= 1,600 kilotons
sardine yearling
PZ
= 300 kilotons
sardine adult
Ps
= 4,000 kilotons
anchovy larvae
P*
= 400 kilotons
anchovy adult
P,
= 1,000 kilotons
competitors
le
= 3,000 kilotons
predators
Pi
= 2,000 kilotons
The initial state in 1932 is also defined by this
biomass vector, P.
Parameter Estimation for the
Sardine Ecosystem Model
First, I point out that the above model represen-
tation is not intended to be a comprehensive descrip-
tion of the sardine ecosystem or to have general ap-
plication for predicting future population dynamics,
at least not as developed here. However, it is pro-
posed as a reasonable representation to demonstrate
the similarity between simulated results and ob-
served system dynamics during the 1932-52 time
frame provided appropriate parameter estimates
can be determined. The value of the difference for-
mation in dealing with the parameter uncertainty
issue will be illustrated in the discussion below of
parameter estimation procedures.
Two model parameters in the equations of Table
1 were estimated directly from available data in the
literature (Murphy 1967; MacCall 1979; Clark and
Phillips 1932; Huppert et al. 1980): adult sardine sur-
vival, Szo = 1.40 (excludes fishing mortality ef-
fects), and adult anchovy survival, S5 = 1.20. The
driver terms in the model, d3(£) and E^t), were
also estimated from available data during the
simulation period. These terms could not, of course,
be definitized without the benefit of present hind-
sight. In a predictive situation, such terms would
generally have a large degree of uncertainty,
because projected fishing pressure is highly
speculative while larvae survival has a strong
stochastic component. Here, however, the available
data will be used to the extent possible to resolve
model terms.
Estimates of sardine fishing parameter, 63(t),
were derived from Murphy's (1966) data and are
shown plotted in Figure 5. The simplified model used
in the simulations ignores detailed yearly variations
and focuses on the major trends. A linear increase
is assumed during the period from a rate of about
0.1 in 1932 to a rate >0.4 in 1936. The fishing rate
is assumed to remain constant for the remainder of
the simulation period.
The assumed model for the sardine larvae survival
term, E^t), is presented in Figure 6 along with
Sette's (1969) data from which it was derived. These
data represent numbers of fish at age class two ver-
sus the year spawned. The survival rate model
assumes that these observed fluctuations in the data
primarily reflect random survival effects during the
first year of life. Ex{t) was obtained by normaliz-
ing Sette's data with respect to the spawning
population biomass and defining a relative scale such
that the integrated value over the 20-yr period from
1932 to 1952 was equal to one.
The remaining model parameters, which repre-
sent the great majority of those in the equations of
Table 1, could not be directly estimated to any
degree of accuracy from available literature data.
Instead, these estimates were derived from the
special nonlinear programming analysis of mine
(1980, in press) mentioned previously. I treated
these ecosystem model parameters as variables with
upper and lower bounds reflecting their uncertain-
ty ranges. The bounds established by me for the sar-
dine ecosystem parameters were typically an order
of magnitude. Implicit parameter constraints were
544
ATK1NSUN: 1-1SH i'Ui'ULAilUIN DflNAMlOS
1.0
ESTIMATED FISHING RATE
DERIVED FROM MURPHY'S (1966) DATA
FISHING RATE MODEL
1930
34
38
42
46
50
YEAR
Figure 5.— Model of sardine fishing rate, 63(t), used in the sardine ecosystem simulations.
SURVIVAL FACTOR MODEL
YEAR CLASS SURVIVAL
ESTIMATE BY SETTE (1969)
24 «
(A
Z
o
20
16
1930
34
38
42
YEAR
46
50
S
o
t
8)
<
<
W
</>
O
a.
>■
at
z
i
<
(0
Figure 6.— Model of sardine larvae survival, E^t), used in the sardine ecosystem simulations.
defined by the assumed equilibrium condition prior
to 1932-52. Setting the time-varying fishing rate at
its pre-1932 value (d3 = 0.10) and fixing the time-
varying larval survival factor at its reference value
(E1 = 1.0), a set of seven equality constraints were
specified corresponding to the seven population
equations in Table 1 with P(t + 1) = P(t) = P.
While there is still significant degrees-of -freedom
in the model (i.e., more parameters than equality
constraints), I was able to greatly resolve their
values based on my nonlinear programming pro-
cedures.
The parameters in Table 2 represent the "nom-
inal" estimates presented by me (1980) based on my
NLP analyses. In searching for minimum and max-
imum population response levels throughout
bounded parameter space, a series of intermediate
search steps were taken that produced suites of
interdependent parameter values satisfying the
pre-1932 equilibrium condition. Population response
levels were equated to the average sardine popula-
tion during the 1932-52 simulation period in this
analysis. The selected nominal parameter suite in
Table 2 gives response levels approximately midway
between the determination of minimum and max-
imum levels.
Note that the parameter values in Table 2 were
not derived from statistical procedures using the
545
FISHERY BULLETIN: VOL. 84, NO. 3
Table 2.— Estimated values of the sardine ecosystem model parameters (from Atkinson 1980).
Parameter
Nominal
Parameter
Nominal
Population
type
Symbol
value
Population
type
Symbol
value
1
Sardine larvae
Survival/growth
s,
7.26
5 Anchovy adult
Survival/growth
s5
1.30
Competition
aii
5 x
10~6
Competition
°53
2.0 x 10"5
Competition
au
2.5 x
10-6
Competition
°55
3.0 x 10-5
Predation
013
7.6 x
10-4
Competition
a56
1.0 x 10'5
Predation
015
3.8 x
10-4
Predation
057
1.0 x 10"4
Predation
016
7.6 x
10~5
Fecundity
^5
0.432
2
Sardine yearling
Survival/growth
s2
2.10
6 Competitor group
Survival/growth
s6
1.65
Competition
o22
3.7 x
10"5
Competition
a63
5.0 x 10~5
Competition
a25
1.8 x
10-5
Competition
a65
5.0 x 10-5
Predation
026
1.8 x
10"5
Competition
a66
5.0 x 10"5
3
Sardine adult
Survival/growth
$3.0
1.40
Predation
067
5.0 x 10~5
Competition
a33
1.5 x
10~5
7 Predator group
Survival/growth
s7
1.23
Competition
°35
1.0 x
10-5
Mortality
*7
0.5
Competition
a36
5.0 x
10~6
Competition
<*77
5.2 x 10~5
Predation
037
1.0 x
10-4
Prey
Y73
2.5 x 10-4
Fecundity
'3
0.468
Prey
Y75
2.5 x 10"4
4
Anchovy larvae
Survival/growth
Competition
Competition
Predation
Predation
Predation
S4
"41
Q'44
043
045
046
0.50
2.5 x
5.0 x
1.5 x
3.0 x
3.0 x
10-6
10-6
10-4
10-4
10~5
Prey
Y76
1.25 x 10"4
population data during the simulation period (Fig.
3). The estimates are uncoupled from these data and,
hence, reflect strictly a priori knowledge as would
exist in applications where predictions are required.
Furthermore, the parameter values are not pro-
posed as best estimates of these parameters, but
simply provide a consistent set of values for use in
the simulation demonstration. The nonlinear pro-
gramming approach of mine is structured in general
to bound future ecosystem response characteristics
given only a priori population data.
Ecosystem Simulations
The simulated sardine ecosystem histories are
presented and compared with estimated sardine and
anchovy population data in Figure 7. The adult sar-
dine population simulation is in reasonably good
agreement with the data of Murphy (1966) giving
the many approximations and simplifying assump-
tions used in the modeling. The major dynamic
features of the adult sardines decline are consistent,
including the sharp rebounds associated with the
favorable conditions for sardine larvae survival in
1938 and 1939 and again in 1947 (Fig. 6).
The simulated anchovy response in Figure 7,
which ignores any fluctuating larvae survival com-
ponent, appears to track the 3-yr averaged estimates
of Murphy (1966). The anchovy population increases
along with the competitor group to fill the ecological
void in this trophic level. The predator biomass
decreased slightly because the decline of the sardine
results in a less desirable food supply, at least ac-
cording to estimated input parameters. Unfortun-
ately, there are no available data for comparing with
the predicted competitor and predator group
responses.
Another simulation run was made to investigate
the speculation that fluctuating larval survival rates,
by themselves, might have caused the sardine col-
lapse. The sardine fishing rate was held at the
relatively low levels that existed before 1932 (d3 =
0.10), and the fluctuating larvae survival model in
Figure 6 was applied. The resulting simulation run
is presented in Figure 8 and shows the predicted
history of the adult sardine population, along with
that of the anchovy, competitor, and predator
groups. The adult sardine population again fluc-
tuates markedly but now remains at relatively high
levels, in no apparent danger of collapsing. It would
appear from these runs that the added fishing
pressure is necessary to explain the actual event dur-
ing this period.
CONCLUSIONS
A general set of discrete-time difference equations
have been developed for use in simulating the im-
portant dynamic processes effecting fish popula-
tions, including
• interactions between competors, predators, and
prey
• birth, growth, and aging processes within a
546
ATKINSON: FISH POPULATION DYNAMICS
4000
ESTIMATED
FROM SARDINE
DATA BY MURPHY (1966)
ESTIMATED FROM
ANCHOVY DATA
BY MURPHY (19661
1932
36
40
44
48
52
YEAR
(a) SARDINES AND ANCHOVY
8000 —
_ 6000
V)
z
o
I-
8
<
g
CQ
4000 —
2000
—
—
COMPETITOR
GROUP
I
PREDATOR
GROUP
^^^^^^^^^^
I I I
1932
36
48
52
40 44
YEAR
(b) COMPETITOR AND PREDATOR GROUPS
Figure 7.— Simulation run for assumed models of increased sar-
dine fishing rate and fluctuating sardine larvae survival rate.
single population group
• spatial and temporal variations.
The sardine subsystem within the California Cur-
rent region was modeled using the multispecies dif-
ference model and simulations computed for the
sardine's collapse period of 1932-52. Input drivers
perturbing the system included representations of
the increased sardine fishing pressure and the fluc-
tuating sardine larvae survival rates during this
period. Simulation results were shown to compare
favorably with the available population history data.
The increased fishing pressure was indicated to be
1000
ANCHOVY
1932
36
40 44
YEAR
48
52
Figure 8.— Simulation run for assumed constant pre-1932 fishing
rate but with fluctuating sardine larvae survival rate.
the fundamental cause for the sardine collapse; the
estimated yearly fluctuations in sardine larvae sur-
vival could not by themselves have caused this sud-
den event.
These simulation results demonstrate the use of
the discrete-time difference model as an efficient
simulation tool. There appear to be many applica-
tions for the model in theoretical and applied multi-
species fisheries studies.
ACKNOWLEDGMENTS
This work was based on a part of a dissertation
submitted in partial satisfaction of the requirements
for the Ph.D. degree at the University of Califor-
nia, Los Angeles. S. E. Jacobsen, chairman of the
dissertation committee, provided guidance and en-
couragement throughout these studies. D. A. Kiefer
of the Department of Biological Sciences, Univer-
sity of Southern California, reviewed early versions
of this paper and made helpful comments.
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1977. A multispecies extension to the Beverton and Holt
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Atkinson, C. A.
1980. Analysis of perturbed dynamic systems under param-
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1974. Modern control theory. Quantum Publishers, Inc.,
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1975. Marine ecology and fisheries. Cambridge Univ. Press,
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1972. Building and testing ecosystem models. In J. N. R.
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1961. Experimental ecology of the feeding of fishes. Yale
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Laevastu, T., and F. Favorite.
1978. Fluctuations in Pacific herring stock in the Eastern
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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.
Reun. Cons. int. Explor. Mer 173:212-230.
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1965. The study of population growth in organisms grouped
by stages. Biometrics. 12:1-18.
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1960. The properties of a stochastic model for the predator-
prey type of interactions between two species. Biometrika
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Levine, S. H.
1976. Competitive interactions in ecosystems. Am. Nat.
110:903-910.
MacCall, A. D.
1979. Population estimates for the waning years of the Pacific
sardine fishery. Calif. Coop. Oceanic Fish. Invest. Rep. 20,
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May, R. M.
1973. Stability and complexity in model ecosystems. Prince-
ton Univ. Press, Princeton, NJ, 265 p. (See p. 13-171.)
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R. M. Laws.
1979. Management of multispecies fisheries. Science 205:
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1983. Seasonal variation in survival of larval northern an-
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1973. A systematic approach to ecosystems analysis. J.
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Murphy, G. I.
1966. Population biology of the Pacific sardine (Sardinops
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1975. Marine trophic interactions by dynamic simulation of
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203.
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1973. Biological oceanographic processes. Pergamon Press,
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1976. Empirical multivariate autoregressive equation predic-
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1958. Handbook of computations for biological statistics of
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Riffenburgh, R. H.
1969. A stochastic model of interpopulation dynamics in
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1969. A perspective of a multi-species fishery. Calif. Coop.
Oceanic Fish. Invest. Rep. 13, p. 81-87.
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1972. The increase in spawning biomass of northern anchovy,
Engraulis mordax. Fish. Bull., U.S. 70:849-874.
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1974. Abundance of pelagic fish during the 19th and 20th cen-
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Steele, J. H.
1979. Some problems in the management of marine re-
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1978. Predation and resource partitioning in one predator-
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548
FECUNDITY OF NORTHERN SHRIMP, PANDALUS BOREALIS,
(CRUSTACEA, DECAPODA) IN AREAS OF
THE NORTHWEST ATLANTIC
D. G. Parsons and G. E. Tucker1
ABSTRACT
Fecundity of the northern shrimp, Pandal-us borealis, and relationships between number of eggs and
carapace length were determined from 15 samples taken in 9 areas of the Northwest Atlantic. The sam-
pling area extended from Davis Strait to the south coast of Newfoundland. Comparisons of samples
suggested that fecundity levels can vary between seasons, years, and areas. A relationship between egg
production and environmental temperature was not evident from available samples.
The northern or pink shrimp, Pandalus borealis, is
a protandric hermaphrodite with a circumboreal
distribution. In the Northwest Atlantic, it occurs
from about lat. 75 °N at West Greenland to about
lat. 42°N at Georges Bank (Squires 1970). Fecun-
dity of this species in the North Atlantic has been
studied in southern Norway (Rasmussen 1953),
northern Norway (Thomassen 1977), the North Sea
(Allen 1959), Iceland (Skuladottir et al. 1978), West
Greenland (Horsted and Smidt 1956), Barents Sea
(Teigsmark 1983), and Gulf of Maine (Haynes and
Wigley 1969). Bottom water temperatures recorded
at depths where shrimp samples were collected dur-
ing these studies varied considerably between areas
but were within the range of tolerance for survival
of adults as reported by Allen in 1959 (-1.68° to
11.13°C).
This paper provides information on the fecundity
of P. borealis in the Northwest Atlantic. Samples
were collected in areas of known shrimp concentra-
tion off Baffin Island, in the eastern Hudson Strait
and Labrador Sea, and off the south coast of New-
foundland. Bottom temperatures at sampling sites
also varied between these areas but were confined
to the lower half of the tolerance range (<7°C). Com-
parisons are made between selected combinations
of the data sets presented. The possible effects of
ambient temperature on fecundity levels also are
considered.
MATERIALS AND METHODS
Samples of ovigerous female shrimp were col-
lected opportunistically during various research
cruises conducted by or for the Department of
Fisheries and Oceans, St. John's, Newfoundland,
Canada, between 1971 and 1982. A total of 15
samples was selected for analysis. These were taken
from the Baffin Island area (east of Cumberland
Sound); Hudson Strait; North Labrador Sea; Hope-
dale, Cartwright, and Hawke Channels (on the
Labrador Shelf); St. Mary's Bay; Fortune Bay; and
the Southwest Newfoundland coast (Fig. 1). For
some areas, only one sample was available while for
others, samples were obtained in different months
and/or different years (Table 1).
Only animals in good condition were selected from
the trawl catches for the study (i.e., no noticeable
damage and egg mass undisturbed). Individuals
were selected over the complete size range of
females, preserved in 10% Formalin2 and returned
to the laboratory. It was assumed that within any
length group the selection (in terms of number of
eggs) was random.
Oblique carapace lengths were measured to the
nearest 0.1 mm using Vernier calipers. This
measurement is the distance between the posterior
margin of the orbit of the eye and the posterodorsal
margin of the carapace (Rasmussen 1953).
All eggs were removed from the pleopods, spread
in a Petrie dish, and oven dried overnight at 60°C.
After drying, eggs were further separated and
counted.
Accuracy of the counts was determined by re-
counting the eggs from 49 animals. Differences from
the initial counts in 48 cases varied between - 5.75%
'Fisheries Research Branch, Department of Fisheries and
Oceans, P.O. Box 5667, St. John's, Newfoundland A1C 5X1,
Canada.
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Manuscript accepted December 1985.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
549
FISHERY BULLETIN: VOL. 84, NO. 3
56° M° 52° 50°
550
PARSONS and TUCKER: FECUNDITY OF NORTHERN SHRIMP
Table 1 .—Regression equations for fecundity (F) vs. length (L) for Pandalus borealis in the Northwest Atlantic.
Temp.
Date N Regression equation r2 °C
Sample
Baffin Island
14 Aug.
1978
48
iog10
F
=
3.0955 log10
L-
-1.1417
0.75
0.7-1.8
Hudson Strait
13 Sept.
1982
24
iog10
F
=
3.8880 log10
L-
-2.3967
0.33
0.6
North Labrador Sea
22 Sept.
1982
43
iog10
F
=
3.2715 log10
L-
- 1 .4550
0.45
0.5
Hopedale Channel
28 Sept.
1978
46
iog10
F
=
2.8045 log10
L-
- 0.7202
0.70
3.0
Hopedale Channel 11
, 25 Sept.
1982
96
log10
F
=
2.8884 log10
L-
-0.8893
0.74
3.2
Cartwright Channel
20 Sept.
1978
45
iog10
F
=
3.1824 log10
L-
- 1 .3059
0.74
3.0
Cartwright Channel 11
, 26 Sept.
1982
87
login
F
=
2.5240 log10
L-
-0.3750
0.68
2.0-2.4
Hawke Channel
24 Aug.
1974
20
iog10
F
=
3.4614 log10
L-
- 1 .6670
0.70
—
Hawke Channel
30 Nov.
1974
24
iog10
F
=
1.4613 log10
L+ 1.1015
0.31
2.9
Hawke Channel
23 Sept.
1975
27
iog,0
F
=
3.0106 log10
L-
-1.0147
0.68
2.7
St. Mary's Bay
18 Mar.
1971
48
login
F
=
2.3954 log10
L-
-0.3691
0.53
—
St. Mary's Bay
28 Feb.
1974
44
iog,0
F
=
2.5290 log10
L-
-0.5476
0.47
—
Fortune Bay
17 Mar.
1978
48
login
F
=
3.0413 log10
L-
-1.1187
0.57
1.0
Fortune Bay
30 Mar.
1979
47
iog,0
F
=
2.6870 log10
L-
-0.6428
0.70
—
SW Newfoundland Coast
27 Feb.
1978
48
iog10
F
=
2.8557 log10
L-
-0.7396
0.78
6.2
and +5.65%. The difference between the total
number of eggs counted and recounted was only
- 0.22% of the initial count. A recount of eggs from
one female indicated a difference of -9.38%. It is
possible that, in this case, some of the eggs were
inadvertently lost between counts.
Parameters for the relationship between number
of eggs and carapace length for each sample were
determined by linear regression using log-log (base
10) transformation. Some data sets were compared
by analysis of covariance, assuming homoscedas-
ticity. All statistical analyses were performed using
the REG (regression) and GLM (general linear
models) procedures of SAS (Statistical Analysis
System).
It must be stressed that samples were obtained
opportunistically and not according to a predeter-
mined sampling design. Consequently, the statistical
analyses were performed based on a practical ap-
proach rather than attempting methods for which
strict sampling procedures are required. It was anti-
cipated that differences in fecundity-length relation-
ships could be due to seasonal, annual, and areal
effects. Our data only permitted simple compari-
sons, investigating each factor separately.
Bottom temperatures at most sample locations
were recorded to the nearest 0.1 °C using either
manual or expendable bathythermographs.
RESULTS
The parameters of the fecundity-carapace length
relationships for all 15 samples are given in Table
Figure 1.— Positions of stations in the northwest Atlantic where
northern shrimp fecundity samples were collected.
1. Data and the fitted line for each sample are
displayed in Figure 2. Coefficients of determination
ranged from 0.31 to 0.78 and all relationships were
significant (differences from zero slope were highly
significant). Intercepts for the log transformed data
were less than zero in all but one case. Slopes ranged
from 2.4 to 3.9 except for the sample with positive
intercept (1.5).
Only two samples were available (Hawke Chan-
nel, August and November 1974) for comparison of
fecundity between seasons. Analysis of covariance
on the log of both variables indicated a highly sig-
nificant difference in slopes (Table 2). The data
showed that larger females (>24 mm), on average,
carried more eggs in August whereas smaller
females showed higher fecundity in November (Fig.
3).
Samples from specific areas and seasons were
compared to determine similarities or differences
between years. Five simple comparisons were possi-
ble: St. Mary's Bay - March 1971 vs. February 1974,
Hawke Channel - August 1974 vs. September 1975,
Fortune Bay - March 1978 vs. March 1979, Cart-
wright Channel - September 1978 vs. September
1982, and Hopedale Channel - September 1978 vs.
September 1982.
No significant differences in either the rate of in-
crease in fecundity with increasing size (slope) or
mean number of eggs produced (intercept) were
detected between years in three of the five areas
compared (Table 2). These were St. Mary's Bay,
1971 and 1974; Hawke Channel, 1974 and 1975; and
Fortune Bay, 1978 and 1979 (Fig. 4a, b, and c,
respectively). Samples from Cartwright Channel
from September 1978 and 1982 showed a significant
difference in slopes at a = 0.05 (Fig. 4d) whereas
samples from the Hopedale Channel for the same
551
FISHERY BULLETIN: VOL. 84, NO. 3
BAFFIN ISLAND
AUG. 1978
• • .
CARTURISHT
SEPT 1878
HUDSON STRAIT
SEPT . 1 982
CARTURISHT
SEPT. 1982
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HOPEDALE
SEPT. 1978
HOPEDALE
SEPT . 1 982
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552
PARSONS and TUCKER: FECUNDITY OF NORTHERN SHRIMP
ST , MARYS BAY
MARCH I 97 \
ST. MARYS BAY
FEB. 1974
see-l
20
2500-
FORTUNE BAY
MARCH 1078
FORTUNE BAY
MARCH 1 07O
2
B
22
ZA
26
28
4000-
S.W. COAST
3000 -
FEB. 1978
•
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.
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a
•
1 000-
•
years were similar in slope but different in eleva-
tion (Fig. 4e). Average fecundity at length was
higher in 1978 than in 1982 in the latter area.
Three comparisons were possible to detect differ-
ences between areas. In 1982, four areas were
sampled during September: Hudson Strait, North
Labrador Sea, Hopedale Channel, and Cartwright
Channel. Analysis of the data indicated no differ-
ence in the rate of increase in fecundity with increas-
ing size but a highly significant difference in the
mean number of eggs produced (Table 2, Fig. 5a).
T-Tests for sample means showed that the sample
from Hudson Strait was different from those taken
off the Labrador coast (Table 3). Fecundity in the
former was less at comparable sizes.
Three areas were sampled in August and Septem-
ber 1978: east of Baffin Island (August), Hopedale
and Cartwright Channels (September). The data
from these samples also were similar in slope but
different in elevations (Table 2, Fig. 5b). T-tests
showed that the lower fecundity observed in the
Cartwright Channel was significantly different (a
= 0.05) from that observed in the other two areas
(Table 3).
Two samples were taken off the south coast of
Newfoundland early in 1978: one from the south-
west coast in February and the other from Fortune
Bay in March. Eggs in both samples were "eyed",
indicating late stage development. The data showed
that average egg production was higher off the
southwest coast over the range of sizes compared
(Fig. 5c). The statistical analysis indicated similar-
ity in slopes but a highly significant difference in
elevations (Table 2).
DISCUSSION
Loss of eggs over the ovigerous period has been
reported in previous studies on fecundity of P.
borealis (Elliot 19703; Ito 1976; Skuladottir et al.
1978; Stickney and Perkins 1979; Stickney 1981).
This loss could be incidental or due to incomplete
fertilization and/or disease. Egg diameter also in-
creases between spawning and hatching (Haynes
and Wigley 1969; Ito 1976), and some eggs that are
3Elliot, D. L. 1970. Fecundity of the northern shrimp, Pan-
dalus borealis. Unpubl. manuscr., 32 p. Bowdoin University,
Brunswick, ME 04011.
Figure 2.— Number of eggs (vertical axis) vs. carapace length in
mm (horizontal axis) for 15 samples of female northern shrimp
taken from areas of the northwest Atlantic.
553
FISHERY BULLETIN: VOL. 84, NO. 3
Table 2.— Analyses of covariance for fecundity-length relationships.
Slopes
Intercepts
Effect
Comparison
F-value
Prob.
F-value
Prob.
Season
Hawke Channel
08/74 vs.
Hawke Channel
11/74
8.19
0.0067
Year
St. Mary's Bay
St. Mary's Bay
Hawke Channel
03/71 vs.
02/74
08/74 vs.
0.06
0.8024
0.18
0.6748
Hawke Channel
09/75
0.42
0.5215
2.30
0.1367
Fortune Bay
Fortune Bay
03/78 vs.
03/79
0.52
0.4707
1.23
0.2709
Cartwright Channel
Cartwright Channel
09/78 vs.
09/82
4.27
0.0408
0.43
0.5141
Hopedale Channel
Hopedale Channel
09/78 vs.
09/82
0.07
0.7861
26.31
0.0001
Area
Hudson Strait
North Labrador Sea
09/82 vs.
09/82 vs.
Hopedale Channel
Cartwright Channel
09/82 vs.
09/82
1.78
0.1490
10.69
0.0001
Baffin Island
08/78 vs.
Hopedale Channel
Cartwright Channel
09/78 vs.
09/78
0.49
0.6140
8.51
0.0003
SW Newfoundland Coast 02/78 vs.
Fortune Bay
03/78
0.17
0.6792
61.32
0.0001
2888-
AUGUST.1974
NOVEMBER, 1974
22
23
24
25
LENGTH CMM5
28
Figure 3.— Comparisons of northern shrimp fecundity between
seasons for the Hawke Channel, based on predicted values from
equations in Table 1.
close to the periphery and loosely attached may be
simply "crowded out".
The evidence of egg loss described in previous
studies is sufficient to suggest that combining data
from different times of year is not appropriate. The
two samples compared in this study produced incon-
clusive results in that average fecunity was not con-
sistently lower over the complete size range in
November compared with the August sample.
Annual variation in fecundity-length relationships
occurred in two of five areas sampled in different
years. The rate of increase in number of eggs with
Table 3. — Paired comparisons for area differences when k (no.
of samples) >2.
P values for H0: Mean, = meany
Date/sample
No.
September 1982
Hudson Strait 1
North Labrador Sea 2
Hopedale Channel 3
Cartwright Channel 4
August 1978
Baffin Island 1
Hopedale Channel 2
Cartwright Channel 3
0.0002
0.0001
0.0001
0.5709
0.0121
0.2141
0.0695
0.0002
0.4525
increasing size only differed significantly in one case,
however. The reasons why fecundity differs between
years are not known but could be related to changes
in environmental conditions and/or egg disease
(Stickney 1981). In support of the latter, it is noted
that the proportion of nonviable eggs in the 1982
Hopedale Channel sample was higher than in the
1978 sample by an order of magnitude (D. G. Par-
sons unpubl. data). Fecundity was significantly
higher in the 1978 data.
Teigsmark (1983) found that variation within a
population during successive years is as great as the
variation between populations in a single year and
was unable to make a conclusive statement about
fecundity of different populations of P. borealis in
the Barents Sea. He speculated that such differences
could be related to availability of food and popula-
tion density.
554
PARSONS and TUCKER: FECUNDITY OF NORTHERN SHRIMP
•T. MARYS BAY. 1974
ST. MARYS BAY. 1971
CARTVRXSHT CHANNEL. 1979-
-CARTWRIBMT CHANNEL. I 902
01
i »
3
CHANNEL. 1992
FORTUNE BAY. 1979-
FORTUNE BAY. I 979
Carapace length (mm)
Figure 4.— Comparisons of northern shrimp fecundity be-
tween years from five different areas, based on predicted
values from equations in Table 1.
Carapace length (mm)
Based on the comparison of samples taken in 1982,
it was shown that the fecunity-length relationships
in three areas off Labrador were similar. Similar-
ity was not apparent in 1978 samples which showed
that fecundity in the Cartwright Channel was lower
than in the Hopedale Channel. This discrepancy in
results from Labrador is due to annual differences
demonstrated for both channels in 1978 and 1982
samples.
The comparison by area for the 1978 data also
implied similarity between the Baffin Island and
Hopedale Channel samples. However, the size
ranges compared were not the same. Female shrimp
ranged in size from 23.7 to 34.5 for the Baffin Island
sample in contrast to 21.7 to 29.0 for the Hopedale
Channel sample. These differences in size likely
reflect separate rates of growth and maturity in the
two areas. Therefore, from a biological viewpoint,
all three areas sampled in 1978 exhibited different
fecundity-length relationships.
The differences between areas, described above,
can be considered in relation to the temperatures
present in these areas. The bottom temperature at
the sampling station off the southwest coast of New-
foundland was 6.2°C, the warmest of all areas
sampled (Table 1). The temperature recorded in
555
FISHERY BULLETIN: VOL. 84, NO. 3
INZ
NORTH LABRADOR SEA-
HUDSON STRAIT
CARTWBIBMT
" HOPEDALE CHANNEL
.Q
4sae-
b
I97« yf
3sae-
BAFfTN ISLANO-^^
zeae-
^^•"^-"^CARTWRIOHT CHANNEL
isee-
•*}PEDALE CHANNEL— ^55^
eea-
NCWTOUNDLAND
33 35
Carapace length (mm)
Figure 5.— Comparisons of northern shrimp fecundity between areas in 1982 and 1978, based on predicted values from equations in
Table 1.
March 1978 in Fortune Bay was 1.0°C, one of the
coldest areas. According to Squires (1968), the
penetration of Atlantic water into the former area
accounts for these warmer temperatures which per-
sist throughout the year. In Fortune Bay, however,
the deep bottom water is of mixed Atlantic and Arc-
tic origin resulting in much colder temperatures.
Thus, the lower fecundity in the Fortune Bay sam-
ple is likely linked with an overall reduction in pro-
ductivity in a cold water environment. Reduced
productivity has been observed previously in the cold
water habitats of le Fjord du Saguenay, Quebec
(Couture 1971) and the Barents Sea (Berenboim
1982).
The sample taken east of Baffin Island showed
relatively high fecundity in cold water (0.7°-1.8°C)
compared with other cold water areas. Also, average
size of females was larger than encountered else-
where with largest females carrying clutches in ex-
cess of 4,300 eggs. This is similar to a situation in
the Sea of Japan where female shrimp carried
similar numbers of eggs as those (at comparable
lengths) off Labrador. Again, greater sizes were
attained and egg counts as high as 4,900 were en-
countered (Ito 1976). Growth and maturation are
delayed in colder water (Allen 1959; Rasmussen
1969; Butler 1971) and shrimp in these two cold
water environments likely live longer than conspe-
cifics on the Labrador Shelf.
Dupouy et al. (1981) concluded that shrimp off
Baffin Island spawned intermittently based on the
high proportion of nonspawning females observed
during a survey in 1979. If all females do not spawn
annually, more time is available for growth. (Oviger-
ous females do not molt.) This can account for the
larger sizes attained in the colder area. Failure to
spawn annually reduces reproductive potential but
is compensated to some degree by the large sizes
females attain (larger females carry more eggs) and
the apparently increased longevity.
Samples taken in 1982 in the Hudson Strait and
North Labrador Sea came from waters of 0.6° and
0.5°C, respectively, but only data from the former
were significantly different (a = 0.05) from samples
taken in the warmer Hopedale and Cartwright
Channels. Data from Haynes and Wigley (1969)
showed higher fecundity in warmer water (~5°C)
of the Gulf of Maine where a 28 mm female can pro-
556
PARSONS and TUCKER: FECUNDITY OF NORTHERN SHRIMP
duce around 2,800 eggs compared with 1,900-2,000
in the Cartwright Channel (2°-3°C). In the Gulf of
St. Lawrence, temperatures were similar to those
in the Gulf of Maine but fecundity in 1970 (E. J.
Sandeman4 unpubl. data) was comparable with
levels observed in the colder Labrador channels.
Allen (1959) reported smaller shrimp and fewer eggs
for P. borealis in the North Sea (~9°C) compared
with the colder area off Southern Norway (7°C).
CONCLUSIONS
Fecundity of Pandalus borealis in the areas of the
Northwest Atlantic considered in this study was
generally lower than observed previously in the Gulf
of Maine (Haynes and Wigley 1969) and off South-
ern Norway (Rasmussen 1953). Fecundity can vary
seasonally, annually, and between areas, making
conclusions based on such data difficult. Skuladot-
tir et al. (1978) concluded that fecundity does not
seem to be a useful characteristic for distinguishing
between populations unless it is certain that no egg
loss or hatching has taken place. The results of the
present study concur with these findings and those
of Teigsmark (1983) which also showed that annual
variation within areas also must be considered.
In some comparisons between areas, there ap-
pears to be reduced egg production in areas with
low environmental temperature. In others, this is
not at all apparent, especially at extremely cold and
warm temperatures. Thus, there is no clear relation-
ship between fecundity and environmental temper-
ature, especially at the extremes of the range of
temperature tolerance.
Squires (1968) described warm water areas as
areas of high reproductive potential for shrimp and
colder regions as areas of low reproductive poten-
tial. The cold water bays of Newfoundland and the
eastern Hudson Strait fit into the latter category
in terms of shrimp fecundity. Other cold water con-
centrations of shrimp appear to be better adapted
such as those off Baffin Island, in the North Lab-
rador Sea and Sea of Japan. In these cases, en-
vironmental conditions other than temperature
(e.g., availability of nutrients) may be more impor-
tant.
ACKNOWLEDGMENTS
We are grateful to the many technicians and
4E. J. Sandeman, Fisheries Research Branch, Department of
Fisheries and Oceans, P.O. Box 5667, St. John's, Newfoundland
A1C 5X1, Canada.
casual employees who assisted in collecting the data
over the years and performed the laborious task of
counting the eggs. In this regard, the services of
W. Edison are particularly appreciated. Assistance
in the statistical analyses was provided by D.
Stansbury.
LITERATURE CITED
Allen, J. A.
1959. On the biology of Pandalus borealis Kr^yer, with
reference to a population off the Northumberland coast.
J. Mar. Biol. Assoc. U.K. 38:189-220.
Berenboim, B. I.
1982. Reproduction of the shrimp Pandalus borealis popula-
tions in the Barents Sea. Okeanologiya 22(1):118-124.
Butler, T. H.
1971. A review of the biology of the pink shrimp, Pandalus
borealis Krtfyer 1838. Can. Fish. Rep. 17:17-24.
Couture, R.
1970. Reproduction de Pandalus borealis Krtfyer (Crustacea,
Decapoda) dans le fjord du Saguenay. Nat. Can. 97:825-
826.
Dupouy, H., C. Leroy, and J. Frechette.
1981. Etude des Stocks de Crevette Pandalus borealis du
Detroit de Davis. Sci. Peche, Bull. Inst. Peches Marit. 311,
mars 1981, 21 p.
Haynes, E. B., and A. L. Wigley.
1969. Biology of the northern shrimp Pandalus borealis in
the Gulf of Maine. Trans. Am. Fish. Soc. 98:60-76.
Horsted, Sv. Aa., and E. Smidt.
1956. The deep sea prawn (Pandalus borealis Kr.) in Green-
land waters. Meddelelser fra Danmarks Fiskeri-og Havun-
ders^gelser. Ny Serie, Bind I, Nr. 11, 118 p.
Ito, H.
1976. Some findings concerning Pandalus borealis Kr^yer
originating in the Sea of Japan. Bull. Jpn. Sea Reg. Fish.
Res. Lab. 27, p. 75-89.
Rasmussen, B.
1953. On the geographical variation in growth and sexual
development of the deep sea prawn (Pandalus borealis Kr.).
Norweg. Fish. Mar. Invest. Rep. 10(3):1-160.
1969. Variations in protandric hermaphroditism of Pandalus
borealis. FAO Fish. Rep. 57:1101-1106.
Skuladottir, U., E. Jonsson, and I. Hallgrimsson.
1978. Testing for heterogeneity of Pandalus borealis popula-
tions at Iceland. ICES CM. Doc. 1978/K:27, 41 p.
Squires, H. J.
1968. Relation of temperature to growth and self-propogation
of Pandalus borealis in Newfoundland. FAO Fish. Rep.
57:243-250.
1970. Decapod crustaceans of Newfoundland, Labrador and
the Eastern Canadian Arctic. Fish. Res. Board Can.,
Manuscr. Rep. Ser. No. 810, 212 p.
Stickney, A. P.
1981. Laboratory studies on the development and survival
of Pandalus borealis eggs in the Gulf of Maine. In T. Frady
(editor), Proceedings of the International Pandalid Shrimp
Symposium, Kodiak, Alaska, 1979, p. 395-406. Sea Grant
Rep. 81-3.
Stickney, A. P., and H. C. Perkins.
1979. Environmental physiology of northern shrimp, Pan-
dalus borealis. Completion Report. Maine Dep. Mar. Res.,
Proj. 3-277-R, 66 p.
557
FISHERY BULLETIN: VOL. 84, NO. 3
Teigsmark, G. Thomassen, T.
1983. Populations of the deep-sea shrimp (Pandalus borealis 1977. Comparisons of growth, fecundity and mortality be-
Kr^yer) in the Barents Sea. Fiskeridir. Skr. Serv. Havun- tween two populations of Pandalus, borealis in Northern Nor-
ders. 17:377-430. way. ICES CM. Doc. 1977/K:38, 16 p.
558
INCIDENTAL DOLPHIN MORTALITY IN THE EASTERN TROPICAL
PACIFIC TUNA FISHERY, 1973 THROUGH 1978
Bruce E. Wahlen1
ABSTRACT
Since the late 1950's, large numbers of dolphins have been killed incidentally in the yellowfin tuna purse
seine fishery in the eastern tropical Pacific. Estimates of numbers of dolphins killed incidentally in this
fishery from 1973 through 1978 were made previously using a stratified ratio estimator. Previous
estimates were revised by reducing the number of strata and incorporating revisions in the data. Revised
estimates of total mortality, which are consistently more precise than previous estimates, declined from
about 100,000 dolphins per year from 1973 through 1976 to about 25,000 and 15,000 during 1977 and
1978. The decline in estimated mortality between 1976 and 1977 was primarily the result of a decline
in the kill rate which coincided with a significant management action in late 1976. Other examples dur-
ing the 1964 through 1982 period of such a temporal correspondence between a change in the number
or distribution of dolphins killed and legal or management actions are discussed.
Since the late 1950's, tuna purse seine fishermen
operating in the eastern tropical Pacific Ocean
(ETP) have exploited several dolphin species— pri-
marily spotted dolphins, Stenella attenuata, and
spinner dolphins, S. longirostris, and also striped
dolphins, 5. coeruleoalba, and common dolphins,
Delphinus delphis— to locate and catch yellowfin
tuna, Thunnus albacares. Perrin (1969) described
the process of deploying, or setting, the net around
the tuna and dolphins, and then releasing the
dolphins while retaining the tuna. During this pro-
cess, however, large numbers of dolphins have been
killed incidentally by becoming entangled in the
purse seines (Smith 1983).
The U.S. Marine Mammal Protection Act of 1972
mandated the Secretary of Commerce to make
periodic assessments of the condition of dolphin
populations involved in this ETP fishery. As a result
of a 1976 ruling by a U.S. District Court regarding
regulations promulgated under the Act, the Federal
Government established annual dolphin mortality
limits for the U.S. registered fleet (Fox 1978). Esti-
mates of annual dolphin mortality have been an in-
tegral component of periodic assessments (Smith
1983).
Estimates of cumulative dolphin mortality made
throughout the year are used to monitor mortalities
relative to the annual limits (Lo et al. 1982). When
a particular limit is reached, regulations prohibit
U.S. registered vessels from fishing on the affected
populations for the remainder of the year. In Octo-
ber 1976, the National Marine Fisheries Service
(NMFS) issued a prohibition notice for the first time
(Federal Register 1976), but because of litigation the
notice did not become effective until November
1976.
In recent years, researchers have published sev-
eral estimates and revisions of estimates of dolphin
mortality incidental to this fishery. For the period
1959-78, estimates have been made by Smith
(19792), Lo et al. (1982), Smith (1983), and Lo and
Smith (1986); for the years 1979-83, see Allen and
Goldsmith (1981, 1982), Lo et al. (1982), Hammond
and Tsai (1983), Hammond (1984), and Hammond
and Hall (1985).
Lo et al. (1982) suggested that previous estimates
of dolphin mortality incidental to this fishery were
based on a stratification scheme with an unneces-
sarily large number of strata. In this paper, I revise
the 1973-78 estimates for U.S. registered purse
seiners by reducing the number of strata and by in-
corporating revisions in the data.
DATA
Sample data were obtained from recorded obser-
vations of scientific observers who had been placed
by the NMFS aboard selected U.S. registered tuna
purse seine vessels fishing in the ETP. Data re-
corded by these observers included the type, date,
'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, P.O. Box 271, La Jolla, CA 92038.
Manuscript accepted September 1985.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
2Smith, T. D. (editor). 1979. Report of the status of porpoise
stocks workshop, La Jolla, Calif., 27-31 August 1979. Southwest
Fish. Cent. La Jolla Lab., Natl. Mar. Fish. Serv., NOAA, Admin.
Rep. LJ-79-41, 120 p.
559
FISHERY BULLETIN: VOL. 84, NO. 3
location, and estimated tuna catch of each set, and
other information describing the fishing operation.
For sets involving dolphins (dolphin sets), the ob-
servers collected additional data, including the
number of dolphins killed by species.
In 1973, all sampled trips were arranged with
vessel captains under a voluntary sampling pro-
gram. Beginning in 1974, trips to be sampled were
determined from a randomly ordered list of vessels.
Which trips were actually sampled during 1974 and
1975 depended on several factors, including the
cooperation of the captains. Because of uncertain-
ties about the cooperation of the captains and the
number of fishing trips that would be made in a year,
observers were placed on vessels as soon as possi-
ble. Thus, before 1976, the planned number of sam-
pled trips was frequently obtained in the first half
of the year. The sampling process became more ran-
dom starting in 1976, when participation in the
sampling program became mandatory for captains
making sets on dolphins.
I extracted independent information for the
population of all fishing trips by U.S. registered tuna
purse seiners in the ETP from the Inter- American
Tropical Tuna Commission (IATTC) logbook data
base. This data base contains abstracts of vessels'
logbooks obtained by IATTC personnel. An in-
dividual entry in the logbook data base provides
information about one or more sets, including num-
ber of sets, set type, date and location, estimated
tuna catch by species, but not numbers of dolphins
killed.
The logbook data are incomplete in that number
of sets may be missing, set type may not be re-
corded, and information for some sets of a trip and
for all sets of some trips may be omitted (Punsly
1983). To compensate for these omissions from the
logbook data, Punsly (1983) estimated the total
number of dolphin sets made by all U.S. and
non-U. S. seiners in the ETP. He then modified this
procedure to estimate the total number of dolphin
sets made by U.S. seiners only (Table 1).
METHODS
I stratified the data to allow for potential differ-
ences in dolphin kills. If kills do indeed differ among
strata, then a stratified estimator may be superior
to an unstratified estimator in two respects. First,
a stratified estimator will have a smaller standard
error and thus be more precise. Second, if the sam-
ple data are unrepresentative of the population with
respect to these strata, a stratified estimator will
be less biased.
Therefore, estimates of incidental dolphin mortal-
ity by species or species grouping were computed
using a stratified kill-per-set ratio estimator, follow-
ing the general approach described by Lo et al.
(1982). I excluded trips which made no dolphin sets
and experimental-gear trips from the sample and
the population. However, I added dolphin kills in-
cidental to the experimental-gear trips as constants
to the mortality estimates.
I stratified the dolphin set data by four factors
used in previously published estimates: 1) year of
the set, 2) fish-carrying capacity of the vessel, or
simply vessel capacity, 3) period within year of the
set, and 4) geographic location of the set. Vessel
capacity was divided into two categories— small and
large. The breakpoint between categories was deter-
mined by examining the cumulative distribution of
sampled trips by capacity. Periods were defined to
be quarters of the year, considering the results of
Wahlen and Smith (1985). The ETP was divided in-
to three geographic areas— North Inside, North Out-
side, and South (Fig. 1)— because mean kill (per set)
after 1978 has been shown to differ among these
areas.3
In previous estimates, the amount of tuna caught
in the set was included as a stratification factor.
However, Hammond and Tsai (1983) found that
stratification by this factor made very little differ-
ence in their estimates. For that reason and to avoid
possible overstratifi cation, I omitted amount of tuna
caught as a stratification factor.
I pooled dolphin set data over strata when it was
determined that between- strata differences in mean
kill were not statistically significant or that sample
sizes were otherwise too small. I prorated the esti-
mated numbers of dolphin sets made by U.S. seiners
(Table 1) among the pooled strata according to pro-
3K. -T. Tsai, Inter-American Tropical Tuna Commission, c/o
Scripps Institute of Oceanography, La Jolla, CA 92093, pers. com-
mun. December 1983.
Table 1.— Estimated number of dolphin sets
made by U.S. purse seiners fishing in the
eastern tropical Pacific, by year.1
Year
Number of dolphin sets
1973
1974
1975
1976
1977
1978
8,341
7,475
7,902
7,126
7,239
4,214
'Peterson, C. L. (editor). 1984. The quarterly
report October-December 1983 of the Inter-American
Tropical Tuna Commission. Inter-Am. Trop. Tuna
Comm., c/o Scripps Inst. Oceanogr., La Jolla, CA
92093.
560
WAHLEW: INCIDENTAL UUL^HIIN MUKiALlTK
40°N
20c -
20e
40"S
1
Si
o
to
CM
r '
' ir7 ' "
NORTH
20°
N.
\-V7
OUTSIDE
5
o
o
0*
5eN.
northVI^)
INSIDE ^^ny^^'
Si (j
o V
i
SOUTH ^ -
i i i \
160»W
140*
120c
100'
80«
Figure 1.— 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.
portions of known dolphin sets which were cal-
culated from logbook data.
I tested for significant between-strata differences
in mean total kill using analysis of variance (ANOVA)
methods of BMDP programs P7D and P2V (Dixon
1983). Violation of the ANOVA assumption of equal
cell variances may seriously distort significance
probabilities in unbalanced models such as in this
study (Glass et al. 1972). Because such distortion
could be great, test results were considered to be
inconclusive when significance probabilities were
close to 0.05.
I was unable to test for the combined effect of all
four stratification factors using the whole data set
because data were sparse or unavailable in many of
the 144 cells of the proposed four-factor stratifica-
tion. Thus, ANOVA results for restricted subsets of
the data containing adequate sample sizes were
assumed to hold for subsets with inadequate sam-
ple sizes. To eliminate significant between-factor
interactions, I tried logarithmic and power trans-
formations of the dependent variable, total number
of dolphins killed. When these transformations failed
to eliminate the interactions, I partitioned the
analysis into individual levels of the interacting
variables.
When it was necessary to determine where the
within-factor differences occurred, £-tests for differ-
ences between all pairs of cell means were made.
Since I tested for differences between all pairs
rather than between a few preselected pairs, a dif-
ference was considered significant if its significance
probability was less than the quotient of 0.05 and
the number of pairs. This Bonferroni adjustment to
the significance level of each test assured a level of
0.05 simultaneously across all tests (Snedecor and
Cochran 1980).
I computed lvalues for pairwise differences using
separate rather than pooled variance estimates
because the cell variances were unequal according
to Levene's test; this test was selected because it
is more robust under nonnormality than either the
common F-ratio or Bartlett's test (Brown and For-
sythe 1974). Degrees of freedom were calculated
with Satterthwaite's approximation, so that sig-
nificance probabilities could be obtained from an
ordinary ^-distribution (Snedecor and Cochran
1980). '
561
FISHERY BULLETIN: VOL. 84, NO. 3
RESULTS
Table 2.— Cumulative distributions of number of sampled U.S.
purse seine trips, by vessel capacity (tons) for the years 1973-78,
with relative frequencies (percents) in parentheses.
Vessel
Year
capacity
(tons)
1973
1974
1975
1976
1977
1978
<200
0
0
0
0
0
0
(0)
(0)
(0)
(0)
(0)
(0)
<300
0
1
1
0
0
0
(0)
(3)
(3)
(0)
(0)
(0)
<400
1
3
2
3
0
0
(4)
(8)
(7)
(7)
(0)
(0)
<600
5
9
5
11
15
8
(22)
(24)
(17)
(24)
(15)
(8)
<800
15
15
8
20
34
27
(65)
(41)
(28)
(43)
(35)
(26)
<1,000
16
20
16
24
39
33
(70)
(54)
(55)
(52)
(40)
(32)
<1,200
20
30
26
34
70
67
(87)
(81)
(90)
(74)
(71)
(66)
Total
23
37
29
46
98
102
(100)
(100)
(100)
(100)
(100)
(100)
Setting the breakpoint between small and large
vessel capacities at 600 tons (or lower) or at 1,200
tons would, in each case, create small and large
vessel categories with severely unbalanced sample
sizes (Table 2). The percent of sampled vessels with
capacity < 1,000 tons was more stable over years
than the percent of sampled vessels <800 tons,
especially from 1973 through 1976. Therefore, the
breakpoint between vessel categories was set at
1,000 tons.
Because of data sparseness, particularly in the
North Outside and South areas (Table 3), I made
three multiway ANOVA tests restricted to subsets
of the whole data set: 1) two-way test of year and
vessel capacity, restricted to the North Inside area
and the second quarter, 2) three-way test of year,
quarter, and vessel capacity, restricted to the North
Inside area and the first two quarters during 1973
through 1976, and 3) four-way test, restricted to the
North Inside and North Outside areas, and the
Table 3.— Number of dolphin sets made during sampled trips, by year, vessel capacity (tons), quarter of the year, and area.
Vessel
capacity
(tons)
Quarter
Area
Total
Year
Vessel
capacity
(tons)
Quarter
Area
Year
North
Inside
North
Outside
South
North
Inside
North
Outside
South
Total
1973
<1,000
1
2
3
4
325
167
0
0
0
47
0
0
9
0
0
0
334
214
0
0
1976
<1,000
1
2
3
4
155
41
18
20
0
27
71
13
0
0
0
4
155
68
89
37
Total
492
47
9
548
Total
234
111
4
349
>1,000
1
2
3
4
116
43
0
0
0
2
0
0
5
0
0
0
121
45
0
0
>1,000
1
2
3
4
129
42
17
16
0
0
80
6
118
0
1
0
247
42
98
22
Total
159
2
5
166
Total
204
86
119
409
1974
<1,000
1
2
3
4
459
88
0
0
0
0
6
0
0
0
0
0
459
88
6
0
1977
<1,000
1
2
3
4
3
239
433
53
0
67
134
0
1
0
0
0
4
306
567
53
Total
547
6
0
553
Total
728
201
1
930
£1,000
1
2
3
4
362
57
31
0
0
0
12
0
0
0
0
0
362
57
43
0
5*1,000
1
2
3
4
0
563
1,034
356
0
86
218
30
2
16
23
31
2
665
1,275
417
Total
450
12
0
462
Total
1,953
334
72
2,359
1975
<1,000
1
2
3
4
404
106
0
0
0
0
0
0
3
4
0
0
407
110
0
0
1978
< 1,000
1
2
3
4
170
75
86
59
0
50
138
6
13
0
0
0
183
125
224
65
Total
510
0
7
517
Total
390
194
13
597
>1,000
1
2
3
4
268
111
47
0
0
0
0
0
0
5
0
0
268
116
47
0
> 1,000
1
2
3
4
320
117
104
165
0
77
255
8
52
1
2
15
372
195
361
188
Total
426
0
5
431
Total
Total
706
6,799
340
1,333
70
305
1,116
8,437
562
WAHLEN: INCIDENTAL DOLPHIN MORTALITY
second and third quarters during 1977 and 1978.
Additionally, pairwise i-tests were made to isolate
annual and quarter differences detected by the
above tests.
Tests for Year Differences
Sample statistics of mean kill by year and vessel
capacity (Test 1) revealed an unbalanced design and
suggested that cell variances were related to cell
means (Table 4). For each of several transformations
of total kill, neither the interaction between vessel
capacity and year nor the difference between vessel
capacities was significant, but the difference among
years was significant.
To determine where the yearly differences oc-
curred, the data were pooled over vessel capacity
so that t-tests for differences between each pair of
yearly means could be made. The resulting one-way
classification by year was unbalanced and charac-
terized by significantly different cell variances (P
< 0.001), and suggested that the means from 1973
Table 4.— Mean of total number of dolphins killed (k), standard
deviation (s), and number of dolphin sets (d) for sampled trips, by
year and vessel capacity (tons) for all sets made in the North In-
side area during quarter two. Significance probabilities (P) obtained
for 2-way ANOVA's on transformed values of total kill: interaction
(P > 0.1 180), year (P < 0.001), and vessel capacity (P > 0.7851).
Vessel
Year
(tons)
tistic
1973
1974
1975
1976
1977
1978
<1,000
k
8.62
6.20
16.33
8.58
3.08
2.35
s
18.84
10.94
40.73
20.08
11.64
7.34
d
167
88
106
41
239
75
>1,000
k
11.49
5.25
8.79
14.57
2.53
1.18
s
25.96
14.08
17.43
32.44
7.84
3.31
d
43
57
111
42
563
117
Pooled
k
9.21
5.83
12.47
11.61
2.69
1.64
s
20.46
12.23
31.23
27.05
9.13
5.28
d
210
145
217
83
802
192
Table 5.— Matrix of significance probabilities
associated with f-tests for differences between pairs of
annual means of total number of dolphins killed. Signifi-
cant values, required by the Bonferroni adjustment to
be <0.0033, are indicated by "*", and nearly signifi-
cant values are indicated by " + ". Data are from sam-
pled dolphin sets made during quarter two in the North
Inside area.
Year
Year 1974 1975 1976
1977
1978
1973
0.0526 0.2007 0.4659
0.0000*
0.0000*
1974
0.0050 0.0681
0.0037 +
0.0002*
1975
0.8139
0.0000*
0.0000*
1976
0.0037 +
0.0013*
1977
0.0344
through 1976 were larger than the means from 1977
and 1978 (Table 4).
Results from pairwise i-tests indicated that means
were not significantly different within each of the
two periods from 1973 through 1976 and from 1977
through 1978 (Table 5). However, each of the means
from 1973 through 1976 was significantly different
(or nearly so) from each of the means from 1977 and
1978 (Table 5). Based on these results, I divided the
data into two periods, 1973 through 1976 and 1977
through 1978, for further tests within each period.
Tests for Differences Within
the 1973-76 Period
The three-way ANOVA table by year, quarter, and
vessel capacity (Test 2) was unbalanced and sug-
gested that cell variances were unequal (Table 6).
Furthermore, no between-f actor interactions were
significant. The test for year differences was incon-
clusive; however, there is evidence for a year effect
within only one cell (1976, quarter 1, small vessels),
and there is no consistent yearly pattern of means
within rows of the table. Therefore, I concluded that
annual means during 1973-76 were not significant-
ly different and, hence, I pooled over years within
this period. I also pooled over vessel capacity since
it was not a significant effect during these years.
Before 1976, sample data were unrepresentative
of quarter and area, since nearly all data were ob-
tained from trips made during the first half of the
year and, thus, within the North Inside area. Data
sparseness in the North Outside and South areas,
Table 6.— Mean of total number of dolphins killed (k), standard
deviation (s), and number of dolphin sets (d) for sampled trips, by
year, quarter, and vessel capacity (tons) for all sets made in the
North Inside area during the first two quarters of 1973-76. Signifi-
cance probabilities (P) obtained for a 3-way ANOVA on total kill:
interactions (P> 0.1374), year (P = 0.0534), quarter (P = 0.0501),
and vessel capacity (P = 0.8219).
Vessel
capacity
(tons)
Year
<1,000
>1,000
itistic
1973
1974
1975
1976
k
23.15
14.10
16.45
3.47
s
69.70
40.39
47.31
8.12
d
325
459
404
155
k
8.62
6.20
16.33
8.59
s
18.84
10.94
40.73
20.08
d
167
88
106
41
k
15.75
11.23
15.45
10.86
s
27.64
24.85
34.37
24.35
d
116
362
268
129
k
11.49
5.25
8.79
14.57
s
25.95
14.08
17.43
32.44
d
43
57
111
42
563
FISHERY BULLETIN: VOL. 84, NO. 3
resulting from the unrepresentative areal sample,
precluded testing for an area effect during the
1973-76 period (Table 3); however, after 1978 mean
kills were shown to differ among the three areas,
as noted earlier. Therefore, to minimize the amount
of bias which might be introduced into the estimates
from a sample which was unrepresentative of area,
I retained the three-area stratification.
Small sample sizes during 1973-76 dictated pool-
ing over all quarters within both the North Outside
and South areas and over quarters 3 and 4 within
the North Inside area (Table 3). The test result for
quarter 1 and 2 differences in the North Inside area
was inconclusive (Table 6). Based on bias considera-
tions similar to those above, I did not pool data from
quarters 1 and 2 in the North Inside area in case
their means did indeed differ.
After pooling over year, vessel capacity, and
quarter as indicated above, five strata remained for
the 1973-76 data: 1) North Inside, quarter 1, 2)
North Inside, quarter 2, 3) North Inside, quarters
3 and 4 pooled, 4) North Outside, all quarters
pooled, and 5) South, all quarters pooled.
Tests for Differences Within
the 1977-78 Period
Interpretation of the four-way ANOVA (Test 3),
restricted by data sparseness to the North Inside
and North Outside areas during the second and third
quarters of 1977-78 (Table 3), was complicated by
significant interaction between quarters and each
of the other three factors (P < 0.0159, for total kill
and all transformations of total kill). Therefore, the
four-way table was partitioned into two, three-way
tables, one for each level of quarter (Tables 7, 8),
and decisions about between-strata differences dur-
ing these years were based on results obtained
separately for each quarter.
For second quarter data, interactions were not
significant (Table 7). However, for third quarter
data, interaction between year and vessel capacity
was significant (P < 0.001) primarily because of the
two large means recorded in the North Inside and
North Outside areas by small vessels during 1978
(Table 8). Omitting the data from one extraordi-
narily large kill set in each of these two cells reduces
their means from 11.27 to 4.68 for the North Inside
and from 9.77 to 5.46 for the North Outside.
Results from the second and third quarter data
were inconsistent for both year and vessel capacity.
Neither effect was significant during the second
quarter (Table 7), but during the third quarter (Table
8) the large means in the two cells noted above pro-
vided some evidence of both a year and vessel
capacity effect. Since the evidence for both a year
and vessel capacity effect was confined to two, third
quarter cells whose means were each strongly in-
fluenced by only one set, I concluded that year and
vessel capacity were not significant effects during
1977-78. Hence, I pooled over year and vessel
capacity within this period. The evidence regarding
an area effect during 1977-78 was also inconsistent
between quarters (Tables 7, 8); however, I retained
area as a stratification factor since it was shown to
be significant after 1978.
Beginning in 1976 when the sampling program
became mandatory the sample data became more
representative of quarter. Thus, for the 1977-78
data, bias considerations were of lesser importance
Table 7. — Mean of total number of dolphins killed (k), standard
deviation (s), and number of dolphin sets (d) for sampled trips, by
area, vessel capacity (tons), and year for all sets made in the North
Inside and North Outside areas during quarter two of 1977-78.
Significance probabilities (P) obtained for a 3-way ANOVA on total
kill: interactions (P > 0.2095), area (P = 0.0060), vessel capacity
(P = 0.8857), and year (P = 0.6050).
Vessel
capacity
(tons)
Statistic
Area
Year
North Inside
North Outside
1977
<1,000
k
3.08
2.94
s
11.64
8.68
d
239
67
>1,000
k
2.53
5.66
s
7.84
13.82
d
563
86
1978
<1,000
k
2.35
4.82
s
7.34
16.00
d
75
50
> 1,000
k
1.18
4.26
s
3.31
21.19
d
117
77
Table 8.— Mean of total number of dolphins killed (k), standard
deviation (s), and number of dolphin sets (d) for sampled trips, by
area, vessel capacity (tons), and year for all sets made in the North
Inside and North Outside areas during quarter three of 1977-78.
Vessel
capacity
(tons)
Statistic
Area
Year
North Inside
North Outside
1977
<1,000
k
2.08
2.33
s
5.72
7.92
d
433
134
>1,000
k
2.85
2.89
s
9.81
6.45
d
1034
218
1978
<1,000
k
11.27
9.77
s
61.74
52.52
d
86
138
>1,000
k
2.00
2.81
s
4.34
10.97
d
104
255
564
WAHLEN: INCIDENTAL DOLPHIN MORTALITY
in stratification decisions than for the 1973-76 data.
The four- way test on 1977-78 data (Test 3) was not
helpful in resolving the question of quarter differ-
ences because of the interactions between quarter
and each of the other three factors. However, pair-
wise t-tests for differences between quarterly means
in the North Inside area during 1977-78, pooled over
Table 9.— Matrix of significance pro-
babilities associated with f-tests for dif-
ferences between pairs of quarterly
means of total number of dolphins
killed. No significant values, required by
the Bonferroni adjustment to be
<0.0083, were attained. Data are from
sampled dolphin sets made in the North
Inside area from 1977 through 1978.
Quarter
Quarter
2
3
4
1
2
3
0.7062
0.2417
0.2623
0.0684
0.0730
0.2831
year and vessel capacity, detected no significant
quarter differences (Table 9). Based on that result,
I pooled over all quarters in the North Inside and
North Outside areas. Finally, I pooled over all
quarters in the South area because of the small sam-
ple sizes (Table 3).
Thus, after pooling over year, vessel capacity, and
quarter as indicated above, only three strata re-
mained for the 1977-78 data: 1) North Inside, 2)
North Outside, and 3) South.
Estimates
I obtained annual estimates of the total number
of dolphins killed by summing estimates for each of
three or five strata, depending on the year. Esti-
mates for a stratum were computed as the product
of (a) total number of dolphin sets (Table 10) and
(b) the corresponding total kill-per-set ratio (Table
11), increased by (c) the observed total number of
dolphins killed during experimental-gear trips (Table
Table 10.-
-Estimated number of dolphin sets (D) and number of trips (N) for the
population of trips, by year within strata.
North Inside
Quarters
North
Year
Statistic
Quarter 1
Quarter 2
3&4
Total
Outside
South
Total
1973
D
3,203
1,670
501
2,591
330
8,295
N
172
104
69
117
34
1974
D
3,486
1,176
242
2,453
12
7,369
N
126
92
38
93
4
1975
D
3,069
1,749
434
2,495
53
7,800
N
119
96
40
96
23
1976
D
1,618
1,520
716
2,001
729
6,584
N
127
98
92
90
76
1977
D
N
5,722
186
1,128
76
252
37
7,102
1978
D
N
2,811
206
1,153
58
162
27
4,126
Table 11.— By-trip means of total number of dolphins killed (k) and of number of
dolphin sets (d), total kill-per-set ratio (R), estimated standard error of the total kill-
per-set ratio (s), and number of sampled trips (n), by strata.
North Inside
North
Quarters
Years
Statistic
Quarter 1
Quarter 2
3&4
Total
Outside
South
1973-76
k
354.51
157.32
155.50
265.06
239.85
d
24.11
15.98
9.31
16.50
7.45
R
14.70
9.85
16.70
16.06
32.19
s
1.19
1.15
4.38
4.21
4.17
n
92
41
16
16
20
1977-78
k
58.66
57.55
22.12
d
19.88
13.71
4.73
R
2.95
4.20
4.68
s
0.23
0.51
1.03
n
190
78
33
565
FISHERY BULLETIN: VOL. 84, NO. 3
12). For example, the total estimated kill for 1977 cept that values for the species or species grouping
(Table 13) was obtained as a sum of estimates of the were substituted for the totals in (b) and (c) above,
total for three strata as [(5,722)(2.95) + 175] + Similarly, I estimated the variance of the number
[(1,128)(4.20) + 15] + [(252)(4.68) + 0]. Estimates of dolphins killed during any year by summing
for each species or species grouping were obtained variance estimates for each stratum. The estimated
in the same manner as estimates of the total, ex- variance of total kill for a stratum was computed
Table 12.— Total number of dolphins killed (/c), number of dolphin sets (d), and number
of experimental-gear trips (n), by year within strata. These data were excluded from
all sample and population statistics.
North Inside
North
Quarters
Year
Statistic
Quarter 1
Quarter 2
3 & 4
Total
Outside
South
Total
1973
k
0
0
513
0
0
513
d
0
0
46
0
0
46
n
0
0
2
0
0
1974
k
0
0
497
192
0
689
d
0
0
70
36
0
106
n
0
0
2
1
0
1975
k
0
0
512
271
0
783
d
0
0
76
26
0
102
n
0
0
2
1
0
1976
k
139
1,400
111
1,886
547
4,083
d
35
256
92
153
6
542
n
2
16
7
5
2
1977
k
175
15
0
190
d
129
8
0
137
n
4
2
0
1978
k
226
27
0
253
d
77
11
0
88
n
6
2
0
Table 13.— Estimates of dolphin mortality incidental to U.S. purse seiners, by species
grouping and year, with coefficients of variation in parentheses.
Year
Species grouping
1973
1974
1975
1976
1977
1978
Spotted
70,000
61,000
63,000
61,000
14,000
9,000
(0.12)
(0.13)
(0.13)
(0.11)
(0.08)
(0.08)
Spinner
Eastern1
12,000
1 1 ,000
1 1 ,600
9,500
1,300
700
(0.16)
(0.11)
(0.11)
(0.12)
(0.12)
(0.11)
Whitebelly
20,000
16,000
17,000
19,000
3,600
2,300
(0.17)
(0.19)
(0.19)
(0.15)
(0.11)
(0.10)
Unidentified
8,700
7,600
7,700
7,500
60
40
(0.24)
(0.26)
(0.25)
(0.25)
(0.18)
(0.17)
Total
41,000
35,000
36,000
36,000
5,000
3,000
Common
8,500
7,000
8,300
6,600
3,000
1,500
(0.22)
(0.25)
(0.22)
(0.20)
(0.23)
(0.24)
Striped
640
380
500
800
200
130
(0.30)
(0.34)
(0.35)
(0.33)
(0.26)
(0.24)
Unidentified
5,000
3,700
4,000
5,400
450
300
(0.19)
(0.20)
(0.19)
(0.26)
(0.12)
(0.12)
Other
180
90
100
280
180
100
(0.45)
(0.26)
(0.26)
(0.64)
(0.22)
(0.26)
Total*
125,000
107,000
112,000
110,000
23,000
14,000
(0.10)
(0.10)
(0.10)
(0.09)
(0.06)
(0.06)
'May include small number of Costa Rican spinner dolphins.
2Sum of estimated kills over species grouping not exactly equal to total estimated kill because
of rounding error.
566
WAHLEN: INCIDENTAL DOLPHIN MORTALITY
as the square of the product of (a) the number of
dolphin sets4 (Table 10) and (b) the corresponding
estimated standard error of the total kill-per-set
ratio (Table 11). I computed the estimated stratum
variance for each species or species grouping, sub-
stituting values for the species or species grouping
for the total in (b) above. I estimated the standard
errors (Table 11) using mean number of dolphin sets
per trip calculated from the sample rather than from
the population (Lo et al. 1982).
My annual estimates of the total number of
dolphins killed incidentally in the U.S. purse seine
fishery of the ETP ranged from a maximum of
125,000 dolphins in 1973 to a minimum of 14,000
dolphins in 1978, with coefficients of variation (CV)
no greater than 10% (Table 13). The estimated mor-
talities of the two species most often exploited,
spotted and spinner dolphins, together accounted
for about 80-90% of each annual total.
DISCUSSION AND CONCLUSIONS
The kill-per-set ratio, or mean kill, declined from
15 dolphins/set during the 1973-76 period to 3
dolphins/set during the 1977-78 period (Table 11,
pooled over quarter and area). Many changes affect-
ing dolphin kill were made during these periods,
including improvements in fishing gear and dolphin-
release procedures and introduction of federal
regulations. The change in mean kill between
1973-76 and 1977-78 coincided with the first NMFS
notice in late 1976 prohibiting fishing on dolphins
for the remainder of the year. This one example of
a correspondence between a change in the number
or distribution of dolphins killed during purse seine
sets and an identifiable legal or management action
is not necessarily indicative of a cause and effect
relationship. There are, however, two other ex-
amples of such a temporal correspondence present
in the data from 1964 through 1982.
In the second example, the data prior to 1973,
while sparse, suggest that the mean kill was substan-
tially higher than during the 1973-76 period. Lo and
Smith (1986) reported a mean kill of 46 dolphins/set
based on 1964 through 1972 data, pooled over vessel
capacity and catch of tuna. They found no consis-
tent differences in annual mean kill during that
period. The decline in the mean from 46 dolphins/
set during the 1964-72 period to 15 dolphins/set dur-
4Numbers of dolphin sets were treated as constants since no
variances were provided for these estimated quantities. Therefore,
my variances of estimated mortality are underestimated to an
unknown, though likely small, degree.
ing the 1973-76 period coincided with the passage
of the Marine Mammal Protection Act in late 1972.
In the third example, Wahlen and Smith (1985)
demonstrated a difference between the two periods
from 1979 through March 1981 and from April 1981
through 1982 in the frequency distributions of
number of dolphins killed during purse seine sets.
While the difference in mean kill during these two
periods was not significant, the percent of dolphin
sets in which no dolphins were killed (zero-kill sets)
decreased significantly. This decrease coincided with
a court order in March 1981 which prohibited using
data collected by NMFS observers to monitor com-
pliance of vessel captains with dolphin-release
procedures.
These three examples suggest that significant
legal or management actions can affect kill rates,
measured by the kill-per-set ratio or by the percent
of zero-kill sets. Furthermore, such effects on the
kill-per-set rate are reflected in the series of esti-
mates of total numbers of dolphins killed presented
here. For example, between 1976 and 1977 the num-
ber of dolphin sets increased slightly (Table 10), yet
total estimated mortality decreased by nearly 80%
(Table 13), due primarily to the significantly lower
kill rate after 1976. The further decline in estimated
mortality to 14,000 dolphins in 1978 reflects both
the lower kill rate and a decline in the number of
dolphin sets. Thus, the decrease in the kill rate
following the first enforcement of dolphin kill limits
in 1976 is reflected in the decrease in the estimates
of total mortality after 1976.
My estimates of total annual dolphin mortality in
U.S. purse seine fishing from 1973 through 1978
(Table 13) are lower, except for 1976, and more
precise than those in the Status of Porpoise Stocks
Workshop Report (SOPS) (Table 14). However, for
each year except 1973, my estimated total is con-
tained inside an approximate 95% confidence inter-
val around the estimated total (t) in SOPS, where
the confidence interval is computed as T ± 2 • CV • T.
Thus, the differences between my point estimates
and those in SOPS are small when the imprecision
(large CV) of the SOPS estimates is considered.
The lower precision of the SOPS estimates may
be due to overstratification because of a concern that
the sample might not be representative of the
population, particularly during the 1973-75 period.
Thus, in order to minimize bias, a large number of
strata (32 per year) were defined. Tests for between-
strata differences in mean kill were not made, but
strata were pooled to the degree that each pooled
stratum contained some sample data. However, even
after pooling, some strata during the years 1973-76
567
FISHERY BULLETIN: VOL. 84, NO. 3
Table 14.— Estimates of dolphin mortality incidental to U.S. purse seiners,
by species and year, from Status of Porpoise Stocks Workshop Report (Smith
text footnote 2). Coefficients of variation of totals in parentheses.
Year
Species
1973
1974
1975
1976
1977
1978
Spotted
114,000
75,000
84,000
57,000
12,000
13,000
Spinner
65,000
62,000
70,000
39,000
5,000
4,400
Common
18,000
3,000
2,300
5,400
6,600
1,000
Striped
40
140
900
2,000
100
250
Unidentified1
0
0
0
0
0
0
Other
0
80
160
690
80
50
Total2
197,000
140,000
157,000
104,000
24,000
19,000
(0.17)
(0.41)
(0.17)
(0.13)
(0.15)
(0.20)
1Kills of unidentified dolphins prorated among known species.
2Sum of estimated kills over species not exactly equal to total estimated kill because
of rounding error.
contained only one dolphin set. Such small sample
sizes within some strata account for the lower preci-
sion of the SOPS estimates relative to my estimates.
While the differences between my point estimates
and those in SOPS are small in a statistical sense,
my estimates are consistently lower except for 1976.
However, these new estimates are to be preferred
on methodological grounds. I tested for statistical-
ly significant between-strata differences in mean kill
and pooled over strata when significant differences
were not detected or when sample sizes were other-
wise too small. Pooling of the data produced esti-
mates which were more precise than the SOPS
estimates because it resulted in fewer strata with
larger sample sizes. However, to minimize the
possibility of introducing bias into the estimates dur-
ing the 1973-76 period, when the sample was un-
representative of area and quarter, I did not pool
over area and I pooled over quarter only in the event
of small sample sizes.
ACKNOWLEDGMENTS
I am grateful to K. E. Wallace, C. J. Orange, and
G. Ver Steeg for providing data, and to R. G. Punsly
for modifying his procedure to estimate numbers of
sets for U.S. seiners only. I also appreciate the
helpful reviews by two anonymous individuals as
well as those by F. G. Alverson, I. Barrett, D. G.
Chapman, P. S. Hammond, R. S. Holt, N. C. H. Lo,
J. M. Michalski, G. T. Sakagawa, and K.-T. Tsai.
Finally, I am especially indebted to T. D. Smith for
his suggestions and encouragement.
LITERATURE CITED
Allen, R. L., and M. D. Goldsmith.
1981. Dolphin mortality in the eastern tropical Pacific in-
cidental to purse seining for yellowfin tunas, 1979. Rep. Int.
Whaling Comm. 31:539-540.
1982. Dolphin mortality in the eastern tropical Pacific in-
cidental to purse seining for yellowfin tuna, 1980. Rep. Int.
Whaling Comm. 32:419-421.
Brown, M. B., and A. B. Forsythe.
1974. Robust tests for the equality of variances. J. Am. Stat.
Assoc. 69:364-367.
Dixon, W. J. (editor).
1983. BMDP statistical software. Univ. Calif. Press,
Berkeley, CA, 733 p.
Federal Register.
1976. Dep. Commer., NOAA, Regulations governing the
taking and importing of marine mammals. Prohibition on en-
circling marine mammals in the course of fishing operations
for yellowfin tuna. Fed. Regist. 41(201):45569.
Fox, W. W., Jr.
1978. Tuna-dolphin program: five years of progress. Oceans
ll(3):57-59.
Glass, G. V., P. D. Peckham, and J. R. Sanders.
1972. Consequences of failure to meet assumptions under-
lying the fixed effects analyses of variance and covariance.
Rev. Educ. Res. 42(3):237-288.
Hammond, P. S.
1984. Dolphin mortality incidental to purse-seining for tunas
in the eastern tropical Pacific, 1982. Rep. Int. Whaling
Comm. 34:539-541.
Hammond, P. S., and M. A. Hall.
1985. Dolphin mortality incidental to purse-seining for tunas
in the eastern tropical Pacific inflicted by the US fleet in 1983
and non-US fleet in 1979-1983. Rep. Int. Whaling Comm.
35:431-433.
Hammond, P. S., and K.-T. Tsai.
1983. Dolphin mortality incidental to purse-seining for tunas
in the eastern Pacific Ocean, 1979-81. Rep. Int. Whaling
Comm. 33:589-597.
Lo, N. C. H., J. E. Powers, and B. E. Wahlen.
1 982. E stimating and monitoring incidental dolphin mortality
in the eastern tropical Pacific tuna purse seine fishery.
Fish. Bull, U.S. 80:396-401.
Lo, N. C. H., and T. D. Smith.
1986. Incidental mortality of dolphins in the eastern tropical
Pacific 1959-1972. Fish. Bull., U.S. 84:27-34.
Perrin, W. F.
1969. Using porpoise to catch tuna. World Fish. 18(6):42-
45.
Punsly, R. G.
1983. Estimation of the number of purse-seiner sets on tuna
568
WAHLEN: INCIDENTAL DOLPHIN MORTALITY
associated with dolphins in the eastern Pacific Ocean dur- Snedecor, G. W., and W. G. Cochran.
ing 1959-1980. [In Engl, and Span.] Inter-Am. Trop. Tuna 1980. Statistical methods. 7th ed. Iowa State Univ. Press,
Comm. Bull. 18:229-299. Ames, 507 p.
Smith, T. D. Wahlen, B. E., and T. D. Smith.
1983. Changes in size of three dolphin (Stenella spp.) popula- 1985. Observer effect on incidental dolphin mortality in the
tions in the eastern tropical Pacific. Fish. Bull., U.S. 81: eastern tropical Pacific tuna fishery. Fish. Bull., U.S. 83:
1-13. 521-530.
569
DISTRIBUTION AND REPRODUCTIVE BIOLOGY OF
THE GOLDEN KING CRAB, LITHODES AEQUISPINA, IN
THE EASTERN BERING SEA
David A. Somerton1 and Robert S. Otto2
ABSTRACT
The golden king crab is a large anomuran that supports a new, rapidly expanding fishery in the eastern
Bering Sea and Aleutian Islands. Based on size, sex, and abundance data collected by U.S. observers
aboard foreign trawlers and by National Marine Fisheries Service personnel aboard research vessels,
we examined latitudinal and depth variation in mean size (carapace length), size at maturity, weight at
size, and relative abundance. Mean size decreases by 6.2 mm for males and 4.6 mm for females with
each 1 degree increase in latitude. Size at maturity decreases with increasing latitude from 130 mm for
males and 111 mm for females in the southern area to 92 mm and 98 mm in the northern area. These
decreases may be due to a temperature induced decrease in growth rate. Weight at size increases by
10% from the southern to the northern area owing to a latitudinal change in body shape. Mean size and
relative abundance of both sexes increase with a decrease in depth, suggesting that an onshore ontogenetic
migration occurs and that adult males migrate into somewhat shallower water than adult females. Fecun-
dity (number of uneyed embryos) of northern females increases with size according to -24815 + 323
CL, where CL is carapace length. This relationship changes with latitude and southern females carry
about 1,330 fewer eggs than equal-sized northern females. Mean length of uneyed eggs is 2.2 mm. Based
on the lack of a clear seasonal change in the occurrence of eyed and uneyed clutches, golden king crab
appear to have protracted, or perhaps year-round, breeding.
The golden king crab, Lithodes aequispina, is a large
anomuran that inhabits the upper continental slope
from southern British Columbia, Canada, northward
to the Bering Sea and westward to Suruga Bay,
Japan (Butler and Hart 1962; Suzuki and Sawada
1978). Although similar in size to red king crab,
Paralithodes camtschatica, and blue king crab, P.
platypus, the traditional species harvested by
Alaskan crab fisheries, golden king crab have not
been intensively harvested because they live in
deeper water than red and blue king crabs and are
therefore more difficult and expensive to capture
(McNair 1983). Since 1980, however, precipitous
declines in abundance of red and blue king crabs
have stimulated growth of directed fisheries for
golden king crab. These fisheries expanded rapidly
in the eastern Bering Sea and Aleutian Islands, and
between 1981 and 1983 the catch of golden king crab
increased from 50 t to 4900 t or 44% of the total
king crab catch from these areas.
Northwest and Alaska Fisheries Center Seattle Laboratory, Na-
tional Marine Fisheries Service, NOAA, 7600 Sand Point Way
N.E., Seattle, WA; present address: Southwest Fisheries Center
Hawaii Laboratory, National Marine Fisheries Service, NOAA,
2570 Dole Street, Honolulu, HI 96822-2396.
2Northwest and Alaska Fisheries Center Kodiak Laboratory, Na-
tional Marine Fisheries Service, NOAA, P.O. Box 1638, Kodiak,
AK 99615.
snt -sr*
Manuscript accepted September 1985.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
The fisheries for golden king crab have been
managed according to regulations designed for red
and blue king crabs (Alaska Department of Fish and
Game 1983; Miller 1976) because little biological in-
formation was available to establish more specific
regulations. Although golden king crab have been
studied before, published reports either concern
Asian stocks (Hiramoto and Sato 1970; Suzuki and
Sawada 1978; Rodin 1970) or are restricted to tax-
onomy (Benedict 1895; Makarov 1938), distribution
(Butler and Hart 1962; Slizkin 1974), or early life
history (Haynes 1981).
In 1981, the National Marine Fisheries Service
(NMFS) began collecting biological data on golden
king crab necessary for establishing minimum size
limits and fishing seasons. We summarize these data
here, focusing our attention on latitudinal and depth
gradients in mean size, size at maturity, weight at
size, and sex ratio as well as various aspects of the
reproductive biology. We then examine the manage-
ment implications of our findings.
MATERIALS AND METHODS
Data Sources
Golden king crab were sampled by NMFS re-
571
FISHERY BULLETIN: VOL. 84, NO. 3
search personnel on stock assessment and tagging
cruises and by NMFS observers aboard foreign
fishing vessels. In the following we distinguish be-
tween survey data and observer data because the
sampling designs differed considerably. In both
cases, however, crabs were measured with calipers
to the nearest millimeter according to the descrip-
tions in Wallace et al. (1949).
Survey Data
From 1981 to 1983, NMFS conducted 10 survey
cruises sampling the eastern Bering Sea population
of golden king crab with either bottom trawls or
commercial king crab pots (Table 1). All crabs were
measured for carapace length, and females were
classified into one of four categories of reproduc-
tive condition:
1) Non-ovigerous - no embryos or empty egg
cases attached to the pleopod setae.
2) uneyed embryos - embryos without conspicu-
ous dark eyes.
3) eyed embryos - embryos with dark eyes.
4) empty egg cases - empty egg cases and funi-
culi attached to the pleopod setae.
When opportunity occurred, one or more of the
following were also collected:
1) height of the right chela of males (excluding
males with partially regenerated right chela).
2) Total wet body weight of males, measured to
the nearest gram on a triple beam balance or to the
nearest 5 g on a handheld spring scale (excluding
males with damaged exoskeletons or missing
appendages).
3) egg masses from females (stored in Formalin3
diluted to 10% with seawater).
Observer Data
Golden king crab, like most of the other large
Alaskan crabs, is classified as a prohibited species
and, as such, may not be retained if captured by
foreign fisheries. Because of this status, NMFS
fishery observers routinely record the carapace
length, sex, and number of golden king crab that
are incidentally caught by foreign vessels during
their normal fishing operations for other species
(Nelson et al. 1981). To delineate the distribution
Table 1.— Inclusive dates, latitude and depth ranges, number of
crabs sampled and type of sampling gear are shown for each of
the 10 golden king crab research cruises conducted by the Na-
tional Marine Fisheries Service.
Latitude
Depth
Number
Year
Dates
(degrees N)
(m)
males
females
Gear
1981
2/12-2/23
54.4-55.1
346-472
4
6
trawl
1982
7/12-8/4
58.3-60.9
168-849
292
341
trawl
1983
1/31-2/8
52.3-52.5
183-366
188
123
pot
2/22-2/24
54.4-55.7
362-461
24
17
trawl
5/9-5/10
56.0-56.1
365-421
288
1,114
pot
5/12-5/15
57.8-58.5
329-365
489
1,753
pot
7/8-7/10
57.7-57.7
347-365
1,073
741
pot
7/14-7/18
55.9-56.3
311-384
1,285
1,012
pot
10/2-10/4
56.2-56.2
347-365
596
1,035
pot
11/15-11/21
52.4-52.6
110-283
376
404
pot
'Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
of golden king crab in the eastern Bering Sea, we
chose to examine the 1981 and 1982 observer data
obtained from Japanese small stern trawlers that
fish for turbot (Reinhardtius hippoglossoides) be-
cause 1) these vessels use trawls designed to remain
in direct contact with the bottom and are therefore
likely to catch crabs, 2) these vessels operate year-
round along nearly the entire length of the continen-
tal slope of the eastern Bering Sea, and 3) turbot
have a depth distribution similar to that of golden
king crab. Although these data are not necessarily
a random sample of the golden king crab population,
they are the most extensive data available and in-
clude samples from the entire depth range of golden
king crab during all four seasons. The number of
crabs measured and the number of trawl hauls
sampled are summarized by year, month, latitude,
and depth (Table 2). Due to a lack of Japanese
fishing effort for turbot, observer data were unavail-
able for areas south of lat. 54°15'N.
Both survey and observer data, in some instances,
were partitioned into three latitudinal strata or
subareas (Fig. 1): northern (north of lat. 58°30'N),
central (between lat. 58°30'N and 54°15'N),
southern (south of lat. 54°15'N and east of long.
173°00'W), which correspond approximately to the
crab management districts used by the Alaska
Department of Fish and Game. In addition, the
observer data were partitioned into two depth strata
separated at the approximate median depth (500 m)
of the samples (nearly the entire depth range of
golden king crab is bounded by the 200 m and 1,000
m isobaths).
Methods of Analysis
Size-frequency distributions by sex were con-
structed from the combined 1981 and 1982 observer
572
SOMERTON and OTTO: DISTRIBUTION AND REPRODUCTION OF GOLDEN KING CRAB
Table 2. — Number of trawl hauls sampled (ex-
cluding hauls without crabs) and number of
crabs sexed and measured by U.S. observers
aboard Japanese small trawlers within the
study area during 1981 and 1982. Data are
summarized by depth, latitude and month.
1981
1982
Hauls
Crabs
Hauls
Crabs
Depth (m)
100
0
0
3
3
200
7
81
23
86
300
30
323
33
848
400
217
2,475
339
3,551
500
456
6,885
548
4,380
600
201
2,065
192
1,112
700
16
97
27
81
800
6
24
1
2
900
2
13
0
0
1,000
1
6
0
0
Latitude (degrees
N)
53
12
18
0
0
54
7
135
132
678
55
34
455
43
184
56
165
1,582
163
879
57
59
376
75
552
58
284
3,936
151
899
59
175
2,995
166
2,019
60
200
2,472
436
4,852
Month
1
18
55
19
125
2
65
443
19
79
3
75
977
66
528
4
114
1,688
41
73
5
104
1,398
102
332
6
112
2,027
136
1,681
7
72
1,528
75
306
8
89
1,121
124
1,215
9
106
927
192
992
10
99
814
194
2,436
11
68
931
150
1,654
12
14
60
48
654
Total
936
1 1 ,969
1,166
10,063
data for each of the two depth strata within the
northern and central subareas to help illustrate
depth and latitude trends in the size distributions
(see Figure 2). Potential bias because of the varia-
tion of fishing effort with depth was minimized by
first partitioning the data into 100 m depth inter-
vals. Within each depth interval, a size-frequency
distribution and an average catch per hour (CPH)
were calculated. Size-frequency distributions,
weighted by the appropriate mean CPH, were then
summed over all 100 m depth intervals within each
of the two depth strata.
Variations in mean size, CPH, and proportion
male with latitude and depth were also examined
using multiple regression. Two normalizing trans-
formations were used: 1) CPH was transformed to
the natural log scale and 2) proportion male was
transformed to the arcsine-square root scale after
replacing 0 with 0.25/N and 1 with (N - 0.25)/JV,
where N is the number of crabs within each trawl
haul (Bartlett 1947).
Egg size was estimated by randomly selecting 10
eggs from each preserved egg mass and measuring
their maximum lengths (eggs are oval) to the nearest
0.1 mm with an ocular micrometer. The remainder
of each egg mass was air dried and, after separating
the eggs from the pleopods and setae, weighed to
the nearest 0.1 mg. Two subsamples of about 200
eggs each were randomly selected from each dried
egg mass and then weighed and counted. Fecundity
was then estimated by dividing the total weight of
an egg mass by the average of the two estimates
of individual egg weight that were obtained from
that egg mass.
Male size at maturity was estimated from the
allometric growth of the right chela. When king crab
chela measurements are plotted against carapace
measurements on log-log axes, the data conform to
two straight lines that intersect at the average
carapace length at maturity (see Figure 3) (Somer-
ton 1980; Somerton and Macintosh 1983). To
estimate this size, we used the computer method
described in Somerton and Macintosh (1983) which
fits a pair of intersecting straight lines by iteratively
varying the carapace length at the intersection point
until the residual sum of squares about the lines is
minimized. Variance of the male size at maturity
was estimated using a computer technique known
as bootstrapping (Efron and Gong 1983). In our ap-
plication, the method consisted of randomly choos-
ing, with replacement, 50 subsamples equal in size
to the original data set. For each subsample, the size
at maturity was estimated by fitting the two line
model. Variance of the estimated size at maturity
was then computed as the variance among the 50
independent estimates.
Although we attempted to detect and exclude par-
tially regenerated chelae in the field, we were not
always successful. Measurements from partially
regenerated chelae can increase the variance of
estimates of male size at maturity; therefore, these
measurements were removed from the data set
before analysis using a sequential outlier elimina-
tion technique described in Somerton and Macin-
tosh (1983).
Golden king crab females were considered to be
mature, if they had eggs or empty egg cases at-
tached to the pleopod setae. Although we are not
certain that this is always true, for red and blue king
crabs, adult females extrude eggs soon after every
molt and the empty egg cases remain attached to
the pleopod setae until the next molt (Somerton and
Macintosh 1985).
573
FISHERY BULLETIN: VOL. 84, NO. 3
61
ST.
MATTHEW
ISLAND
/l S
fV MAT
^V-ISL
NORTHERN
PRIBILOF
ISLANDS
PftlBILOF
CANYON
CENTRAL
59
-57
■55
-53
*fr/^'
SOUTHERN
51
180
178
176
174
172
170
168
Figure 1.— Areas of the Bering Sea and eastern Aleutian Islands where golden king crab were sampled by
U.S. fishery observers and National Marine Fisheries Service research cruises. Golden king crab occur primarily
in a region bounded by the 200 m (solid line) and 1,000 m (dashed line) isobaths. The dark lines indicate the
separation of this region into the three latitudinal strata discussed in the text.
Female size at maturity was estimated as the size
at which 50% of the crabs were mature. Weighted
nonlinear regression (weights equal to the inverse
of the binomial variance at each size) was used to
fit a logistic equation to the percentage mature
within 5 mm size intervals. The fitted logistic equa-
tion was then evaluated to determine the carapace
length corresponding to 50% maturity. Variance of
this size was estimated using the formula provided
in Somerton (1980).
574
SOMERTON and OTTO: DISTRIBUTION AND REPRODUCTION OF GOLDEN KING CRAB
BIOLOGICAL VARIATION WITH
DEPTH AND LATITUDE
Mean Size
Size-frequency distributions of golden king crab,
based on the combined 1981 and 1982 observer data,
are shown by sex, area, and depth strata in Figure
2. Linear trends in mean size with depth and latitude
were examined statistically using multiple regres-
sion. For each sex in each year, when carapace
length was regressed against latitude and depth
simultaneously, ignoring interaction, both the
latitude coefficient and the depth coefficient were
negative and highly significant (P < 0.001). Aver-
aged over both years, mean size decreased by 6.2
mm for males and by 4.6 mm for females for each
1 degree increase in latitude, and mean size de-
creased by 7.9 mm for males and by 6.2 mm for
females with each 100 m increase in depth.
The latitudinal decrease in size probably reflects
a latitudinal decrease in growth rate. Two shallow-
water Bering Sea crabs, Chionoecetes bairdi and C.
opilio, also show a latitudinal decrease in size, and
this decrease was correlated with a latitudinal
decrease in maximum summer water temperature
(Somerton 1981a). Although we lack sufficient tem-
perature data from the depths inhabited by golden
king crab to allow a statistical test, it is likely that
mean annual bottom temperature also decreases
0.25 -I
MALES NORTHERN AREA
0.35 FEMALES NORTHERN AREA
0.00
0 25 50 75 100 125 150 175 200
0.00
0 25 50 75 100 125 150 175 200
0.25 MALES CENTRAL AREA
0.00
0 25 50 75 100 125 150 175 200
CARAPACE LENGTH (MM)
0.35 FEMALES CENTRAL AREA
0-30 -
0.25 -
<
o
0.20
o
I
UJ
CL
x 0.15-
o
0. 10
0.05 -
0.00
<500 M
>500 M
CARAPACE LENGTH (MM)
Figure 2.— Size-frequency histograms for males and females of golden king crab, by depth strata and subarea. Due to differences
in the sampling intensity with depth (Table 2), frequencies have been standardized to catch per hour of trawling.
575
FISHERY BULLETIN: VOL. 84, NO. 3
with increasing latitude along the slope. If this is
true, then it is reasonable to assume that growth
rates are lower in higher latitudes. Part of the lat-
itudinal decrease in mean size, however, is due to
the greater relative abundance of small (25-50 mm)
crabs in the northern area (Fig. 2). Since we have
only two years of data, we do not know if the greater
abundance of small crabs in the northern area is a
persistent feature of the distribution. But if it is, it
may indicate that greater larval settlement occurs
in the northern area because of the advection of lar-
vae by the northwesterly currents over the continen-
tal slope (Kinder and Schumacher 1981).
The decrease in size with depth may reflect an
ontogenetic upslope migration. Another slope dwell-
ing crab, Chionoecetes tanneri, also displays a de-
crease in size with depth, and this was attributed
to an offshore advection of pelagic larvae followed
by an onshore migration of juveniles (Pereyra 1968).
Although an onshore migration might explain the
size variation with depth of golden king crab in the
eastern Bering Sea, offshore advection depends on
local oceanographic conditions and may not occur
everywhere ovigerous golden king crab occur. For
example, studies of golden king crab in other areas
indicated that adults could be found in shallower
water than juveniles (Hiromoto and Sato 1970), or
at similar depths as juveniles but in different areas
(Rodin 1970) or in deeper water than juveniles (N.
Sloan4).
Size at Maturity
The change in the relative growth of a male's chela
which occurs at maturity is more pronounced for
golden king crab than it is for either blue king crab
(Somerton and Macintosh 1983) or red king crab
(Somerton 1980), and this allows greater precision
in the estimates of size at maturity (Fig. 3). Never-
theless, the estimates of male size at maturity are
less precise than those for females (Fig. 4). For both
sexes, however, the estimated sizes at maturity dif-
fer significantly between areas and progressively
decrease with increasing latitude (Fig. 4).
The decrease in the size at maturity is consistent
with a latitudinal decrease in growth rate; however,
the decrease is greater for males than it is for
females (Fig. 4). If golden king crab are similar to
red king crab (Weber 1967) in that males and
females grow identically while they are immature,
4N. Sloan, Department of Fisheries and Oceans, Pacific Bio-
logical Station, Nanaimo, British Columbia, V9R 5K6, Canada,
pers. commun. 1984.
576
then the greater latitudinal decrease in male size at
maturity implies that female age at maturity in-
creases, relative to that of males, with latitude. This
could occur if females and males have different life
history strategies to maximize their reproductive
values (Bell 1980). The reproductive value of a
female is largely determined by her lifetime fecun-
dity. Since fecundity increases markedly with size
and somatic growth decreases abruptly at matur-
ity, under conditions of reduced growth, female
reproductive value might be increased by delaying
maturity until some optimum size is reached. The
reproductive value of a male, however, is largely
determined by the number of females he is able to
mate with over his lifetime. Unless access to females
is strictly limited to the largest males, male repro-
ductive value is unlikely to be increased by delay-
ing maturity. Along a gradient of decreasing growth
rate, such strategies would lead to a divergence
between male and female sizes and ages at maturity.
Weight at Size
Weight-size relationships of males were deter-
mined for each of the three subareas by regressing
body weight on carapace length after transforming
both variables to natural logarithms. Analysis of
covariance showed that the slopes of the regression
lines were not significantly different (F = 0.49, df
= 2, 1,079, P = 0.613), but that the intercepts were
significantly different between areas (F = 19.03, df
= 2, 1,081, P < 0.001). Pairwise £-tests further
showed that the intercept for each area differed
significantly from the other two (Bonferroni critical
values; maximum P < 0.05) and that the intercepts
progressively increased with increasing latitude.
Males in higher latitudes are therefore propor-
tionately heavier than equal-sized males from lower
latitudes.
This proportionate change in weight with latitude
might be due to changes in body shape, such as the
relative size of the chelae, that are coincident with
the onset of maturity. Since the rate of chela growth
increases, relative to carapace growth, at maturity,
and since the size at maturity decreases with lat-
itude, mature males in northern areas should have
larger chelae than equal-sized males in southern
Figure 3.— For the golden king crab males, chela heights, carapace
lengths, and the best fitting two line model are shown for each
subarea. For the females, percentage mature, within 5 mm size
intervals, and the fitted logistic equation are shown for each sub-
area. Estimated sizes (carapace length) at maturity are indicated
by dotted lines.
SOMERTON and OTTO: DISTRIBUTION AND REPRODUCTION OF GOLDEN KING CRAB
MALE FEMALE
80-,
60
NORTHERN
SM = 92.0
SD = 2.4
N = 205
o
UJ
00
90
80 -
70 -
60 -
50 -
40 -
30
20
10 i
0
NORTHERN
SM = 97.7
SD = 0.5
N = 324
200
10
30
50
70
80-|
60
CENTRAL
SM = 107.0
SD = 4-6
N = 1866
UJ
CD
<
O
a:
UJ
200
80]S0UTHERN
eo^SM = 1 30.0
.SD = 4.0
N = 299
40
20-
10
8
40 60 80 100
CARAPACE LENGTH (MM)
200
UJ
UJ
o
<
o
UJ
Q.
00
90
80
70
60
50
40
30
20
10
0
SOUTHERN
SM = 110.7
HSD = 0.8
N = 527
50
70 90 110 130 150
CARAPACE LENGTH (MM)
577
FISHERY BULLETIN: VOL. 84, NO. 3
1 40 1
30
X
120
I—
CD
-z.
UJ
_J
1 1 0
UJ
o
<
100
<
en
<
o
90
80
-• — MALE
-— FEMALES
1 1 1 1
SOUTH CENTRAL NORTH
AREA
Figure 4.— For both sexes of golden king crab, estimated sizes
at maturity, and their 95% confidence intervals, are plotted against
area.
areas. To test whether this is true, chela height and
carapace length relationships for adult males were
compared between areas. Analysis of covariance
showed that the slopes did not differ (F = 0.14, df
= 2, 1,998, P = 0.87), but the intercepts differed
significantly (F = 146.7, df = 2, 2,000, P < 0.001).
Pairwise i-tests further showed that each intercept
differed significantly (Bonferroni critical values;
maximum P < 0.05) from the other two and, similar
to the weight-size relationships, that the intercepts
progressively increased with latitude. Thus north-
ern males, which are the heaviest, have the largest
chelae.
By itself, chela size is unlikely to be responsible
for latitudinal differences in weight because chela
weight is only a small proportion of total body
weight. However, chela size may be correlated with
other body dimensions (for example, length of walk-
ing legs) that also increase relative to carapace
length at maturity. We therefore used chela height
as a proxy for these dimensions and examined
whether the difference in chela height could account
for the difference in weight-size relationships. This
was done by comparing the weight-size relationships
between areas including the logarithm of chela
height as a covariate. Two additional modifications
of the previous weight-size comparison were made.
First, since weights and chela measurements were
not obtained from the same crabs in the southern
area, the comparison was restricted to the northern
and central areas. Second, since chela height and
carapace length are linearly related only over the
adult (or juvenile) size range, the comparison was
restricted to males greater than the size at matur-
ity in each area. When the northern (N = 129) and
central (N = 614) areas were compared consider-
ing only carapace length as a covariate, the slopes
were not significantly different (F = 0.06, df = 2,
739, P = 0.81), but the intercepts were significant-
ly different (F = 7.36, df = 1, 740, P = 0.007). When
chela height was included as a covariate, however,
neither the slopes (P = 0.316) nor the intercepts (P
= 0.430) differed significantly between areas. This
indicates that latitudinal changes in chela size, and
perhaps other body measurements that also increase
at maturity, account for the observed latitudinal in-
crease in body weight.
Juvenile weight-size relationships were also com-
pared between the northern (N = 10) and central
(N = 207) areas and neither the slopes (F = 0.06,
df = 1, 213, P = 0.938) nor the intercepts (F = 0.19,
df = 1, 214, P = 0.664) were significantly different.
The weight-size relationship for male golden king
crabs is therefore described by one equation for
juveniles and three equations for adults. Trans-
formed back to a linear scale, these relationships
are
Juveniles W = 0.000365 CL3-099 (N = 217, R2 = 0.88)
Adults
Northern W = 0.000225 CL3206 (N = 139, R2
Central W = 0.000219 CL3206 (N = 632, R2
Southern W = 0.000204 CL3206 (N = 100, R2
0.93)
0.91)
0.91)
where W is body weight in grams and CL is cara-
pace length in millimeters. Within the adult size
range, males from the northern area are 10.3%
heavier and males from the central area are 9.8%
heavier than equal-sized males from the southern
area.
Relative Abundance and
Proportion Male
Relative abundance, or catch per hour (CPH),
based on combined 1981 and 1982 observer data,
is shown by sex, latitude, and depth in Figure 5.
Linear trends in CPH with depth and latitude were
examined statistically using multiple regression
(depth and latitude were considered simultaneous-
ly; interaction was ignored). The latitude coefficient
for males was not significant (P > 0.05) in either
year, but the latitude coefficient for females was
positive and highly significant (P < 0.01) in both
years. The depth coefficient for males was negative
578
SOMERTON and OTTO: DISTRIBUTION AND REPRODUCTION OF GOLDEN KING CRAB
3.0 -, . 3.0
54 55 56 57 58 59 60
700
0.7
0.7
55
56 57 51
LATITUDE
59 60
100 300 500 700
DEPTH
Figure 5.— Catch per hour, by sex, and the proportion of males of golden king crab are shown as a function
of latitude (left panels) and depth (right panels).
and highly significant in both years (P < 0.01), but
the depth coefficient for females, although negative
in both years, was significant (P < 0.05) in only one.
Although male CPH decreases significantly with
depth whereas female CPH decreases significantly
with latitude, CPH is not a strict linear function of
depth and latitude; therefore, linear approximations
mask aspects of the variability. The important point
is that both male and female CPH generally increase
with an increase in latitude or a decrease in depth,
but at more southerly latitudes or at the shallowest
depth, male CPH is considerably higher than female
CPH (Fig. 5).
Different trends in CPH between sexes suggested
that the sex ratio of golden king crab varied spatial-
ly. To investigate this further we examined the
variation in proportion of males within trawl hauls
having at least five crabs. The proportion of males,
based on combined 1981 and 1982 observer data,
is shown by latitude and depth in Figure 5. When
the proportion of males was regressed against
latitude and depth (using weights equal to the num-
ber of crabs within each trawl haul), the latitude
coefficient was negative and highly significant (P
< 0.01) in both years; and the depth coefficient,
although negative in both years, was significant (P
< 0.05) in only one.
From a biological perspective, the latitudinal
decrease in the proportion of males is difficult to ex-
plain; therefore, we considered possible sampling
bias that could lead to an apparent change in the
proportion of males. Since males are considerably
larger than females in the central area but nearly
the same size as females in the northern area, the
proportion of males might vary with latitude due to
size selectivity of the trawls. This hypothesis was
tested by comparing the proportion of males be-
tween the northern and central areas considering
only crabs within an equal size range. To eliminate
a possible confounding effect due to a sexual differ-
ence in growth rate that begins at maturity, we
restricted the comparison to crabs <90 mm. Based
579
FISHERY BULLETIN: VOL. 84, NO. 3
on the combined 1981 and 1982 observer data, the
proportion of males was 0.51 (N = 1,375) in the cen-
tral area and 0.43 (N = 8,271) in the northern area.
Since the proportion of males still differed signifi-
cantly between areas (2x2 contingency table, x2
= 30.7, df = 1, P < 0.001), it is unlikely that the
change in the proportion of males was due to size
selectivity. Furthermore, since the difference in the
proportion of males appears to be established before
maturity, biological explanations such as sexual dif-
ferences in migratory behavior or natural mortal-
ity are also unlikely.
Although we cannot explain the latitudinal varia-
tion in the proportion of males, we believe that the
depth variation, especially the abrupt increase in the
proportion of males in the shallowest depth zone,
is due to sexual segregation. Sexual segregation by
depth has been observed for another slope-dwelling
crab, C. tanneri (Pereyra 1966). Adult female C. tan-
neri occur within a rather narrow depth zone
throughout the year while adult males undergo a
seasonal migration from relatively shallow water in
summer to the deeper water occupied by females
during the winter mating period. To determine if
golden king crab have a similar seasonal migration,
we examined the proportion of males from the
northern area at depths <400 m (the northern area
had nearly equal sampling in all four seasons). Using
pooled 1981 and 1982 data, analysis of variance
showed that the proportion of males did not vary
significantly between seasons (F = 0.13, df = 3, 179,
P > 0.05). Although adult males of golden king crab
probably congregate in somewhat shallower water
than adult females, unlike C. tanneri this segre-
gation appears to be maintained throughout the
year.
REPRODUCTIVE BIOLOGY
significance. Since the coefficient was not signifi-
cantly different from zero (F = 3.85, df = 1, 57,
P = 0.06), we chose a linear relationship to describe
the data.
Fecundity-size relationships for females with
uneyed embryos (N = 46) and eyed embryos (N =
19) from the central area were compared to deter-
mine whether the relationships changed with stage
of embryo development. Analysis of covariance
showed that the slopes did not differ (F = 0.77, df
= 1, 61, P = 0.38) but that the intercept for eyed
embryos was significantly less (F = 4.89, df = 1,
62, P = 0.03) than that for uneyed embryos. At 114
mm, the median size of adult females in all areas
combined, uneyed clutches were 18% greater than
eyed clutches. Similar to other crab species (Wear
1974), golden king crab lose a significant number
of embryos between egg extrusion and the appear-
ance of embryonic eyes.
Fecundity-size relationships were then compared
between the northern (N = 59), central (N = 46),
and southern (N = 24) areas considering only those
clutches with uneyed eggs. Analysis of covariance
showed that the slopes did not differ (F = 0.74, df
= 2, 123, P = 0.48), but the intercepts differed
significantly between areas (F = 4.38, df = 2, 125,
P = 0.01). Pairwise i-tests indicated that southern
and central intercepts did not differ (P = 0.99) from
each other, but that both differed significantly (P
= 0.01, P = 0.04) from the northern intercept. Data
from the southern and central areas were therefore
pooled and compared with those from the northern
area. Again, the slopes did not differ (F = 1.25, df
= 1, 125, P = 0.27), but the northern intercept was
significantly greater (F = 8.83, df = 1, 126, P =
0.004) than the pooled central and southern inter-
cept. Assuming equal slopes, the resulting fecundity-
size relationships are
Fecundity
Fecundity-size relationships for golden king crab
were estimated stagewise by examining 1) the form
of the relationship, 2) whether the relationships
varied with stage of embryo development, and 3)
whether the relationships varied between areas.
The fecundity of king crabs has been reported to
increase as either a linear (Haynes 1968) or a curvi-
linear (Somerton 1981b) function of carapace length.
To determine which form was more appropriate for
golden king crab, a second degree polynomial was
fitted to the fecundity and size data from the north-
ern area (all clutches contained uneyed embryos) and
the coefficient of the quadratic term was tested for
Northern
Central-southern
E = -24815 + 323 CL
(N = 59, R2 = 0.79)
E = -26145 + 323 CL
(N = 68, R2 = 0.74)
where E is number of uneyed eggs and CL is cara-
pace length in millimeters. Females from the north-
ern area carry, on average, 1,330 more eggs than
equal-sized females from the central and southern
areas. For 114 mm females, this represents a 12.6%
difference in fecundity.
Northern females may be more fecund than equal-
sized central and southern females because they are
older and size-specific fecundity often increases with
age (Pianka and Parker 1975). But, it is also likely
580
SOMERTON and OTTO: DISTRIBUTION AND REPRODUCTION OF GOLDEN KING CRAB
that the observed difference in fecundity is an arti-
fact due to a difference in mean embryo age. We
attempted to eliminate the effect of embryo age by
considering only clutches with uneyed embryos, but
this may not have been a sufficiently sensitive
criterion of age and northern females could have had
more embryos simply because they had younger em-
bryos. Considering that for equal-sized females the
percent difference in clutch size between eyed and
uneyed stages was greater than the percent differ-
ence in clutch size between areas, it is possible that
the loss of embryos within the uneyed stage is suf-
ficient to account for between-area differences.
More precise embryo aging techniques are needed
to clarify this.
Egg Size
To estimate the size of golden king crab eggs, we
considered 1) whether egg size varied with stage
of embryo development and 2) whether egg size
varied between areas. When mean lengths of uneyed
eggs (N = 42) and eyed eggs (N = 26) from the cen-
tral area were compared, eyed eggs were found to
be significantly larger than uneyed eggs (two sam-
ple £-test, P < 0.001). Golden king crab eggs
therefore appear to increase in size, as has been
reported for other crab species (Wear 1974), dur-
ing embryonic development. When mean length of
uneyed eggs from the southern (N = 25) and cen-
tral (N = 42) areas (no egg length data was collected
from the northern area) were compared, no signifi-
cant difference was found (two sample £-test, P =
0.25). Mean length of uneyed eggs, based on the
pooled central and southern data, is 2.2 mm (SD =
0.1).
Our estimate of egg length is similar to those
reported for Asian populations of golden king crab
(2.38 mm, Hiramoto and Sato 1970; 2.30 mm, Suzuki
and Sawada 1978), and it is also similar to egg
lengths reported for other Lithodes species (L. ant-
arctica, 2.2 mm, Guzman and Campodonico 1972;
L. couesi, 2.3 mm, Somerton 1981b). However, this
size is more than twice as large as the egg lengths
reported for Paralithodes species (P. camtschatica,
1.0 mm, Haynes 1968; P. platypus, 1.2 mm, Sasa-
kawa 1975). The larger eggs of golden king crab are,
in turn, reflected in the relatively large size of their
first stage zoea (L. aequispina, 7.3 mm TL, Haynes
1981; P. camtschatica, 4.6 mm TL, Sato and Tanaka
1949; P. platypus, 4.9 mm TL, Hoffman 1968). The
larger size of L. aequispina larvae may allow them
to withstand starvation for a longer period or may
allow them to capture a wider size range of prey
than Paralithodes larvae. If this is true, golden king
crab larvae may not need to ascend to the photic
zone but instead stay at greater depths. Evidence
supporting this hypothesis is provided by a study
on crab larvae that sampled the upper 50 m near
the edge of the eastern Bering sea continental shelf
(Fig. 1). Although both P. platypus and P. cam-
tschatica larvae were found, L. aequispina larvae
were not (D. Armstrong5).
Seasonality of Reproduction
King crabs either can be synchronous and seasonal
in their egg extrusion and embryo hatching, as
reported for P. camtschatica (Powell et al. 1973),
or they can be asynchronous and lack seasonal
periodicity, as reported for L. couesi (Somerton
1981b). To determine which pattern better charac-
terizes golden king crab, we tabulated the percent-
age of mature females in each of the three reproduc-
tive conditions by area and by quarter (Table 3). If
the reproductive cycle were synchronous and
seasonal, then each of the three categories of repro-
ductive condition should predominate sequentially
over the course of a year, but such a pattern is not
evident. Regardless of the area or the season in
which a sample was collected, all three reproduc-
tive categories were always obtained. This sug-
gests that golden king crab have an asynchronous
reproductive cycle lacking distinct seasonal vari-
ation.
Table 3.— Percentage of adult females in each of three categories
of reproductive condition: 1) uneyed embryos, 2) eyed embryos,
and 3) empty egg cases, and total sample size (W) by subarea and
quarter.
South
Central
North
Quarter 1 2 3
N 1
2 3 N
1 2 3 N
1 55 33 12
2
3
4 28 67 5
67 50
28
14
384 61
8 42 12
63 9 1,307
36 50 1,399
16 23 859
78 3 19 224
The apparent lack of seasonality conflicts with
previous studies of golden king crab reproduction.
Hiramoto and Sato (1970) reported that egg extru-
sion occurs from July to October and embryo hatch-
ing occurs from February to July along central
Japan. However, Hiramoto and Sato found embryos
in late stages of development throughout the year,
6D. Armstrong, College of Fisheries, University of Washington,
Seattle, WA 98195, pers. commun. 1984.
581
FISHERY BULLETIN: VOL. 84, NO. 3
indicating that embryo hatching was probably occur-
ring at times other than the peak season. Rodin
(1970) reported that egg extrusion occurs from
August to September based on the relatively high
incidence of recently molted females with new em-
bryos. However, Rodin based this on only one sum-
mer sample and some of our samples, especially
those from the northern area, if examined alone
would have also incorrectly led to the same conclu-
sion. Our findings, however, are consistent with
those for other deep water crabs (L. couesi, Somer-
ton 1981b; Geryon quinquedens, Haefner 1978)
which have asynchronous or protracted spawning.
Asynchronous spawning is also consistent with
two of our other observations. First, the larvae of
golden king crab, due to their large size and pre-
sumably deep habitat, should be relatively insen-
sitive to seasonal changes in primary production.
Second, adult males and females of golden king crab
appear to segregate by depth and this segregation
appears to be maintained throughout the year. Such
year-round sexual segregation is unlikely for a
seasonally reproducing species; however, it is con-
sistent with an asynchronous reproducing species
if only the reproductively active individuals migrate
between depth zones.
IMPLICATIONS FOR
FISHERY MANAGEMENT
Two of our findings, the latitudinal decrease in the
size at maturity and the asynchronous reproductive
cycle, pertain to regulations used to manage the
golden king crab fisheries in Alaska.
Commercial harvest of king crabs is restricted to
males larger than a minimum legal size (maximum
carapace width including spines) which is specified
for each species in each management area. These
minimum sizes are set at the average size of a male
three years after reaching maturity based on the ra-
tionale that such a size would preserve sufficient
males for breeding even when the exploitation rate
is high (North Pacific Fishery Management Coun-
cil 1981). Thus, to establish a minimum size limit that
conforms to this rule, both an estimate of the size
at maturity and an estimate of male growth rate are
needed. Unfortunately, we lack sufficient data to
estimate the growth rates of golden king crab in any
of the three management areas considered here and
therefore cannot determine appropriate minimum
size limits. However, our estimates of male size at
maturity can be used to judge, in a qualitative sense,
the adequacy of the current minimum size limits.
These size limits and the estimated sizes at matur-
ity, expressed in terms of carapace length, are as
follows:
Minimum size limit Size at maturity
(mm CL) (mm CL)
Northern area
123
92
Central area
123
107
Southern area
134
130
The current minimum size limits decrease with
increasing latitude, but not in proportion to the esti-
mated sizes at maturity. Based solely on the relative
magnitude of our estimates, we believe that the cur-
rent minimum size limit in the southern area, and
perhaps in the central area as well, is too low.
However, we believe that the prolonged or year-
round breeding of golden king crab would allow
males more opportunities for mating than would be
possible with a short breeding season; therefore,
relative to seasonally breeding king crabs, fewer
males would be sufficient for the breeding needs of
the population. If this is true, then minimum size
limits based on the criteria established for red and
blue king crabs may be unnecessarily conservative
for golden king crab.
Commercial harvest of king crabs is also restricted
to a legal fishing season specified for each species
in each area. Although economic or logistic factors
are considered when fishing seasons are established,
of primary importance is the timing of the breeding
and molting seasons. During the breeding season,
females molt while aggregated together with the
males (Powell et al. 1973); and if fishing were per-
mitted at this time, not only would females be caught
in greater numbers, they would also be injured by
the fishing gear. During and soon after the male
molting season, the recovery rate (ratio of recover-
able meat to total body weight) is low; and if fishing
were permitted at this time, the value of the crabs
would also be low. Since the breeding seasons tend
to occur in the late winter and early spring and the
male molting seasons occur in late spring, the fish-
ing seasons usually begin in the fall. For golden king
crab, however, there is no clear seasonality in breed-
ing; and adult males and females appear to be
spatially segregated throughout the year. Although
we lack sufficient data to determine if there is any
seasonality in male molting, it appears that there
is no compelling biological reason to restrict the
golden king crab fisheries to any particular time of
the year. Therefore, we believe that, at present,
fishing seasons should be determined primarily by
what is most convenient or beneficial to fishermen
and processors.
582
SOMERTON and OTTO: DISTRIBUTION AND REPRODUCTION OF GOLDEN KING CRAB
ACKNOWLEDGMENTS
We thank Peter Cummiskey, Steven Meyers, and
Kenneth Cronk (NMFS, Kodiak) for providing in-
valuable assistance in both field and laboratory data
collection; David Stanchfield (FV Morning Star), Joe
Wabey (FV American Eagle), Scott Bowlden (FV
Valiant), Edward Compton (FV Valiant), John
Atwell (RV Miller Freeman), and Edward Gelb (RV
Miller Freeman) for their cooperation and exper-
tise in the operation of the research vessels; Kevin
Bailey, James Balsiger, Nicholas Bax, Robert Fran-
cis, and Nancy Pola for providing helpful reviews
of the manuscript. In addition, we express our
gratitude to Dennis Peterson, Barry Collier and the
North Pacific Fishing Vessel Owner's Association
for arranging and supporting the charter of the FV
American Eagle.
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1983. The new king crabbing: How much harder can this
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Miller, R. J.
1976. North American crab fisheries: regulations and their
rationales. Fish. Bull., U.S. 74:623-633.
Nelson, R., Jr., R. French, and J. Wall.
1981. Sampling by U.S. observers on foreign fishing vessels
in the eastern Bering Sea and Aleutian Island region, 1977-
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Pereyra, W. T.
1966. The bathymetric and seasonal distribution, and repro-
duction of adult tanner crabs, Chionoecetes tanneri Rathbun
(Brachyura: Majidae), off the northern Oregon coast. Deep-
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1968. Distribution of juvenile tanner crabs, Chionoecetes tan-
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1970. Novye dannye o ravnoshipom krabe (New data on the
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SLIZKIN, A. G.
1974. Osobennosti raspredeleniya krabov (Crustacea, Deca-
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1980. A computer technique for estimating the size of sex-
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584
A MODEL OF THE DRIFT OF NORTHERN ANCHOVY,
ENGRAULIS MORDAX, LARVAE IN THE CALIFORNIA CURRENT
James H. Power1
ABSTRACT
The drift of northern anchovy, Engraulis mordax, larvae in the California Current to unfavorable offshore
areas may be an important factor contributing to larval mortality, and hence it may affect recruitment
and subsequent adult population size. A simulation model based on a finite-difference approximation to
the advection-diffusion equation was developed to aid in the study of larval anchovy drift. Model com-
ponents included the long-term mean geostrophic and wind-driven current velocities to 50 m depth, and
turbulent diffusion. The model predicted larval distributions in the Southern California Bight and off-
shore regions after 30 days of drift, and these distributions were used to assess the extent of cross-shore
and alongshore larval transport that occurs when spawning takes place at different locations, seasons,
and during times of increased offshore-directed Ekman transport.
Offshore transport was minimal in most simulations. Simulations of drift starting from the location
of peak spawning showed strongest seasonal effects, with currents during the season of peak northern
anchovy spawning (March) resulting in reduced offshore dispersal when compared with currents at other
times of the year. March currents also produced the greatest downshore (southeasterly) transport of
larvae, and strong seasonal currents, such as the nearshore, northwesterly flowing California Counter-
current, can greatly affect the alongshore 30-day larval distributions. Offshore directed Ekman trans-
port, associated with upwelling, does not strongly affect the drift of larvae in the nearshore region, but
large increases in overall Ekman transport, or extension of spawning into offshore regions, can result
in significant seaward transport of larvae out of the Southern California Bight.
The total population of northern anchovy, Engraulis
mordax, a common pelagic fish off the west coast
of North America, is comprised of three subpopula-
tions (Vrooman et al. 1981): northern (found north
of lat. 36°30'N); central (between lat. 29° and 38°N);
and southern (south of lat. 29 °N). The central sub-
population inhabits the Southern California Bight
region, and in recent times has exhibited substan-
tial changes in population biomass (e.g., Smith 1972).
Analysis of northern anchovy scales deposited in
sediments indicates that large northern anchovy
population fluctuations have also occurred in the
past few centuries (Soutar and Isaacs 1974). Histor-
ically the central subpopulation of northern anchovy
has supported a significant fishery (Messersmith and
Associates 1969; Sunada 1975; Stauffer and Charter
1982), and although the U.S. fishery has recently
declined, there is still a significant Mexican fishery.
The northern anchovy fishery, the recent and histor-
ical changes in anchovy population size, and the
fish's important role in the marine ecosystem all pro-
vide the motivation for studying the mechanisms
'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038; present address: Coastal Fisheries Institute, Center for
Wetland Resources, Louisiana State University, Baton Rouge, LA
70803-7503.
that may cause interannual variations in northern
anchovy stock size.
Such changes in stock size may be a consequence
of variations in the previous spawning stock size,
or they can also arise as a result of interannual dif-
ferences in mortality during prerecruit life history
stages (Rothschild et al. 1982). Because the egg and
larval stages have the highest mortalities, it seems
possible that processes affecting the relative mor-
tality during these stages can have a significant ef-
fect on subsequent recruitment. Two major causes
of larval mortality are starvation and predation
(Smith and Lasker 1978; Hunter 1981). A factor that
may contribute to these is larval drift. The northern
anchovy eggs and larvae, lacking adequate motil-
ity, can be involuntarily transported away from
nearshore spawning areas. It is the nearshore
regions in the Southern California Bight that most
frequently contain adequate food concentrations for
growth and survival of first feeding northern an-
chovy larvae (Lasker 1978, 1981).
Although eddies and other short-term mesoscale
features are important in the Southern California
Bight (Mooers and Robinson 1984; Simpson et al.
1984), the broad and relatively slow equatorward
flow termed the California Current is the dominant
feature in the region that persists on evolutionary
Manuscript accepted September 1985.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
585
FISHERY BULLETIN: VOL. 84, NO. 3
time scales. Hence, it seems plausible that northern
anchovy spawning strategies have developed in
response to the relatively predictable seasonal and
spatial trends in the California Current. Possible
relationships between time and location of fish
spawning and the currents off the west coast of
North America have been discussed by Parrish et
al. (1981). They noted that in the Southern Califor-
nia Bight the Ekman (wind-driven) currents are
generally diminished relative to other areas along
the coast. This reduced offshore transport is favor-
able for the retention of fish eggs and larvae.
However, some weak offshore directed Ekman
transport is consistently present in the Southern
California Bight year round (Nelson 1977; Parrish
et al. 1981; Bakun and Parrish 1982).
Smith (1972) analyzed historical records of north-
ern anchovy larval distribution in the Southern
California Bight and found that samples taken
farther offshore had a higher proportion of older lar-
vae than that of samples taken nearshore. Assum-
ing a uniform spatial and temporal distribution of
spawning, this result implied that a significant frac-
tion of northern anchovy eggs and larvae were
transported offshore after nearshore spawning.
Bailey (1981) found that the average distance off-
shore of Pacific hake, Merluccius productus, larvae
north of Point Conception was positively correlated
with offshore Ekman transport and that the magni-
tude of subsequent Pacific hake recruitment was
negatively correlated with offshore transport.
Hewitt and Methot (1982) compared the distribu-
tions of northern anchovy larvae sampled in 1978
and 1979 and found that the bulk of the larvae in
1979 were farther offshore than those in 1978 and
that mortality of 0-group northern anchovy was
greater in 1979 when compared with those spawned
in 1978. The year 1979 was one of enhanced upwell-
ing and colder temperatures (both concomitants of
offshore Ekman transport) relative to 1978.
The studies cited above suggest drift may play an
important role in larval ecology, but the conclusions
drawn from plankton sampling must be viewed with
caution. Inferences drawn from field collections
about the drift of larvae usually carry the assump-
tion that both northern anchovy spawning and lar-
val mortality were uniform in space and time,
because the time and distance scales involved largely
preclude synoptic sampling of eggs and larvae
throughout the region. Hence, only correlative ex-
planations for the observed distribution can be
made, and other causal factors affecting the larval
distribution may be hidden. For example, an obser-
vation of greater proportions of older larvae in off-
shore waters could also result from earlier spawn-
ing or greater early mortality (possibly coupled with
increased spawning activity) in those waters, and
not drift. Additionally, the mesoscale variability
present in the Southern California Bight and the
considerable patchiness of early and late larvae (due
to northern anchovy schooling behavior; Hewitt
1980, 1981a) further confound the conclusions
drawn from plankton samples and diminish the value
of interannual comparisons. Therefore, as an alter-
native to field studies, a simulation model of north-
ern anchovy drift in the California Current was
developed to help evaluate the role of drift in larval
ecology. The objective was to use the model to deter-
mine the effect of differences in northern anchovy
spawning location and time on the subsequent larval
distribution and to evaluate the effects on larval
distribution when offshore Ekman transport is in-
creased above its normal mean value.
METHODS
The drift simulation was based on the two-dimen-
sional (x,y) form of the advection-diffusion equation:
dF d
dt dx
U-K,?l\+ 3
vF
dx
dy
where F = the concentration of eggs and larvae;
u and v = current velocities in the respective x
and y directions; and
Kx and Ky = eddy diffusivity coefficients for the x
and y directions.
An analytical solution to this equation cannot be
evaluated relative to northern anchovy larval drift
in the California Current, although a numerical ap-
proximation that specifies larval concentration as
a function of location and time can be determined.
This was accomplished by approximating each of the
derivatives in the equation by weighted finite-
differences, so that the model was algebraically
formulated as the current and diffusivity-mediated
fluxes of larvae among geographic points in the
Southern California Bight. Apart from the assump-
tion that larvae continually maintained themselves
in surface waters, the northern anchovy were
assumed to be conservative and completely passive
drifters, i.e., no mortality or movement due to lar-
val swimming was incorporated into the model.
Details of the numerical methods used are presented
in Power (1984).
The geographic grid for the model was defined
586
POWER: MODEL OF NORTHERN ANCHOVY DRIFT
using the California Cooperative Oceanic Fisheries
Investigation (CalCOFI) coordinate system. The
CalCOFI grid is a regular coordinate system of
cross-shore "lines" and alongshore "stations". The
model and CalCOFI grids are oriented with respect
to the coast so that increasing station number
corresponds to increasing offshore distance and in-
creasing line number implies the downshore (south-
easterly) direction. Each line unit increment is
spaced 12 nm apart, and each station unit represents
4 nm. The grid for the model was defined to form
cells that were 37 km (20 nm) on a side, and the
fluxes of larvae were among grid ceil centers. Model
coverage was from CalCOFI lines 70 to 120, and ex-
tended offshore to CalCOFI station 120 (Fig. 1).
Unless northern anchovy utilize a strategy where-
by spawning is initiated in response to the presence
of an eddy or other short-term mesoscale features,
it can reasonably be expected that spawning time
and location have evolved partially in response to
predictable current features. For this reason,
seasonal currents based on interannual means were
used in the model. Northern anchovy spawning
behavior relative to eddies, etc., is presently un-
known, and there are persistent seasonal trends in
spawning, e.g., northern anchovy spawn through-
out the year, but March is typically the peak time
of spawning (Smith 1972; Methot 1981).
Geostrophic currents for the model were cal-
culated using the geopotential anomalies computed
by Lynn et al. (1982). Lynn et al. used CalCOFI data
collected between 1950 and 1978 to compute the
average geopotential anomaly relative to 500 m for
four seasonal periods (nominally January, April,
July, and October) at 175 locations in the Califor-
nia Current. Average geopotential anomalies were
computed for an additional 23 locations for this
study to augment the Lynn et al. (1982) coverage
125
120
115
35-
125
120
115
Figure 1.— Geographic grid used in the northern anchovy drift simulations, and the corresponding
CalCOFI line and station coordinate system. Lettered locations are starting points for simulation presented
in this paper. Mean geopotential anomolies (used for computing geostrophic currents) were calculated
for the locations indicated by dots (Lynn et al. 1982; this study).
587
FISHERY BULLETIN: VOL. 84, NO. 3
(Fig. 1). The top 50 m of the water column is the
predominant depth range of anchovy larvae
(Ahlstrom 1959), therefore mean anomaly values for
the surface and for 10, 20, 30, and 50 m of depth
were used in this study. The anomalies at each
standard depth were interpolated to model grid
nodes using the bivariate interpolation algorithm of
Akima (1978). Geostrophic current velocities normal
to each grid cell interface were computed for each
of the standard depths, and average geostrophic cur-
rent velocities were then calculated for a layer ex-
tending from the surface to 50 m.
Wind speed and direction data used in this study
were from the data base summarized and discussed
by Nelson (1977). The raw wind observations were
converted to surface wind stress (t) values using the
relation
where p
Cd
w
T = RCdW2
air density (1.22 kg m
drag coefficient; and
wind speed.
3);
The drag coefficient was computed as a function of
wind speed using the empirical relation of Amorocho
and DeVries (1980, 1981). The computed wind stress
vectors were partitioned by month of observation
and resolved into alongshore and cross-shore com-
ponents. A monthly mean wind stress component
for each model grid cell interface was then computed
by averaging the appropriate component of the
stress vectors in the 37 km by 37 km area bisected
by the grid cell interface. Total Ekman or wind-
driven transport in the direction 90° to the right of
the wind can be approximated by dividing the wind
stress by the Coriolis parameter (Neumann and Pier-
son 1965), and this calculation was performed for
the mean wind stress components. The mixed layer
depth in the California Current is seldom >50 m,
and is often <20 m in the Southern California Bight
during the summer (Husby and Nelson 1982). It was
assumed that Ekman transport occurring deeper
than 50 m was negligible, and the Ekman transport
values were converted to a mean wind-driven
velocity for the surface to 50 m layer by dividing
the transport by the 50 m layer thickness.
The final current velocities were calculated as the
vector sum of the seasonal geostrophic and appro-
priate monthly Ekman components. Vector addition
of the two components appears to be a reasonable
assumption (Parrish et al. 1981), and no compensa-
tion for redistribution of mass owing to sustained
winds was performed. The final seasonal current
fields for the simulations were January, March
(April geostrophic velocities plus March Ekman
velocities), July, and October currents.
Figure 2 illustrates the general trends in the
California Current for the January and March
seasons. This figure should be interpreted with cau-
tion. Apart from the large potential differences
between actual synoptic conditions and the average
pattern used in the simulations, the resultant vec-
tor for a cell was necessarily computed for Figure
2 by averaging the current components of oppos-
ing cell faces and then calculating the resultant. A
distortion is introduced wherever components on op-
posite faces of a cell differ in magnitude or sign, so
that Figure 2 best represents features of the Califor-
nia Current that are consistent over several model
grid cells. The California Current is evident as two
regions of intensified southeasterly flow at the left
margins and midlines of the plots. During all parts
of the year except spring, the current turns toward
shore at the southern end of the Southern Califor-
nia Bight. A northwesterly flow near the coast sub-
sequently forms the inshore portion of a large
cyclonic eddy (the Southern California Eddy; Owen
1980) that occupies most of the Southern Califor-
nia Bight. During most of the year part of this eddy's
northeasterly flow continues past Point Conception,
to form the California Countercurrent (Hickey 1979;
Fig. 2, January plot). In the spring the southeast-
erly flow of the California Current moves closer to
shore to obliterate the surface portion of the
Countercurrent (Fig. 2, March). Tsuchiya (1980, fig.
2) gives a clear picture of the seasonal inshore-
offshore movements of the California Current at
CalCOFI lines 90 and 93. Close to shore in the south-
ern half of the modeled region there is another
region of intensified southeasterly flow, most evi-
dent in the March current plot. Lynn et al. (1981)
provided detailed illustrations of the geostrophic
flow regimes used in the simulations, and Nelson
(1977) presented graphical representations of the
wind stress fields along the west coast of North
America. Hickey (1979) presented a comprehensive
review of seasonal and spatial variations of the
California Current and the possible driving mech-
anisms involved, and Owen (1980) reviewed the in-
cidence and ecological consequences of eddies in the
California Current system.
Two additional current fields were calculated in
order to assess the effects of increased offshore
directed Ekman transport on larval northern an-
chovy distribution. As mentioned earlier, the mean
wind stress is consistently directed downshore
during March in the modeled region, a condition
588
POWER: MODEL OF NORTHERN ANCHOVY DRIFT
MARCH
Figure 2.— Resultant mean current vectors for the normal January and the March seasonal current data used in this study. See text
for cautions concerning figure interpretation. Length of arrow indicating north direction corresponds to a current velocity of 10 cm/s.
producing offshore directed Ekman transport. Two
current fields were obtained by increasing the cross-
shore component of the mean March Ekman
velocities by the factors 1.5 and 3.0, and then com-
bining the April seasonal geostrophic and aug-
mented March Ekman velocities. Wind stress, and
hence transport, is proportional to the square of
wind speed. This means that roughly a 22% increase
in a downshore wind speed increases the corres-
ponding offshore directed Ekman transport by the
factor 1.5. A threefold increase in offshore Ekman
transport results from about a 77% increase in the
downshore wind speed. Bakun and Nelson (1976)
presented extensive statistical analyses of an
"up welling index" (defined as the offshore directed
component of Ekman transport) for the location lat.
33°N, long. 119°W (this point is very close to loca-
tion A used in the simulations; see below). Over an
annual cycle the mean upwelling index for this loca-
tion changes by at least a factor of two, with a rapid
increase in both mean and standard deviation dur-
ing the spring. The March mean index at this point
was about 50 t/s per 100 m of coastline with a stan-
dard deviation of roughly 80, hence upwelling at this
particular time and location can be highly variable.
Further, Bakun and Nelson (1976) found that en-
hanced or diminished upwelling persists on a
seasonal time scale, so incorporation in the model
of prolonged increased Ekman transport was not
unrealistic.
Diffusion was incorporated into the model solely
to parameterize subgrid scale mixing; including
larger scale and more ephemeral mixing processes
would obscure the broad seasonal trends the model
was intended to illustrate. The eddy diffusivity
parameter was computed using scale-dependent dif-
fusion formulae of Okubo (1976) and a regression
analysis of diffusion data presented by Okubo (1971).
The finite-difference representation of diffusion re-
quired the use of a pseudo-Fickian diffusivity coeffi-
cient, so the mean scale-dependent diffusivity for
the 37 km grid spacing (Kx = Ky = 101 m2/s) was
589
FISHERY BULLETIN: VOL. 84, NO. 3
used for all locations and all times in the model. The
numerical method incorporated diffusion as the
weighting factor coth [(uh)/(2K)] for the flux at each
grid cell interface, where u is the current velocity
at the interface and h is the 37 m grid spacing (see
Power 1984 for further details). Hence, diffusion
becomes important in regions of low current
velocity, and at higher velocities diffusion is less im-
portant and advection dominates the flux. For the
current velocities in most of the modeled region, the
above hyperbolic cotangent function is usually
evaluated to a magnitude near unity, making the
contribution of turbulent transport to larval drift
minimal relative to advective (current velocity)
transport.
Simulations were carried out by starting an ini-
tial point source of northern anchovy eggs or larvae
at various locations historically known to be larval
anchovy habitat (Hewitt 1980). Examples of simula-
tions for four starting locations (Table 1; Fig. 1),
which are representative of the overall patterns pro-
duced by the simulations, are presented here. The
four locations will be referred to in the text by their
letter designations indicated in Figure 1 and Table
1. Northern anchovy larvae begin to school at about
27 d (Hunter and Coyne 1982); therefore larval
distributions after 30 d of drift are presented.
Thirty-d-old larvae are also rapidly increasing their
"patchiness" (Hewitt 1981a), indicating that they
could then exert significant control over their posi-
tion. The time step in the simulations was 1 d.
Results from a simulation using the actual northern
anchovy egg distribution found in 1982 as the ini-
tial condition can be found in MacCall (1983).
Table 1.— Geographic and CalCOFI coordinates of start-
ing locations for simulations presented in this paper. Letter
designation corresponds to the same locations in Figure 1 .
Starting
location
Coordinates
CalCOFI
Lat. N
Long. W
Line
Station
A
B
C
D
33°08.4'
32°54.1'
31°59.3'
32°14.1'
118°51.4'
117°47.3'
118°05.4'
119°09.2'
89.17
92.5
95.83
92.5
42.5
32.5
42.5
52.5
Northern anchovy larval concentrations in the
contour plots are relative to starting concentration;
the unitless contour value of 10~2 represents a lar-
val concentration two orders of magnitude below the
starting concentration, and only concentrations
down to 10 "7 are illustrated. Larvae were per-
mitted to be advected out the borders of the modeled
area, except for the border along the coast. Grid cells
bordering the Santa Barbara Channel (at about lat.
34°N, long. 120°W; Fig. 1) between the Channel
Islands and Point Conception were open, and lar-
vae advected into this region were considered to be
lost from the system. Larvae were not permitted
to be transported across any of the islands in the
modeled region. Because March is the peak spawn-
ing time of northern anchovy, the effects of different
starting locations on the 30-d larval distributions
during March conditions will be presented first. The
effects of spawning in different seasons and en-
hanced offshore Ekman transport during March will
then be presented for comparison. The simulation
results nominally represent larval northern anchovy
distributions, but the results also apply to any plank-
tonic species that begin drift at the same locations
and maintain themselves in the top 50 m of the
California Current.
The overall extent of onshore-offshore and along-
shore transport was of major interest in this study.
A convenient way of summarizing the simulated
larval distributions relative to their cross-shore
distribution was to sum all larval concentrations in
the cells having the same CalCOFI station coordin-
ates. These sums were converted to percentages of
the total number of larvae at 30 d, and the cumula-
tive percentage of larvae present as one progressed
offshore was plotted versus CalCOFI station coor-
dinates. A similar procedures using CalCOFI line
coordinates was done to summarize alongshore
transport.
RESULTS
Effects of Starting Location,
Normal March Currents
Northern anchovy larvae that began drift at loca-
tion B, near the coast, were transported downshore
by March currents (Fig. 3B). This was an effect of
the nearshore southeasterly current (Fig. 2), and
because of this flow only 15% of the larvae were at
or upshore of the starting location after 30 d of drift
Figure 3.— Distribution of northern anchovy larvae after 30 d of
drift in March currents. Letter designation corresponds to a simula-
tion with northern anchovy begun at the corresponding lettered
location in Figure 1 and Table 1; starting location is marked in
this and subsequent contour plots with asterisks. Locations A and
C share the same CalCOFI station coordinate; points B and D have
the same CalCOFI line coordinate. Concentration contour inter-
vals are proportions of the starting concentration, decreasing in
order of magnitude steps. Tic marks around perimeter are at whole
degrees of latitude and longitude; dots are at intervals of 3.33
CalCOFI line units from lines 70 to 120 and intervals of 10 station
units offshore to station 120 (i.e., every 74 km).
590
POWER: MODEL OF NORTHERN ANCHOVY DRIFT
591
FISHERY BULLETIN: VOL. 84, NO. 3
(Fig. 4). The alongshore distribution of larvae below
the starting point was quite uniform, and the lower
larval concentrations had reached the southern
border of the modeled region (CalCOFI line 120).
Dispersal offshore was minimal, and a majority of
the larvae lay in a band near the coast with about
equal proportions inshore and offshore of the start-
ing point; 92% of the larvae were on or inshore of
CalCOFI station 37.5. After initial southeasterly
transport, some larvae were transported in an off-
shore, southwesterly direction.
Extensive downshore transport also occurred to
northern anchovy larvae begun at location C, and
in fact only 3% of the larvae remained at or upshore
of the starting location after 30 d of drift (Figs. 3C,
4). The larvae begun at point C were also concen-
trated in a narrow band along the coast, but unlike
those started at point B most of the larvae begun
at C moved inshore of the starting location after 30
d of drift.
Northern anchovy larvae begun at the offshore
location D showed much less extensive downshore
transport than those begun at B or C (Figs. 3D, 4).
Only 10% of the larvae remained at or upshore of
the starting point, but 86% of the total remained
at or between CalCOFI line 92.5 (location C's line
coordinate) and line 102.5, a span of 222 km. Most
larvae were inshore of location D, and the cross-
shore distribution was slightly more uniform than
those begun farther inshore. Starting point D's
distance from the coastline permitted the slightly
broader cross-shore distribution.
Larvae begun at location A showed an alongshore
cumulative percentage distribution after 30 d of drift
which was similar to that of larvae that begin drift
at point D, although it was displaced farther upshore
(Fig. 4). Location A produced the greatest percent-
age of larvae remaining at or upshore of the start-
ing location, and there is a small patch of high
(10 _1) larval concentrations present at the starting
location (Fig. 3A). This reduced dispersal of larvae
begun at A also produced the strongest cross-shore
gradient of larvae. A majority of the larvae were
again on or inshore of the starting location after 30
d of drift.
In summary, the distributions of northern anchovy
larvae that began drift at locations A through D and
that were produced by March currents were formed
as relatively strong cross-shore gradients, so that
the 30-d distributions were bands (ca. 100 km wide)
parallel to the coast. The results of starting larvae
at locations A, C, and D were that more than 85%
of the larvae were inshore of the starting location
after 30 d of drift. Larvae that began drift at loca-
STATION
120 105 90 75 60 45 30
100-
120 115 110 105 100 95 90 85 80 75 70
LINE
Figure 4.— Cumulative percentages of northern anchovy larvae
after 30 d of drift, progressing offshore (increasing CalCOFI sta-
tion number) and downshore (increasing CalCOFI line number),
for the four starting locations under March current conditions.
Cross symbols are at the starting location's corresponding
CalCOFI line or station coordinate. Distance between tic marks
on the abscissae is equivalent to a distance of 111 km. Note that
a steep curve implies a compact distribution of larvae, while more
gradual slopes imply more widely dispersed larvae.
tions B and C were extensively carried downshore
of the starting location. Most of the larvae that
started at points A and D also moved downshore
from those locations, but the bulk of the larvae were
not as widely dispersed from the starting location
as those begun at points B and C.
Effects of Seasonal Current Fields
on Larval Distribution
The distributions of northern anchovy larvae
started at the same location but using different
seasonal current regimes appear very different to
the eye (Figs. 3, 5-7). Part of this effect is real, but
part is also due to displacement of the contours for
the lower larval concentrations (e.g., 10~7), which
represent few larvae. The cumulative percentage
plots (Fig. 8) indicate that, when summarized on a
model-wide basis, the overall cross-shore distribu-
tions of larvae begun at locations B, C, and D were
not greatly different when currents from the four
seasonal periods were used in the simulations. A
fixed distance offshore there were some large differ-
ences in the cumulative percentages among seasons
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POWER: MODEL OF NORTHERN ANCHOVY DRIFT
"7 . V I
Figure 5.— Distribution of northern anchovy larvae after 30 d of drift in normal July currents.
593
FISHERY BULLETIN: VOL. 84, NO. 3
Figure 6.— Distribution of northern anchovy larvae after 30 d of drift in normal October currents.
594
POWER: MODEL OF NORTHERN ANCHOVY DRIFT
Figure 7.— Distribution of northern anchovy larvae after 30 d of drift in normal January currents.
595
FISHERY BULLETIN: VOL. 84, NO. 3
STATION
120 105 90 75 60 45 30
100
STATION
120 105 90 75 60 45 30
120 115 110 105 100 95 90 85 80 75 70
LINE
STATION
120 105 90 75 60 45 30
100-
'120 115 110 105 100 95 90 85 80 75 70
LINE
STATION
120 105 90 75 60 45 30
100-
~120 115 110 105 100 95 90 85 80 75 70
LINE
"120 115 110 105 100 95 90 85 80 75 70
LINE
Figure 8.— Cumulative percentage plots of northern anchovy larval concentrations after drift in the four seasonal current regimes. Letter
designation corresponds to starting locations indicated in Figure 1 and Table 1.
for larvae begun at the same location, but a com-
parable percentage was usually present a short
distance away, i.e., most curves in Figure 8 are
closely spaced on the CalCOFI station abscissae.
Most larvae begun at the offshore location D moved
inshore regardless of season, and the seasonal dif-
ferences were in the relative extent of inshore move-
ment, the maximum occurring during July. In all
simulations the cross-shore distributions of larvae
formed strong gradients, regardless of season.
Starting location A is within the Southern Califor-
nia Bight proper, the region that most consistently
has high larval concentrations of northern anchovy
(cf. Hewitt 1980). Larval distributions started at
location A did exhibit notable seasonal differences
in their 30-d cross-shore distributions, with the
greatest offshore dispersal occurring during July
(Figs. 5A, 8A), and the largest inshore movement
596
POWER: MODEL OF NORTHERN ANCHOVY DRIFT
occurring during March current conditions (Figs.
3A, 8A). January and October were intermediate
between these two extremes. In all cases the cross-
shore gradients of larvae were strong.
In contrast, the alongshore distributions of larvae
differed markedly when the simulations were done
with currents from the four seasonal periods. Vir-
tually all larvae were carried upshore of starting
location A by the California Countercurrent in the
January simulation (Figs. 7A, 8A), but when the
model was run using March currents, a majority of
the larvae were downshore of point A after 30 d of
drift (Fig. 3A). The July and October simulation
results for point A seemed to indicate an annual pro-
gression between the March and January extremes
(Fig. 8A).
The seasonal differences in the overall alongshore
distributions were even more dramatic for northern
anchovy larvae begun at locations B and C. The
uniform downshore distribution produced by March
currents differed from the distributions formed in
all other seasons. Larvae begun at location B were
all transported upshore of the starting location dur-
ing October current conditions (Fig. 6B). When
January currents were used (Fig. 7B), the upshore
movement had lessened, so that only 62% of the
larvae were at or upshore of location B, and the lar-
vae were more evenly distributed along the coast
(Fig. 8B). March currents yielded the greatest down-
shore movement, and the July distribution (Fig. 5B)
was intermediate between that produced by March
and October conditions, with the alongshore
gradient of larvae again steepening. The changes
on an annual basis between upshore, then down-
shore transport were similar for larvae begun at
location C, except that the July current conditions
produced the greatest upshore transport (Figs. 5C,
8C); March again produced the maximum down-
shore transport for larvae begun at point C (Fig.
3C). Larvae begun at location C formed a relative-
ly compact distribution after 30 d of drift in the
January currents (Fig. 7C).
The overall alongshore distributions of northern
anchovy larvae that started drift at point D ap-
peared to be least influenced by seasonal changes
in the currents, although March conditions again
produced the greatest transport downshore of the
starting point (Fig. 3D), with July currents again
yielding the greatest upshore transport (Fig. 5D).
January currents also produced a very compact
distribution of larvae started at location D, similar
to that of larvae begun at point C.
In summary, only northern anchovy larvae begun
at location A appeared to have notable differences
in their model-wide, cross-shore distributions after
30 d of drift. Larvae begun at all four locations did
have substantial seasonal differences in their along-
shore distributions, with March currents consistent-
ly producing the greatest downshore dispersal. The
least downshore dispersal occurred during January,
October, July, and July current conditions for larvae
started at locations A, B, C, and D respectively.
January currents generally seemed to produce the
most compact 30-d distributions of larvae (least
dispersal).
Effects of Increased Offshore
Ekman Transport, March Currents
Increasing the March cross-shore Ekman trans-
port by a factor of 1.5 had little effect on the 30-d
distributions of northern anchovy larvae begun at
locations B and C (Fig. 9); these curves are also
closely spaced on the CalCOFI station abscissae. In-
creasing the average or "normal" offshore Ekman
component by a factor of three produced more
noticeable changes in the cross-shore distributions
of larvae begun at points B and C, but this effect
was not substantial; the contours representing the
lower concentrations extended far offshore (Fig.
10B, C), but the higher concentration contours,
which delimit the majority of the larvae, were not
greatly displaced from those of normal March cur-
rents (Fig. 3B, C). This is also evident in the cum-
ulative percentage, curves.
In comparison, northern anchovy larvae begun at
locations A and D underwent about the same in-
crease in offshore dispersal with a 1.5 x offshore
directed Ekman component increase as those begun
at points B and C did with the 3 x offshore Ekman
increase (Fig. 9). When the offshore directed Ekman
transport was increased to three times its normal
mean value, the effects on larvae begun at points
A and D were substantial. A majority of the larvae
were carried offshore of starting locations A and D,
and a large fraction were transported a significant
distance (Fig. 10 A, D), well seaward of the South-
ern California Bight. The increase in offshore
Ekman transport also noticeably affected the along-
shore distributions of larvae begun at locations A
and D (Fig. 9). The overall pattern of alongshore
distribution is similar to that produced by the nor-
mal mean conditions, but the larvae were general-
ly farther downshore.
DISCUSSION
Models have inherent assumptions and simplifica-
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FISHERY BULLETIN: VOL. 84, NO. 3
STATION
120 105 90 75 60 45 30
_1 1 I I I L
STATION
120 105 90 75 60 45 30
100-
120 115 110 105 100 95 90 85 80 75 70
LINE
120 115 110 105 100 95 90 85 80 75 70
LINE
STATION
120 105 90 75 60 45 30
STATION
120 105 90 75 60 45 30
100"
120 115 110 105 100 95 90 85 80 75 70
LINE
120 115 110 105 100 95 90 85 80 75 70
LINE
Figure 9.— Cumulative percentage plots of northern anchovy larval concentrations after 30 d drift in the three March Ekman current
regimes ("normal" or long-term mean, 1.5 x offshore directed Ekman transport, 3x offshore directed Ekman).
tions, and thus approximate what occurs in nature.
The geostrophic current information, while some of
the best available, nonetheless constrained the
spatiotemporal resolution of this model, and incor-
porating Ekman transport required several assump-
tions. Further, there can be considerable interannual
variability in the modeled region (Mooers and Robin-
son 1984; Simpson et al. 1984), and presumably the
model is of "average" conditions and cannot be
representative of any specific year; I felt that in-
cluding such variability (assuming adequate data
were available) would complicate the results without
significantly contributing to biological insight. An
Figure 10.— Distribution of northern anchovy larvae after 30 d
of drift in March currents with three times the normal offshore
directed Ekman transport.
598
POWER: MODEL OF NORTHERN ANCHOVY DRIFT
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FISHERY BULLETIN: VOL. 84, NO. 3
additional confounding factor is the lack of biological
information in the model; consistent larval behavior
patterns (e.g., diurnal vertical migrations) and
spatially heterogeneous mortality could produce
distributional patterns differing from those pre-
sented here. In spite of these caveats, the simula-
tions do demonstrate that variations in northern
anchovy spawning location and time, and changes
in the magnitude of offshore directed Ekman trans-
port, can have significant consequences for the
subsequent larval distribution. By inference, these
changes in distribution can result in increased or
reduced larval mortality, and ultimately affect adult
northern anchovy population size.
Offshore transport was not significant in the sim-
ulations done with the unaugmented or "normal"
March (seasonal April geostrophic + March Ekman)
currents. A majority of the northern anchovy lar-
vae that began drift at the four starting locations
were inshore of their starting points after 30 d of
drift, and the cross-shore distributions indicated that
most larvae occupied a relatively narrow range of
distances close to shore. Mais (1974) and Methot
(1981) reported that most juvenile northern anchovy
occupy inshore areas in the fall, and the model in-
dicates that this inshore movement could be facil-
itated by passive drift. As mentioned earlier, the
consensus is that nearshore regions provide more
hospitable food conditions for the northern anchovy
larvae. Lasker (1978, 1981) summarized the results
of surveys of larval food distributions in the South-
ern California Bight. His figures indicate that suit-
able larval food concentrations decline rapidly as one
progresses offshore. O'Connell (1980) reported the
results of a survey for starving northern anchovy
larvae in the Southern California Bight, the degree
of starvation being defined by histological criteria.
He found apparently healthy larvae at locations as
far as about 250 km offshore (at lat. 32°30'N, long.
120°W), where model concentrations were <10~7
after 30 d in all March simulations except for lar-
vae begun at A, where they were <10~4. Despite
the good condition of these offshore larvae, the
simulation results indicate a low likelihood of their
being recruited to the nearshore juvenile population.
The low offshore larval concentrations will also
hinder the development of schooling (Hewitt 1981a).
The minimal offshore transport situation found in
the March current simulations was also generally
true when simulations were done using currents
from other seasons, except for northern anchovy lar-
vae begun at location A. This point is the most in-
terior starting location within the Southern Califor-
nia Bight proper and is primary northern anchovy
spawning habitat (Hewitt 1980) and where seasonal
changes in the currents are especially important
(Tsuchiya 1980). Spring is a time when currents in
the Southern California Bight are not as well
organized as other times of the year, and the
Southern California Eddy is often absent (Hickey
1979; Owen 1980). It is interesting that currents
during March, the peak spawning period, produced
the least offshore transport of larvae begun at loca-
tion A when compared with other seasons, even
though March is the time of greatest overall Ekman
transport (Bakun and Nelson 1976). There is signifi-
cant spawning in January (Methot 1981), and the
January simulations also had reduced dispersal of
larvae. The model results support the hypothesis of
Parrish et al. (1981) that northern anchovy spawn-
ing in the Southern California Bight do so at a time
and place that minimizes offshore transport of eggs
and larvae.
It is clear that the overall 30-d alongshore distribu-
tions of northern anchovy larvae produced by
normal March currents depended largely on the
spawning location's proximity to the well-defined
southeasterly current present near the coast in the
southern half of the modeled region. Larvae that
started drift near this current underwent extensive
downshore transport. Larvae begun farther into the
Southern California Bight (location A), and farther
offshore (location D), were also transported down-
shore, but to a much lesser extent. This again con-
firms the role of the Southern California Bight as
an area where minimal transport of spawning
products takes place. The southwesterly, offshore
transport that occurred in many of the simulations
at the southern margin of the modeled region
(between CalCOFI lines 110 and 120) is consistent
with the evidence that this region forms a faunal
boundary between species of the Southern Califor-
nia Bight and those of Baja California to the south,
and that this faunal boundary is created by current
patterns (Hewitt 1981b). This is also a region of in-
creased surface convergence (Parrish et al. 1981).
The extent of alongshore transport was marked-
ly different for northern anchovy larvae begun at
the same starting location when currents from the
different seasons were used. Depending on start-
ing location, seasonal changes in currents could pro-
duce almost complete reversals between predom-
inantly upshore or downshore transport. March
currents consistently produced the greatest down-
shore transport. These effects were due to the pres-
ence or absence of the Southern California Eddy and
the Southern California Countercurrent. Because
the Southern California Countercurrent is present
600
POWER: MODEL OF NORTHERN ANCHOVY DRIFT
year-round, except during peak spawning in the
spring, it is clear that the relationship between the
time of northern anchovy spawning and the time
that this countercurrent diminishes is critical. The
simulations indicated that eggs and larvae from
early spawning (i.e., January) are carried upshore
into the Santa Barbara Channel and north of Point
Conception, while those from later spawning
(March) move in the opposite, southeasterly direc-
tion. The sizes and birth dates of juveniles collected
in the fall of 1978 and 1979 were in accordance with
this pattern. Methot (1981) reported that juvenile
northern anchovy collected during both fall seasons
in the northern portion of the Southern California
Bight had birth dates (as determined from daily
growth increments in otoliths) in the preceding
months of December and January, and these fish
were generally larger than those collected farther
to the south. The northern anchovy collected in the
south had predominantly February and March birth
dates. It may be that the northern group, contain-
ing fish from early spawning, were advected to the
north by the Southern California Countercurrent
and that the southern group of fish from late spawn-
ing were produced when the surface countercurrent
had diminished. Future studies of the transport and
distribution of northern anchovy larvae or other
planktonic species in the Southern California Bight
should incorporate as much information as is avail-
able on the presence and magnitude of the South-
ern California Countercurrent and the Southern
California Eddy.
Nearshore winds in the Southern California Bight
are relatively weak, and downshore wind speeds
generally increase farther offshore (Bakun and
Nelson 1976; Nelson 1977; Dorman 1982). The
implication, in terms of offshore transport, is that
larvae closest to shore are affected least by offshore
transport, while those farther offshore experience
a much greater impact. Thus the areal extent of
northern anchovy spawning interacts with offshore
Ekman transport; in years when most northern an-
chovy spawn close to shore there will be decreased
offshore transport, because of weak inshore winds,
than in years when northern anchovy spawn farther
offshore. The impact on the products of offshore
spawning will depend on the magnitude of the winds
in the offshore areas in each particular year. North-
ern anchovy larvae that began drift farthest north
in the Southern California Bight (location A) and at
the more offshore location (D) were most affected
by increases in offshore directed Ekman transport,
indicating southerly and inshore spawning are best
for reduced dispersal in March. Hewitt and Methot
(1982) stated that the area of northern anchovy
spawning was more compact and more northerly in
1978 than in 1979. Survival of young larvae was
about the same in both years, indicating that early
mortality from starvation and predation was not
substantially different in the two years. Survival
through the juvenile stage was greater in 1978 than
in 1979, however, and Hewitt and Methot (1982)
cited increased offshore transport in 1979 as a possi-
ble reason.
Superimposed on the effects of spawning location
is the interaction between the increase in downshore
wind speeds (offshore directed Ekman transport) as
one progresses offshore and the magnitude of inter-
annual variations in the wind speeds. In the simula-
tions the effects of the 3 x increase in Ekman trans-
port were substantially greater than those of the
1.5 x increase. The 1.5 x change was not a great
enough increase to carry many northern anchovy
larvae into offshore regions of higher, offshore
directed Ekman transport. The inshore 3 x increase
carried a greater fraction of larvae farther offshore,
and the 3x increase in the offshore region subse-
quently operated on a greater proportion of the
larval population. Thus there was an interaction
between enhanced offshore directed Ekman trans-
port in the nearshore area and increased Ekman
transport farther offshore, the two of these acting
together to produce the extensive drift evident in
the simulation results. Years in which downshore
winds increase in only the inshore or the offshore
regions would not produce as much overall offshore
dispersal. Bakun and Nelson's (1976) statistical
analyses of the "upwelling index" indicates that pro-
longed increased Ekman transport is feasible,
although the 3 x condition would probably be a par-
ticularly bad year. It should also be noted that
Ekman transport was incorporated into the model
as acting uniformly on the 50 m surface layer, and
presumably the model depicts the drift of "average"
larvae. Larvae that remain near the surface or at
50 m would undergo greater or lesser transport,
respectively. Alternatively, it is known that winds
in the Southern California Bight have a strong diur-
nal periodicity (Bakun and Nelson 1976; Dorman
1982), and a diurnal vertical migration coupled with
diurnal changes in the winds could significantly alter
larval drift.
In summary, the simulation results indicated that
seaward dispersal of northern anchovy larvae is
generally small, but that seasonal effects are strong-
est in the area of peak spawning (location A) and
that March spawning at this point minimizes off-
shore dispersal. Spawning at locations or times near
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FISHERY BULLETIN: VOL. 84, NO. 3
well-defined currents, such as the California
Countercurrent, can produce major changes in
larval distribution, and consequently may affect lar-
val survival. The effect of offshore directed Ekman
transport on the larval population depends on the
areal extent of northern anchovy spawning, and the
spatial distribution of any changes in wind stress
and subsequent Ekman transport; an increase in
Ekman transport in both the inshore and offshore
regions will act together to produce maximum off-
shore dispersal.
ACKNOWLEDGMENTS
This work was done while the author held a Na-
tional Research Council Research Associateship. I
thank Reuben Lasker and John Hunter for their
hospitality and advice, as well as for the opportu-
nity to conduct this research. Larry Eber and Craig
Nelson were instrumental in providing dynamic
height and wind speed data, without which this work
could not have been done. I also thank Andy Bakun,
Roger Hewitt, Ron Lynn, Alec MacCall, Rick
Methot, Bob Owen, Dick Parrish, and Paul Smith
for their stimulating discussions, advice, and review
of this work. This manuscript was revised while the
author held a CIMAS (Cooperative Institute for
Marine and Atmospheric Sciences) postdoctoral
fellowship at the University of Miami, and this sup-
port is gratefully acknowledged.
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SOUTAR, A., AND J. D. ISAACS.
1974. Abundance of pelagic fish during the 19th and 20th cen-
turies as recorded in anaerobic sediments off the Califor-
nias. Fish. Bull., U.S. 72:257-273.
Stauffer, G. D., and R. L. Charter.
1982. The northern anchovy spawning biomass for the 1981-
82 California fishing season. Calif. Coop. Oceanic Fish. In-
vest. Rep. 23:15-19.
Sunada, J. S.
1975. Age and length composition of northern anchovies,
Engraulis mordax, in the 1972-73 season California anchovy
reduction fishery. Calif. Fish Game 61:133-143.
Tsuchiya, M.
1980. Inshore circulation in the Southern California Bight,
1974-1977. Deep-Sea Res. 27A:99-118.
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.
603
PARASITES OF BENTHIC AMPHIPODS: DINOFLAGELLATES
(DUBOSCQUODINIDA: SYNDINIDAE)
Phyllis T. Johnson1
ABSTRACT
During a 2V2-yr survey, 13 species of benthic amphipods collected from the continental shelf of the north-
eastern United States were found infected by dinoflagellates. Prevalences ranged from <1% to 67%,
depending on amphipod species, time, and place of collection. The parasites are assigned to the order
Duboscquodinida, family Syndinidae, based on similar life histories and a similar kind of mitosis ("mitose
syndinienne"). Two types of organisms were involved, both apparently more closely related to
Hematodinium Chatton and Poisson than to other described syndinids. Morphology and development
of the parasites and host-parasite interactions are discussed. A cytochemical method used to determine
presence or absence of basic nuclear proteins was strongly positive for basic proteins in spores and
prespores but negative in most other stages. A few spores in four infections possessed a distinct flagellum,
but in the absence of living material, shape of spores and whether they were biflagellate could not be
determined. With three possible exceptions in the group of 303 infections studied, the syndinids were
not recognized as foreign by their hosts, and in joint infections of syndinids and fungi, only the fungi
were being attacked by host hemocytes. High prevalences in certain of the amphipod species suggest
that the syndinids might be population regulators in these species.
This paper is one of three that describe and discuss
the more common parasites found in populations of
benthic amphipods of the continental shelf of the
northeastern United States. The other papers con-
cern microsporidans and ciliates (Johnson 1985,
1986).
Because my observations on the parasites dis-
cussed in this paper were based on examination of
histological sections, I could not determine whether
spores were typical "dinospores". However, agree-
ment with other developmental stages of well-
studied species of syndinids from copepods and an
amphipod, and the nuclear type, indicates that the
parasites of benthic amphipods are related to species
currently placed in the Syndinidae, order Dubosc-
quodinida (sensu Chatton 1952 and Cachon 1964).
Previously described syndinids occur intracellular-
ly in radiolarians and in copepod and shrimp eggs
(Chatton 1952; Stickney 1978) and extracellu-
larly in the hemocoel of copepods, an amphipod,
and portunid and cancrid crabs (Chatton and Pois-
son 1931; Chatton 1952; Manier et al. 1971;
Newman and Johnson 1975; MacLean and Ruddell
1978).
The relationship of the Duboscquodinida to free-
living dinoflagellates is in doubt (Cachon 1964; Ris
and Kubai 1974; Siebert and West 1974; Hollande
1975; Loeblich 1976; Herzog et al. 1984). Lacking
a definitive consensus, the parasitic protists dis-
cussed here are provisionally referred to the Dino-
flagellata.
The data presented and discussed in this paper
show that species of syndinids are probably ubiqui-
tous hemocoelic parasites of benthic and epibenthic
amphipods, and may be population regulators in
some species.
METHODS
The data are based on material collected during
monitoring surveys carried out over a 2V2-yr period
by the Northeast Fisheries Center, National Marine
Fisheries Service. The 35 stations where benthic am-
phipods were collected during the surveys are shown
in Figure 1. Amphipods were sampled during 11
cruises, but not all stations were visited on each
cruise, so that stations were sampled from 1 to 10
times each during the survey. A Smith-Mclntyre2
grab and occasionally an epibenthic sled or scallop
dredge were used to obtain the samples. The 11 sta-
tions indicated by solid circles on Figure 1 had the
most consistent and numerous populations of am-
phipods, and were sampled at least five times each.
They yielded the majority of data presented here.
Amphipods were preserved in 10% seawater
Formalin. Up to 30 individuals of each species pres-
'Northeast Fisheries Center, National Marine Fisheries Service,
NOAA, Oxford, MD 21654.
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Manuscript accepted October 1985.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
605
FISHERY BULLETIN: VOL. 84, NO. 3
50 100 150
KILOMETERS
Project on a'tei IWXjpi 1965 I
68°
tf C NMFS Sano, ►
Figure 1.— Benthic stations where gammaridean amphipods were sampled during the survey.
ent in a sample, and sometimes more, depending on
numbers present, were prepared for histological
study. Details of collecting procedures and histo-
logical preparation of the amphipods are given by
Johnson (1985). Sections were cut at 6 ^m. Stain-
ing methods included Harris' hematoxylin and eosin
(H&E), the Feulgen reaction, and Alfert and Gesch-
wind's (1953) fast-green method for demonstration
of basic nuclear proteins. Harris' hematoxylin and
eosin is specified because this combination stains
nuclei of the parasites purple during certain stages.
Other hematoxylin solutions, used with eosin, will
not necessarily impart the same distinct purple
color. Unless otherwise indicated, references to
staining properties of the organisms are to H&E-
stained specimens.
OBSERVATIONS
Thirteen amphipod species were infected with syn-
606
JOHNSON: PARASITES OF BENTHIC AMPHIPODS
dinids (Table 1). The organisms occupied the
hemocoel and morphologically were most like Hema-
todinium perezi Chatton and Poisson, which was
described from European portunid crabs. There
were two distinct types, based on morphology and
development. There is not enough information about
the life history stages of Hematodinium to warrant
assigning either or both types to that genus, and
they are identified casually in this paper as "Type
A A" and "Type AV" (Table 2). The Type AA forms
were similar in all the amphipod species they in-
fected, but there was variation in forms assigned
to Type AV, and probably more than one species was
involved.
Host and Geographic Distribution
Juvenile and mature amphipods of both sexes
were attacked. Only Type AA was found in Am-
pelisca agassizi (Judd), Byblis serrata Smith, and
Table 1 .—Amphipod species infected with Type AA and Type AV parasites.
Species of amphipod
Type of
parasite
Prevalence
positive stations
(%)
Prevalence
all stations
(%)
Ampelisca agassizi (Judd)
Byblis serrata Smith
Harpinia propinqua Sars
Ampelisca vadorum Mills
Ampelisca verrilli Mills
Casco bigelowi (Blake)
Leptocheirus pinguis (Stimpson)
Melita dentata (Kr0yer) s. lat.
Monoculodes edwardsi Holmes
Protohaustohus wigleyi Bousfield
Phoxocephalus holbolli Krflyer
Rhepoxynius epistomus
(Shoemaker)
Unciola species (probably all
U. irrorata Say and U. inermis
Shoemaker)
AA
7 (101/1468)
4 (101/2403)
AA
14 (24/170)
8 (24/316)
AA1
18 (3/17)
3 (3/116)
AV
41 (74/181)
17 (74/448)
AV
18 (7/38)
15 (7/48)
AV
67 (6/9)
10 (6/60)
AV
4 (7/163)
0.8(7/913)
AV
8 (1/12)
2 (1/44)
AV
27 (25/93)
23 (25/110)
AV
20 (1/5)
0.9 (1/110)
AV
27 (10/37)
14 (10/73)
AA and AV
20 (7/35)
3 (7/249)
AA and AV
9 (37/404)
3 (37/1365)
1 Parasites in two of the infections may not be either Type AA or Type AV.
Table 2. — Main characteristics of Type AA and Type AV.
Stage Characteristic
Type AA
Type AV
I Nuclear diameter
<3 to >5 \im
2.5 to 3 ^m
Nuclear color
Blue or purple
Purple
Chromosomes
Usually condensed
Not condensed
Plasmodia
Present, small
Present, small
Single cells
Common
Absent or uncommon
Cytoplasm
Scanty
Abundant, faintly
fibrous
IA Dense bodies
Not present
Present, <2 ^m in
diameter
Nuclear diameter
—
2.5 to 4 film
Nuclear color
—
Purple
Plasmodia
—
Present, small
Single cells
—
Present
II Nuclear diameter
4 to 5.5 ^m
3 to 4 ^m
Nuclear color
Purple
Purple
Chromosomes
Indistinct, partly
Distinct, partly
condensed
condensed
Plasmodia
Uncommon, small
Very rare
Cytoplasm
Vacuolate
Homogeneous
III Nuclear diameter (spore)
2.5 to 3 urn
<2 urn
Nuclear color (spore)
Deep blue
Deep blue
Chromosomes (spore)
Always condensed
Always condensed
Cytoplasm (spore)
Scanty
Scanty
Plasmodia
Absent
Present
Nuclear diameter
—
3.5 fjm
(Plasmodia)
Nuclear color (Plasmodia)
—
Purple
607
FISHERY BULLETIN: VOL. 84, NO. 3
Harpinia propinqua Sars. Both Types AA and AV
occurred in Rhepoxynius epistomus (Shoemaker) and
Unciola species (U. irrorata Say and U. inermis
Shoemaker), and only Type AV occurred in the re-
maining species (Table 1). Both types of syndinids
were present in Unciola species taken in a single
sample at station 35, but individual specimens were
parasitized by only one type. There are not enough
data to indicate whether or not incidence varies by
time of year in any of the amphipod species infected
with these parasites. Infected amphipods were not
found at the most northern and southern of the sta-
tions, but these stations were sampled fewer times
than most of the "positive" stations (i.e., stations
where amphipods with syndinid infections occurred).
There were 18 positive stations. Only Type AA was
found at stations 23, 37, and 50. Only Type AV
occurred at stations 33, 40, 56, and 62. Both types
were represented at stations 20, 27, 35, 38, 47, 48,
49, 51, 57, 63, and 64.
Whether one or both types occurred at a single
station depended variously on which amphipod
species were present, and on unknown factors. Two
species of Ampelisca, A. vadorum Mills and A.
agassizi, were common at inshore station 33. Prev-
alence of Type AV in A. vadorum was 35% (56/158).
However, Type AA did not occur at station 33
although a favored host, A. agassizi, was abundant
there. In contrast, only Type AA was found at
station 23, no doubt because of 2,811 amphi-
pods collected there, only 23 were not A. agas-
sizi.
Development and Morphology
All forms were similar in that extensive plasmodia
were never present and chromosomes were con-
densed in the interphase nuclei of the spores. There
were four, possibly five, chromosomes. There was
no metaphase plate. At telophase the apices of the
two sets of chromosomes were touching (see Figure
3), and at all stages of mitosis the chromosomes of
each group were juxtaposed basally (where they
presumably were attached to the nuclear membrane)
and spread out apically to varying degrees, like the
spokes of a parasol (Figs. 2-4). These events are
typical of "mitose syndinienne" (Chatton 1921). Syn-
dinid chromosomes are V-shaped, so that each has
two arms. In tissue sections the V shape was best
seen in cells that had lysed, leaving only the chro-
mosomes (Fig. 5). During telophase there were often
only four (sometimes five?) visible arms of chro-
mosomes in each daughter nucleus. If sectioning
artifact was not responsible for the small number
w
*<
m
W
M
Figures 2-3.— Mitosis in Type AV parasites in Ampelisca
vadorum (arrowheads). Interphase parasites of Figure 3 are
stage II.
Figure 4.— Mitosis in a Type AA parasite in Ampelisca agassizi
(arrowhead). Chromosomes form a rosette in the interphase
nucleus to the right (asterisk).
Figure 5.— Chromosomes in a lysed Type AA parasite from
Byblis serrata (arrowhead). The V shape of the chromosomes
is evident. Figures 2-5, x 1500.
of visible arms, the cells might have been haploid.
Before spore formation, chromatin disposition in
nuclei was variable, depending on the type of
parasite and the stage of development. Resting
nuclei with unfolded chromosomes were granular or
vesicular, and sometimes rimmed with chromatin
(see Figures 8, 17). In nuclei with partially unfolded
chromosomes, clumps of chromatin often were ar-
ranged so that they created a dashed or dotted line
in the position that would be occupied by a complete-
ly condensed chromosome (see Figure 9). When seen
in a polar view, chromosomes or chromatin clumps
formed rosettes (Figs. 4, 5). Morphology of the per-
sistent chromosomes of spores was variable and will
be described later.
608
JOHNSON: PARASITES OF BENTHIC AMPHIPODS
Staining characteristics of nuclei differed depend-
ing on the stage. Except for spores, prespores, and
some cells in early Type AA infections, nuclei tended
to be purple, not blue, with both chromatin and the
matrix staining similarly in some cases. When nuclei
at these stages were in mitosis, the chromosomes
were little, if at all, bluer than chromatin in resting
cells, although sometimes chromatin was more deep-
ly staining in the dividing cells. Types of chromo-
somes that stained with fast green by the Alfert and
Geschwind method (indicating presence of basic pro-
teins on the chromosomes) would stain blue in H&E
preparations. Chromatin and chromosomes that did
not stain with fast green in the Alfert and Gesch-
wind method would stain purple with H&E.
A comparison of Types AA and AV, by develop-
mental stage, is given in Table 2. Infections con-
sisting of few parasites were considered to be the
earliest ones and are here designated stage I infec-
tions. Stage II infections consisted of more numer-
ous and generally larger organisms, and stage III
infections consisted of prespores and spores that
usually filled the hemocoel.
Type AA
Most Type AA infections were in Ampelisca
agassizi (Table 1). Type AA chromosomes of all
developmental stages were usually thicker than
those of Type AV (compare Figures 2 and 4), and
the organisms and their nuclei were larger (Table
2). Stage I organisms were scattered through the
hemocoel, never numerous, and variable in mor-
phology and staining characteristics. The one com-
mon attribute was scanty and poorly staining cyto-
plasm. Chromosomes were usually distinct. The
most usual stage I infection consisted of scattered
single cells and small plasmodia with nuclei that
measured 3 to 4 /urn and had rather distinct chro-
mosomes or chromatin clumps that stained a clear
blue. Mitotic figures were not frequent, but were
more common than in the other stages. A few cells
in a late stage I (or very early stage II) infection
probably were polyploid. They had many rather
long, tangled chromosomes that sometimes formed
partially separated groups within the nuclear area.
The nuclei of these cells measured more than 7 ptm
in the greater dimension.
Stage II organisms were more numerous and dis-
tinguished by having voluminous vacuolate or foamy
cytoplasm (Fig. 6). Chromosomes and chromatin
clumps were often obscured because the nuclear
matrix stained almost as strong a purple as the
chromatin. The nuclear matrix did not stain in the
Feulgen reaction. Plasmodia were uncommon,
always small, and sometimes consisted of short
chains of joined cells. Mitosis was rarely seen in
stage II and stage III, and probably was closely syn-
chronized, which would reduce the probability of
finding mitotic figures in fixed material. As the
spore stage was approached, nuclei became smaller
and bluer, and chromatin clumps and chromosomes
gained clear outlines, because the matrix no longer
stained.
By the time of spore formation (stage III), organ-
isms filled the hemocoel, and infected amphipods in
H&E-stained sections could be distinguished with
the naked eye because of their overall dark-blue
color. Spore nuclei were spherical, and chromosomes
were condensed but tightly packed and impossible
to count (Fig. 7). In one infection, synchronized
nuclear division had apparently just taken place, and
daughter cells had not yet separated, so that bi- and
6 4
•
i
f
4P
•I
Figures 6-7.— Type AA parasites in Ampelisca agassizi. 6:
Stage II. Nuclei do not have distinct clumps of chromatin and
the cytoplasm is vacuolate. 7: Stage III (spores) (arrowhead).
An unidentified fungus was also infecting the amphipod
(asterisk). Figures 6-7, x 1500.
609
FISHERY BULLETIN: VOL. 84, NO. 3
quadrinucleate plasmodia were common. Cytoplasm
of spores was scant. Sometimes spores were shaped
like teardrops but generally they had amorphous
outlines. A flagellum was visible on a few spores in
an individual of Unciola species.
8
** *"
• I *
Type AV
This description is based on the organisms that
infected Ampelisca vadorum. Stage I consisted of
scarce and scattered small plasmodia, typically each
with 2 to 10 nuclei. Their cytoplasm was faintly
fibrous. Chromatin and the nuclear matrix were
always purplish and nuclei were often rimmed with
chromatin (Fig. 8). The nuclear matrix was not
Feulgen positive, and chromatin did not stain
strongly by this method. Slightly more advanced in-
fections, with more parasites, had irregularly shaped
single cells as well as plasmodia. The single organ-
isms were often elongate, their nuclei were as above,
and their cytoplasm was faintly stained.
Stage I A, which I presume follows stage I, and
which did not occur in Type AA, had moderate num-
bers of small plasmodia and single cells. Chromatin
patterns were rather distinct in most nuclei, par-
ticularly in the larger ones. Chromatin stained pur-
ple. Stage IA was distinguished by the presence of
small, densely staining bodies. They were usually
spherical but sometimes oval, and were usually sur-
rounded by thin rims of cytoplasm. The bodies were
associated with the plasmodia (Fig. 9) and also scat-
tered through the hemocoel. They were intensely
Feulgen positive and stained bright green by the
Alfert and Geschwind method. The dense bodies
were never extremely abundant and were present
only in the company of many stage IA cells.
Chromosomes of stage II cells were partially con-
densed, and chromosomes and chromatin clumps
were distinct because there was minimal staining
in the nuclear matrix, unlike Type AA parasites in
stage II. The cytoplasm was usually densely and
homogeneously stained (Fig. 3). Cells were often
very numerous and closely packed, but were not
plasmodial. Occasionally there were a few dense
bodies like those associated with stage IA.
Occasional stage III infections were not as heavy
as some stage II infections. There was apparently
an abrupt transition from stage II cells to stage III
prespores and spores. In one infection, a mass of
spores with distinct deep-blue chromosomes oc-
cupied a circumscribed area in the hemocoel, and
larger single cells with condensed chromosomes that
stained purple, and were probably very late stage
II, occupied the remainder of the hemocoel (Fig. 10).
%
--
1
€ 4
10
1 J,
t
,;;;.,f!pP
' ill
- r .-
*
r
*4*
tt
'
«A *%♦.*
Figures 8-10.— Type AV parasites in Ampelisca vadorum. 8:
Stage I. Several nuclei in the plasmodia are rimmed with chrom-
atin. 9: Stage IA. Plasmodia with associated spherical dense
bodies. Nuclei are pale and chromosomes are partially unfolded
in some nuclei (arrowhead). 10: Late Stage II (larger, pale nuclei
to the left— arrowhead) and Stage III (smaller, deeply staining
nuclei to the right— open arrow). A demonstration of syn-
chronized division of the parasite. Larger host nuclei are also
present. Figures 8-9, x 1500; Figure 10, x 600.
Presumably, the mass of spores resulted from syn-
chronized but circumscribed division of a part of the
population of the larger cell type. The roughly
spherical nuclei of the spores in this infection were
<2 /urn in diameter; nuclei of the larger cells were
slightly >3 ^m in diameter.
610
JOHNSON: PARASITES OF BENTHIC AMPHIPODS
Cells presumed to represent spores had either
elongate or spherical nuclei (Figs. 11, 12). The two
types did not occur together. Mitosis took place in
very small cells, and possibly cells with spherical
nuclei were prespores. They might also have been
spores that had not yet acquired their final form,
because cells of an intermediate shape also occurred.
Chromosomes of the spherical nuclei were short;
those of elongate nuclei were longer, somewhat
more slender, and beaded. Because the cytoplasm
was usually indistinct or invisible, outlines of spores
were also indistinct. It is probable that spores often
ruptured during fixation, resulting in loss of all cell
components except the chromosomes, as shown in
Figure 11.
A probable polyploid cell was present in one early
stage III infection, and there were small plasmodia
in all stage III infections (as in Figure 17). Nuclei
in plasmodia had purple-staining chromatin and did
not stain by the Alfert and Geschwind method,
unlike chromosomes of the spores. The relationship
of the small plasmodia to spore formation was not
obvious.
Numbers of Type AV-infected individuals of
species other than A. vadorum and M. edwardsi
were small, and all stages of development were not
usually represented. Stage IA infections, as well as
Figures 11-12.— Type AV, Stage III (spores), in Ampelisca
vadorum. 1 1 : Elongate spores. Note the beaded appearance of
the chromosomes in one spore (arrowhead). 12: Spherical
spores. Figures 11-12, x 1500.
some or all the other stages, were seen in Ampelisca
verrilli Mills, Leptocheirus pinguis (Stimpson),
Casco bigelowi (Blake), and Unciola species. Stage
I A infections of A. verrilli and C. bigelowi differed
from those of A. vadorum because the small dense
bodies were often irregularly shaped or composed
of two or three contiguous particles rather than be-
ing single and spherical or oval. In one of two stage
III infections in L. pinguis, spores had almost
spherical chromosomes (Fig. 13). In the other,
chromosomes were indistinct because they were
closely packed, but were longer than in the first in-
fection and apparently beaded. All stages of infec-
tion were represented in Unciola species. Spore
nuclei were round or oval and a flagellum was visi-
ble on a few spores in two infections. The final divi-
sions were just taking place in one of these infec-
tions, and many cells were still binucleate. Most of
the single spores had rounded outlines, but spores
with a visible flagellum were oval.
Monoculodes edwardsi had the highest overall
prevalence of Type AV (Table 1). The 25 infections
encompassed all stages except Stage IA. There were
polyploid cells in stage II infections. Their nuclei
were sometimes over 6 ^m in diameter, often had
chromatin separated into several areas (Fig. 14), and
their chromosomes were seldom completely con-
densed, except in mitotic cells. Polyploid cells in
mitosis had at least three sets of chromosomes. Out-
lines of both the interphase nucleus and the entire
cell were often highly irregular. Plasmodia that
presumably resulted from nuclear division of the
polyploid cells often had nuclei of two or more sizes
(Fig. 15), suggesting that all chromosome sets did
not divide at the same time, or that the genetic
material was not distributed equally at the time of
division, so that a single Plasmodium might have
contained haploid, diploid, and polyploid nuclei.
Nuclei of Type AV spores in M. edwardsi were about
1 /um in diameter (Fig. 16). A single flagellum (not
pictured) was visible on some spores in the infec-
tion presented in Figure 16. As typical of Type AV,
plasmodia were present in all stage III infections
(Fig. 17).
Host Response
Reactions against the syndinid parasites were ex-
tremely rare. One Type AV-infected specimen each
oiMelita dentata (Kr0yer) s. lot. and Unciola species
had scattered, melanized, amorphous nodules in the
hemocoel, but the nodules could not be definitely
associated with the syndinid infections. In one
specimen of L. pinguis, hemocytes were associated
611
FISHERY BULLETIN: VOL. 84, NO. 3
« «• *.
14
15
#
m
I
16
17
'■-'
# •
*'-,
•A.
%
Figures 13-17.— Type AV parasites. 13: Stage III (spores) in
Leptocheirus pinguis. The chromosomes are spherical (arrow-
head). 14: Stage II in Monoculodes edwardsi. Two of the para-
sites are polyploid (arrowheads). Note separate groups of
chromosomes or chromatin clumps in both these parasites. 15:
Plasmodium resulting from nuclear division of a polyploid
parasite in M. edwardsi. Note differently sized nuclei. 16: Stage
III (spores) in M. edwardsi. There were flagellated spores in this
infection. 17: Prespores, some dividing, in M. edwardsi. A
Plasmodium, with rimmed nuclei, is also present (arrow-
head). Figures 13-17, x 1500.
with Type AV organisms, and karyorrhexis had oc-
curred in unidentified cells in the area. With the
possible exception of the Type AV infection in L.
pinguis, the syndinids were not being attacked by
hemocytes at the time of fixation.
There was another sign that the syndinid parasites
successfully evaded detection by their hosts. Two
specimens of A. agassizi, both collected at station
47 but at different times, were infected jointly and
heavily with Type AA and an unidentified fungus
(Fig. 7). Of the more than 7,000 examined micro-
scopically, these were the only two amphipods that
had systemic fungal infections. Fungi were being
phagocytized by hemocytes and fixed phagocytes,
and other groups of fungi were being transformed
into melanized nodules. (Probably the latter fungi
had originally been phagocytized and killed by
hemocytes that did not survive the process them-
selves.) Although hemocytes and fixed phagocytes
were actively destroying fungi, there was no indica-
tion that the accompanying syndinids were recog-
nized as foreign.
Numbers of hemocytes apparently decreased dur-
ing syndinid infection, but even in heavy infections
some hemocytes remained and were still functional
as shown by their ability to phagocytize the fungi
discussed above. It is probable that the two suc-
cessful fungal infections in syndinid-infected amphi-
pods resulted in part from the fungi multiplying
more rapidly than they could be phagocytized and
degraded by the few remaining hemocytes and the
fixed phagocytes associated with the heart.
The syndinid parasites did not castrate their hosts.
Whether death ensues from every infection with
these parasites is not known. However, the general
lack of discernible host response makes it unlikely
that amphipods could successfully combat the
parasites.
DISCUSSION
Like species of Syndinium described from cope-
pods, Types AA and AV have a small number of
chromosomes which are permanently condensed in
spores and partially condensed in certain other
stages; plasmodia (small and multiple in the case of
Types AA and AV) are present during some devel-
opmental stages; and spore formation takes place
in the hemocoel of the host. However, species of
Syndinium in copepods differ from Types AA and
AV in that they develop from a Plasmodium that is
first applied to the wall of the gut and then expands
to fill the entire hemocoel. The massive Plasmodium
then fragments to form individual dinospores. By
612
JOHNSON: PARASITES OF BENTHIC AMPHIPODS
the time of sporulation, the host is castrated (Chat-
ton 1910, 1920). Types AA and AV resemble Hema-
todinium, not Syndinium, in that apparently none
of these organisms develop from a primary Plas-
modium associated with the gut, but instead they
multiply from a few single cells and small plasmodia
in the general hemocoel and never form a single
massive Plasmodium. Further, these parasites do
not castrate their hosts (Newman and Johnson 1975;
MacLean and Ruddell 1978; P. T. Johnson, unpubl.
data).
Syndinium gammari, like Types AA and AV, is
perhaps more closely related to Hematodinium than
to Syndinium. Syndinium gammari was assigned
to Syndinium by Manier et al. (1971) on the assump-
tion that a massive Plasmodium was present dur-
ing development. However, none of the infections
studied by these authors had either a primary
Plasmodium associated with the gut or a later and
massive Plasmodium throughout the hemocoel. The
first stage of S. gammari observed consisted of
small irregular plasmodia up to 15 pm in diameter,
which Manier and coworkers assumed resulted from
the splitting-up of a large plasmodium. The small
plasmodia then divided to form "diplococcal" forms,
and these divided to give round, single organisms
which transformed into spores measuring 7-8 /urn by
3-3.5 ^m. In the later stages of division, typical
"dinomitosis" and "dinokaryons" were present.
Considering the course of development in the ap-
parently related parasites of benthic amphipods,
Types AA and AV, it is possible that S. gammari
does not have a primary plasmodium associated with
the gut wall and does not develop an extensive
Plasmodium in the hemocoel. If early stages of S.
gammari consist of a few single cells or small
plasmodia, these could have escaped notice because
the parasites were observed after their removal
from the host amphipod, either alive or in fixed and
stained smears (Manier et al. 1971). Scattered
organisms could more easily be missed by this tech-
nique than by inspection of paraffin-embedded and
sectioned whole amphipods.
Chromosomes of Solenodinium globiforme and
three species of Syndinium, all parasites of radio-
larians, stain with fast green in the Alfert and
Geschwind method for demonstration of basic
nuclear proteins (Ris and Kubai 1974; Hollande
1975). Ris and Kubai remarked that chromosomes
of the Syndinium species they studied also stained
brightly in the Feulgen reaction. Although not
definitely stated by the above authors, apparently
chromosomes of all developmental stages of the
above parasites stained equally with fast green.
Chromosomes of these species tend to remain con-
densed through the entire developmental cycle. On
the other hand, Hollande (1975) found that trophont
nuclei of the duboscquodinids Amoebophrya ceratii
and Duboscquella melo do not stain by the Alfert and
Geschwind method. He pointed out that chromo-
somes are not condensed in the trophont nuclei of
these forms and that he did not investigate stain-
ing properties of the condensed chromosomes of
spores. Hollande did find that a portion of the
nucleolus of A. ceratii stains with fast green in the
Alfert and Geschwind method. Like the syndinid
parasites of radiolarians, chromosomes of Type AA
and AV spores stain brightly in both Alfert and
Geschwind's technique and the Feulgen reaction.
However, Feulgen staining is less intense in stages
I and II nuclei and these nuclei do not stain at all
with fast green.
Eukaryotes have a greater quantity of histone in
rapidly dividing cells than in quiescent ones (DuPraw
1968; Wu et al. 1982), and nonhistone basic nuclear
proteins— although scarce at all times— are much
more abundant in log-phase than in stationary-phase
cultures of the free-living dinoflagellates Gyro-
dinium cohnii and Peridinium trochoideum (Rizzo
and Nooden 1974). It would be interesting to deter-
mine the relative amounts of basic nuclear proteins
through the developmental cycle of syndinids and
other duboscquodinids, and to determine whether
basic proteins of the amphipod parasites increase
when cells are dividing rapidly; and whether these
proteins are masked by other substances (acidic pro-
teins?) in stages where both chromatin and nuclear
matrix stain purple with H&E and do not stain in
the Alfert and Geschwind method.
Probably fixation and paraffin embedment not
only damaged flagella and were responsible for ap-
parent lack of flagella on most spores of Types AA
and AV, but also distorted spores of these parasites.
Cachon (1964) cautioned that because spores of
parasitic dinoflagellates become distorted or rup-
tured both on fixation and when physical conditions
are not proper, their shapes must be determined in
living material.
Origin and function of the small dense bodies pres-
ent in Type AV, stage IA infections were not evi-
dent. These bodies might represent necrotic nuclei
like those seen in Syndinium infections (Jepps
1936-37), discarded chromatin resulting from reduc-
tion divisions, or, perhaps, nuclei of microspores
(Cachon 1964).
Numbers of Gammarus locusta (Linn.) infected
with Syndinium gammari in the Etang de Thau,
France, varied from few to all members of a popula-
613
FISHERY BULLETIN: VOL. 84, NO. 3
tion (Manier et al. 1971). The infected amphipods
these authors examined were apparently unaffected
by the parasite. However, before one could deter-
mine the mortality rate due to syndinid infection,
it would be necessary to examine moribund and dead
amphipods found in the field for presence of syn-
dinids, as well as to follow progress of infection in
the laboratory. Syndinids appear to be unaffected
by host defense mechanisms. Spores of syndinids
that parasitize the hemocoel must exit through
breaks in the exoskeleton or gut. Because hemocytes
are in short supply by time of sporulation and other
host resources can be expected to be depleted, host
defense mechanisms probably would not be suffi-
cient to prevent death by infection with other micro-
organisms that would enter through the breaks or
death by leakage of body fluids. Assuming, on the
basis of evidence presented in this paper, that
amphipods are unable to contain syndinid infections
and that most infections would therefore progress
to the spore stage, syndinid infection could serve
as a population regulator in heavily parasitized
species. Monoculodes edwardsi and Ampelisca
vadorum, which had overall prevalences of syndinid
infection of 23% and 17% respectively, are examples
of species that might be affected in this manner.
ACKNOWLEDGMENTS
Sara V. Otto, Maryland Department of Natural
Resources, Oxford, MD, aided in translation of ar-
ticles from the French, and the following person-
nel from the Oxford and Sandy Hook Laboratories
of the Northeast Fisheries Center helped as follows:
Frank Steimle, David Radosh, Linda Dorigatti,
Gretchen Roe, and Sharon MacLean collected the
amphipods; Ann Frame and Linda Dorigatti aided
in their identification; and Gretchen Roe, Dorothy
Howard, Cecelia Smith, and Linda Dorigatti
prepared the specimens for histological examination.
My thanks to all of the above.
LITERATURE CITED
Alfert, M., and I. I. Geschwind.
1953. A selective staining method for the basic proteins of
cell nuclei. Proc. Nat. Acad. Sci. USA 39:991-999.
Cachon, J.
1964. Contribution a l'etude des Peridiniens parasites. Ann.
Sci. Nat. Zool. Fr., Ser. 12, 6:1-158.
Chatton, E.
1910. Sur l'existence de Dinoflagelles parasites coelomiques.
Les Syndinium chez les Copepodes pelagiques. C. R. Acad.
Sci. Paris, 151:654-656.
Chatton, E.
1920. Les Peridiniens parasites. Morphologie, reproduction,
ethologie. Arch. Zool. Exp. Gen. 59:1-475.
Chatton, E.
1921. Sur un mecanisme cinetique nouveau: la mitose syndi-
nienne chez les Peridiniens parasites plasmodiaux. C. R.
Acad. Sci. Paris, Ser. D, 173:859-862.
Chatton, E.
1952. Classe des Dinoflagelles ou Peridiniens. In P. P.
Grasse (editor), Traite de Zoologie, Vol. 1, p. 309-390.
Masson et Cie, Paris.
Chatton, E., and R. Poisson.
1931. Sur l'existence, dans le sang des Crabes de Peridiniens
parasites: Hematodinium perezi n.g., n. sp. (Syndinidae).
C. R. Soc. Biol. 105:553-557.
Du Praw, E. J.
1968. Cell and molecular biology. Academic Press, N.Y.
Herzog, M., S. von Boletzky, and M.-O. Soyer.
1984. Ultrastructural and biochemical nuclear aspects of
eukaryote classification: independent evolution of the dino-
flagellates as a sister group of the actual eukaryotes?
Origins Life 13:205-215.
Hollande, A.
1975. Etude comparee de la mitose syndinienne et de celle
des Peridiniens libres et des Hypermastigines infrastructure
et cycle evolutif des Syndinides parasites de Radiolaires.
Protistologica 10:413-451.
Jepps, M. W.
1936-37. On the protozoan parasites of Calanus finmarchicus
in the Clyde Sea area. Q. J. Microsc. Sci. 79:589-662.
Johnson, P. T.
1985. Parasites of benthic amphipods: microsporidans of
Ampelisca agassizi (Judd) and some other gammarideans.
Fish. Bull., U.S. 83:497-505.
1986. Parasites of benthic amphipods: ciliates. Fish. Bull.,
U.S. 84:204-209.
Loeblich, A. R., III.
1976. Dinoflagellate evolution: speculation and evidence. J.
Protozool. 23:13-28.
Maclean, S. A., and C. L. Ruddell.
1978. Three new crustacean hosts for the parasitic dino-
flagellate Hematodinium perezi (Dinoflagellata: Syndinidae).
J. Parasitol. 64:158-160.
Manier, J.-F., A. Fize, and H. Grizel.
1971. Syndinium gammari n. sp. peridinien Duboscquodinida
Syndinidae, parasite de Gammarus locusta (Lin.) Crustace
Amphipode. Protistologica 7:213-219.
Newman, M. W., and C. A. Johnson.
1975. A disease of blue crabs (Callinectes sapidus) caused by
a parasitic dinoflagellate, Hematodinium sp. J. Parasitol.
61:554-557.
Ris, H., and D. F. Kubai.
1974. An unusual mitotic mechanism in the parasitic proto-
zoan Syndinium sp. J. Cell Biol. 60:702-720.
Rizzo, P. J., AND L. D. Nooden.
1974. Isolation and partial characterization of dinoflagellate
chromatin. Biochim. Biophys. Acta 349:402-414.
Siebert, A. E., and J. A. West.
1974. The fine structure of the parasitic dinoflagellate Haplo-
zoon axiothellae. Protoplasma 81:17-35.
Stickney, A. P.
1978. A previously unreported peridinian parasite in the eggs
of the northern shrimp, Pandalus borealis. J. Invertebr.
Pathol. 32:212-215.
Wu, R. S., S. Tsai, and W. M. Bonner.
1982. Patterns of histone variant synthesis can distinguish
G0 from Gj cells. Cell 31:367-374.
614
FOOD HABITS AND DIET OVERLAP OF TWO CONGENERIC SPECIES,
ATHERESTHES STOMIAS and ATHERESTHES EVERMANNI, IN
THE EASTERN BERING SEA
M. S. Yang1 and P. A. Livingston2
ABSTRACT
Stomachs of 196 arrowtooth flounder, Atheresthes stomias, and 152 Kamchatka flounder, A. evermanni,
collected from the same area of the eastern Bering Sea in summer 1983 were examined. Each species
was divided into four fork-length groups: less than 201 mm, 201-300 mm, 301-400 mm, and greater than
400 mm. The principle diet of both species was comprised of walleye pollock, Theragra chalcogramma,
shrimp (mostly Crangonidae), and euphausiids. Pollock was the most important prey item for both species
in all four size groups, ranging from 56 to 86% and 66 to 88% of the total stomach content weight of
Kamchatka flounder and arrowtooth flounder, respectively. Schoener's indices of diet overlap were
calculated between the two species for each size group. The high value of the indices (ranging from 0.67
to 0.90) indicate that these two congeneric species basically consume the same resources.
The genus Atheresthes of the family Pleuronectidae
has two species: Kamchatka flounder, A. evermanni
(Jordan and Starks), and arrowtooth flounder (Nor-
man, 1934), A. stomias (Jordan and Gilbert). Ather-
esthes evermanni is distributed from northern Japan
(Hokkaido) through the Sea of Okhotsk to the
western Bering Sea north to Anadyr Gulf (Willimov-
sky et al. 1967). Atheresthes stomias is distributed
from Central California to the eastern Bering Sea.
In the Bering Sea, it meets about on a line with Saint
Matthew Island, overlaps with, and is replaced by
A. evermanni (Hart 1973).
Because the morphological differences between A.
evermanni and A. stomias are subtle, they have been
recorded as one species, A. stomias, in the eastern
Bering Sea resource assessment surveys of the
Northwest and Alaska Fisheries Center (NWAFC)
(Smith and Bakkala 1982). Food habits of A. stomias
have been studied by some researchers (Gotshall
1969; Kabata and Forrester 1974; Smith et al. 1978),
but none of those studies covered the food habits
of A. evermanni. Shuntov (1970) studied the feeding
intensity of the two Atheresthes species, but he did
not compare the diets of these species.
Using electrophoretic examination, Ranck et al.
(1986) have confirmed that these two types of Ather-
esthes are separate species. The purpose of this study
is to analyze stomach samples of these two con-
1 Fisheries Research Institute, University of Washington, WH-10,
Seattle, WA 98195.
2Northwest and Alaska Fisheries Center, National Marine
Fisheries Service, NOAA, 7600 Sand Point Way N.E., Seattle, WA
98115.
Manuscript accepted December 1985.
FISHERY BULLETIN: VOL. 82, NO. 3, 1986.
generic species collected in the area of their distri-
butional overlap in the eastern Bering Sea and
compare the diets of both fish species to calculate
the degree of diet similarity to determine whether
the two species can be considered trophically
equivalent.
COLLECTION AND PROCESSING OF
SAMPLES
Specimens were collected from 6 July to 16 July
1983 in the eastern Bering Sea aboard the Alaska,
a research vessel participating in the annual sum-
mer resource assessment survey conducted by the
Resource Assessment and Conservation Engineer-
ing (RACE) division of the NWAFC in Seattle, WA.
Stomachs of arrowtooth flounder and Kamchatka
flounder were taken at standard resource assess-
ment stations where half-hour tows were made
using an 83-112 Eastern bottom trawl net with an
estimated 2.3 m vertical and 16.4 m horizontal
mouth opening.
The samples were collected in an area around and
to the northwest of the Pribilof Islands at bottom
depths ranging from 71 to 137 m (Fig. 1, Table 1).
A random subsample of individuals of both arrow-
tooth flounder and Kamchatka flounder was ob-
tained at each station with a total collection of 348
stomachs from 19 stations.
Individual fish were first checked for signs of re-
gurgitation, i.e., food items in mouth or gill plates
or flaccid stomach, and were discarded if any such
signs were noted. Stomachs from the remaining fish
615
FISHERY BULLETIN: VOL. 84, NO. 3
63 00N
■- 61 00N
59 00N
- 57 00N
55 00N
- 53 00N
5) OON
179 OOE
1 76 OOW
171 OOW
166 OOW
161 OOW
56 OOW
Figure 1.— Sampling locations for arrowtooth flounder, Atheresthes stomias, and Kamchatka flounder, A. evermanni, in summer 1983
in the eastern Bering Sea.
were excised along with the anterior portion of the
body (including head, stomach, and intestines), and
these samples were sent to the laboratory for species
identification. Each specimen was placed in a muslin
bag with a specimen label bearing fork length, sex,
and station information. All samples were preserved
in 10% Formalin3.
In the laboratory, two characters were used for
species identification: the position of the left eye
relative to the dorsal profile and gill rakers. Kam-
chatka flounder has the upper eye completely on the
right side of the head and 13 or fewer gill rakers
on the first arch. Arrowtooth flounder has an up-
per eye which interrupts the dorsal profile of the
head and 15 or more gill rakers on the first arch
(Norman 1934; Willimovsky et al. 1967).
3Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Stomachs were analyzed individually. Prey items
were identified to the lowest taxonomic level prac-
tical, counted, and weighed damp to the nearest
milligram. The standard length of fish prey were
also measured.
DATA ANALYSIS
Specimens of A. stomias and A. evermanni were
divided into 100 mm fork-length groups for data
analysis: <201 mm, 201-300 mm, 301-400 mm, and
>400 mm. Percent of frequency of occurrence
(% FO), percentage of total stomach content weight
(% W), percentage of total prey number (% N) and
the Index of Relative Importance [IRI = % FO (% N
+ % W)] (Pinkas et al. 1971) were calculated for ma-
jor categories of prey items in the 100 mm size
groupings of A. stomias and A. evermanni.
Based on a review of dietary overlap measures
616
YANG and LIVINGSTON: FOOD HABITS AND DIET OF TWO CONGENERIC SPECIES
Table 1 .—Station information and number of stomachs collected at each station of arrowtooth
flounder (ATF) and Kamchatka flounder (KF) in the eastern Bering Sea for the summer 1983.
Alaska
Haul
Bottom
No. ATF1
No. KF1
daylight
depth
temp.
Latitude
Longitude
stomachs
stomachs
Haul
Date
time
(m)
(°C)
N
W
collected
collected
100
7/6
1000
71.3
3.1
56°29.46'
169°15.61'
14 (6)
19(17)
101
7/6
1200
71.3
3.1
57°19.25'
168°59.13'
4 (5)
2(1)
102
7/6
1400
76.8
2.6
57°10.87'
169° 10.22'
14(6)
7(6)
105
7/7
0800
102.4
2.7
56°39.96'
168°55.22'
18 (9)
7(4)
106
7/7
1100
133.5
3.8
56°20.18'
168°53.24'
11 (2)
10 (3)
107
7/7
1600
111.6
3.5
58°20.01'
170°02.15'
12 (0)
12 (1)
108
7/8
0800
96.9
3.8
56°40.00'
170°04.47'
5(1)
3(1)
114
7/9
1400
75.0
2.7
57°39.23'
170°16.12'
13 (1)
2 (0)
135
7/13
1900
96.9
1.5
58°22.09'
171°37.39'
6(1)
0(0)
136
7/14
0700
100.6
2.8
58°01.90'
171°33.37'
5 (0)
1 (0)
137
7/14
1000
100.6
3.0
57°41.94'
171°31.16'
7(0)
0(1)
138
7/14
1300
102.4
3.7
57°21.05'
171°28.26'
8 (3)
6(1)
139
7/14
1500
109.7
3.9
57°02.54'
171°25.63'
11 (0)
6(1)
140
7/14
1800
120.7
3.7
56°43.42'
171°23.38'
6 (0)
9 (0)
141
7/15
0700
137.2
4.0
56°42.72'
172°32.33'
2(6)
7(2)
142
7/15
0900
124.4
3.6
57°00.84'
172°39.37'
5 (6)
7(2)
144
7/15
1500
122.5
3.7
57°40.10'
172°47.92'
3(1)
2 (0)
146
7/16
0600
111.6
2.6
58°20.10'
172°55.00'
2 (2)
9 (0)
147
7/16
0900
115.2
2.6
58°40.07'
172°59.18'
3(0)
3(0)
Total
149 (47)
112 (40)
'Stomachs containing food, number of empties in parentheses.
(Cailliet and Barry 1979; Linton et al. 1981),
Schoener's (1970) index was chosen because it was
found to measure overlap accurately over most of
the range of potential overlap (Linton et al. 1981).
Schoener's index, Cxy, is calculated as
Cxy = 1.0 - 0.5(I|p^ - VJ)
where px t and pyi are the estimated proportions by
weight of prey i in the diets of species x and y,
respectively (the percentage by weight of prey items
in Table 2). The index ranges from 0 which indi-
cates no dietary overlap to a maximum overlap of
1 when all prey items are found in equal propor-
tions.
communis, were the dominant shrimp consumed.
Walleye pollock constituted the highest proportion
of the diet for all size groups of flounder, ranging
from 56% by weight of the diet for Kamchatka
flounders 301-400 mm long to about 88% by weight
for arrowtooth flounders >400 mm long. Miscella-
neous food items consumed included polychaetes,
copepods, cumaceans, hippolytid shrimps, ophi-
uroids, and various fish species.
Mean stomach content weight of those stomachs
with food was similar between arrowtooth flounder
and Kamchatka flounder for all but the largest size
group. The mean stomach content weight ranged
from about 1.4 g for the small flounders to over 20
g for the largest size group.
RESULTS
General Feeding Trends
A total of 348 stomachs were analyzed; 87
stomachs (25%) were empty. Table 2 shows the per-
centages by weight of all prey items found in the
stomachs of both flounder species by size group. In
general, both species consumed the same prey
species or groups: euphausiids, pandalid and
crangonid shrimps, and walleye pollock (Fig. 2).
Thysanoessa inermis and T. raschii were the domi-
nant euphausiids consumed. Some pandalid shrimps
were eaten by smaller (<301 mm) flounders of both
species, but crangonid shrimps, mainly Crangon
Diet Comparisons Within Size Groups
The principle diet of both Atheresthes species in
the <200 mm size group was comprised of walleye
pollock, euphausiids, and shrimps (Fig. 3). Walleye
pollock comprised 58% and 65.5% by weight of the
diet of Kamchatka flounder and arrowtooth
flounder, respectively. Euphausiids comprised the
highest percentage by numbers of the diet of both
species, 53% for Kamchatka flounder and 69.4% for
arrowtooth flounder. Shrimps, including Crangon
communis, Pandalus goniurus, Pandalus tridens,
and Eualus avinus, constituted 17.1% and 7.2% by
weight of the diet of Kamchatka flounder and arrow-
tooth flounder, respectively. Other less important
617
FISHERY BULLETIN: VOL. 84, NO. 3
Table 2.— Percentage by weight of prey items in the stomachs of arrowtooth flounder (ATF) and Kam-
chatka flounder (KF) by 100 mm FL categories; and Schoener's indices (Cxy) of diet overlap between
the two species.
Predator size
group (mm)
<200
201-300
301-400
>400
Prey item
KF
ATF
KF
ATF
KF
ATF
KF
ATF
Invertebrates
Polychaeta
—
—
—
0.28
—
—
—
—
Copepoda
—
0.01
—
—
—
—
—
—
Mysidacea
0.45
0.34
0.12
—
—
—
—
—
Cumacea
—
—
0.01
—
—
—
—
—
Amphipoda
0.22
—
0.52
—
0.07
—
—
—
Euphausiiacea
Unidentified
5.64
8.99
0.23
9.10
0.54
3.86
—
0.22
Thysanoessa rachii
—
2.76
—
1.35
—
2.32
—
—
T. inermis
4.28
10.67
3.55
9.33
7.40
10.03
4.09
6.55
Caridea
Unidentified
1.05
1.31
—
—
—
0.08
—
—
Hippolytidae
Eualus avinus
0.88
—
—
0.05
—
—
—
—
Pandalidae
Unidentified
—
1.08
—
—
—
—
—
—
Pandalus goniurus
3.89
—
—
—
—
—
—
—
Pandalus tridens
4.77
—
—
—
—
—
—
—
Pandalus sp.
0.54
0.37
0.24
—
—
—
—
—
Crangonidae
Unidentified
0.34
2.98
2.15
0.10
—
—
0.07
—
Crangon dalli
—
—
0.85
0.61
—
—
—
—
C. communis
5.67
1.43
5.53
0.70
0.31
0.15
—
0.22
Paguridae
—
0.01
—
—
0.58
—
—
—
Ophiuroidea
—
0.19
—
—
0.03
—
—
—
Chaetognatha
Sagitta sp.
—
0.03
—
0.01
—
—
—
—
Pisces
Gadidae
Unidentified
—
—
5.40
4.62
2.70
5.65
8.20
—
Theragra chalcogramma
58.03
65.51
81.55
71.69
55.78
76.99
85.87
87.96
Zoarcidae
Unidentified
—
—
—
—
5.55
—
—
5.06
Ly codes brevipes
—
—
—
—
8.20
—
—
—
Cottidae
—
1.15
—
—
—
—
—
—
Stichaeidae
Unidentified
3.00
—
—
—
—
—
—
—
Lumpenus maculatus
—
3.16
—
1.97
9.47
—
—
—
Pleuronectidae
Unidentified
7.50
—
—
—
9.36
—
1.77
—
Atheresthes sp.
3.73
—
—
—
—
—
—
—
Unidentified organic
material
—
—
0.05
0.19
—
0.92
—
—
No. of stomachs with food
32
40
43
53
20
40
19
14
Total weight of stomach
content (g)
46.96
57.24
93.29
167.66
181.89
291 .43
383.32
467.91
Mean stomach content
weight (g)
1.47
1.43
2.17
3.16
9.09
7.29
20.17
33.42
Mean fish length (mm)
187.80
184.60
250.10
260.70
350.50
341.30
441.10
450.00
Cxy
0.72
0.82
0.67
0.90
food items were stichaeids, pleuronectids, cottids,
mysids, and amphipods.
Walleye pollock, the dominant food of both
Atheresthes species in the 201-300 mm size group
(Fig. 3), constituted 81.6% and 71.7% by weight of
the diet of Kamchatka flounder and arrowtooth
flounder, respectively. Euphausiids comprised 20%
by weight of the diet of arrowtooth flounder. How-
ever, euphausiids only comprised 3.8% by weight
(39.9% by number) of the diet of Kamchatka
flounder. Shrimps (Crangonidae, Pandalidae) were
more important food for Kamchatka flounder (8.8%
by weight) than for arrowtooth (1.4% by weight).
Unidentified gadoids comprised 5.4% and 4.6% by
weight of the diet of Kamchatka flounder and arrow-
tooth flounder, respectively. Other less important
food items were polychaetes, mysids, amphipods,
and the stichaeid Lumpenus maculatus; they were
618
YANG and LIVINGSTON: FOOD HABITS AND DIET OF TWO CONGENERIC SPECIES
N = 32 40 43 53 20 40 19 14
100 r-
50 -
>
.a
O
0 u
yr.
■
Euphausiids
Shrimp
Other fish
Pollock
Other
KAKAKAKA
<200 201-300 301-400 > 400
Predator length group (mm)
Figure 2.— Percentage by weight of major prey categories in the diet of arrowtooth
flounder (A), Atheresthes stomias, and Kamchatka flounder (K), A. evermanni, for dif-
ferent length groups of fish collected from the eastern Bering Sea in summer 1983.
all <5% by weight of the diet of both Atheresthes
species.
The principle diet by weight of Kamchatka
flounder in the 301-400 mm size group was com-
prised of 55.8% walleye pollock, 13.8% zoarcids,
9.4% pleuronectids, 9.5% stichaeids, and 7.9%
euphausiids (Table 2, Fig. 3). Walleye pollock also
dominated the diet of arrowtooth flounder (77% by
weight). The other two main items of arrowtooth
flounder were euphausiids (16.2% by weight) and
unidentified gadoids (5.7% by weight). Shrimps were
not important food for either Atheresthes species of
this size; they contributed <1% by weight of the diet.
Other less important prey items were ophiuroids and
pagurids. Numerically, euphausiids dominated the
food for both species (90.7% for Kamchatka
flounder, 96.0% for arrowtooth flounder).
Walleye pollock dominated the food of the two
Atheresthes species in the >400 mm size group (Fig.
3). It constituted 85.9% and 88.0% by weight of the
diet of Kamchatka flounder and arrowtooth
flounder, respectively (Table 2). Though euphausiids
dominated the food by number (91.5% for Kam-
chatka flounder, 97.0% for arrowtooth flounder),
they only contributed 4.1% and 6.8% by weight of
the diet of Kamchatka flounder and arrowtooth
flounder, respectively. In addition to walleye pollock,
unidentified gadoids comprised 8.2% and pleuronec-
tids comprised 1.8% by weight of the diet of Kam-
chatka flounder. Zoarcids comprised 5.1% by weight
of the diet of arrowtooth flounder. Shrimps played
a less important role in the food of both Atheresthes
species (<1% by weight).
Diet Comparison Among Size Groups
There was not much difference in diets among size
groups in the proportion by weight of the prey
categories such as euphausiids and fish (Fig. 2).
However, shrimps disappeared from the diets of
flounders in the two larger size groups. The number
of different species in the diet also changes with size.
The <200 mm size group of flounders consumed
about 11 or 12 different prey categories while the
>400 mm size groups consumed only 3 or 4 differ-
ent prey types (see Table 2).
Even though the proportion by weight of fish in
the diet remained fairly constant over flounder size
groups, the size of individual fish consumed did
change with flounder length. Figure 4 shows the fre-
quency distribution of fish prey lengths found in the
stomachs of different size A. evermanni. Most of the
prey fish were age-0 juvenile pollock (<100 mm) for
the two smaller size groups and age-1 juvenile
619
FISHERY BULLETIN: VOL. 84, NO. 3
A. evermanni
A. s torn i as
CM
2 %N 40
ii 20
in 0
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£" %W 40-
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in
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i i i
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100
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80
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o %N 40
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>- II
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on
-
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CRA
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N
STI
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i i i i i i i i i i i
%w
100
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ion
EUP
80
60
40
20
0
-
U GAD
POL /^AMP
CRA
2U
40
_
60
80
i i i i i i
100
200
(N
II
en
o *-
g "
ioor
80
%N 60
%W
40
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0
20
40
60
80
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/
U GAD
-1 1 1 L
ro
ii
UJ
O '
o
%N
%W
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EUP
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-
40
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CRA
/
0
-
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20
40
\
ZOA
60
-
80
100
-
i 1 1
1, 1
l l 1 l l
0
100
200
100
200
% F.O.
% F.O.
Figure 3.— Indices of Relative Importance of major prey items in the diets of Atheresthes evermanni and A. stomias
of different size groups. % F.O., percent frequency of occurrence; % N, percentage of prey number; % W, percent-
age of total stomach content weight; POL, pollock; EUP, Euphausiacea; CRA, Crangonidae; PAN, Pandalidae;
AMP, Amphipoda; PLE, Pleuronectidae; MYS, Mysidacea; STI, Stichaeidae; HIP, Hippolytidae; ZOA, Zoarcidae;
U. GAD, Unidentified Gadidae; COT, Cottidae; S, number of stomachs containing food; E, number of empty
stomachs.
620
YANG and LIVINGSTON: FOOD HABITS AND DIET OF TWO CONGENERIC SPECIES
(U
Q-
Pollock
Other fish
Predator length:
• 400 mm
n= 15
x= 147.2
1
> I i | I | ' I
T
Predator length
301-400 mm
n = 15
x = 117.58
I 'T ' I ' I ' I i | ' |
Predator length:
201-300
n = 10
x = 72.31
I l I ' I l I I I i I i I ' I
Predator length:
< 200 mm
n = 47
x = 43.03
c"*
I "i"l i I I I ' I I I ' I I 1 1 I i I
120 160 200 240 280
Prey (fish) length (mm)
Figure 4.— Frequency distribution of standard lengths of prey fish
found in the stomachs of Atheresthes species from the eastern
Bering Sea in summer 1983.
pollock (100-200 mm) for the two larger size groups.
The fish prey length was plotted against the
predator length (Fig. 5). Fish prey size appears to
increase linearly with increasing predator size.
Diet Overlap
Values for Schoener's (1970) index of dietary over-
lap were obtained from a comparison (by weight)
between the diets of Kamchatka and arrowtooth
flounder of the same size groups (Table 2). All the
values obtained were >0.60, an indicator of high
dietary overlap (Langton 1982). The <200 mm size
group had an overlap value of 0.72 and the 201-300
mm size group had an overlap value 0.82. Within
each of these two size groups, fairly similar propor-
tions by weight of walleye pollock, euphausiids, and
shrimps were consumed. The 301-400 mm size group
had the lowest overlap value of 0.67. This is probably
because Kamchatka flounder ate less walleye pollock
by weight (56%) than did the arrowtooth flounder
(77%). Most of the remainder of the diet for Kam-
chatka flounder in this size group was composed of
different fish groups, such as zoarcids, stichaeids,
and pleuronectids, which were almost totally absent
from the arrowtooth' s diet at this size. The largest
size group of flounders (>400 mm) had the highest
overlap value of 0.90. This size group ate very
similar proportions by weight of walleye pollock and
euphausiids.
DISCUSSION
From this study, it appears that both Kamchatka
flounder and arrowtooth flounder are largely fish
feeders. Walleye pollock was the most frequently
observed prey and contributed the largest percent-
age by weight to the diets, followed by euphausiids
and shrimps (Table 2, Fig. 3). Gotshall (1969) found
that ocean shrimp, Pandalus jordani, was the most
common food item of arrowtooth flounder (because
the stomachs were collected on commercial shrimp
grounds), followed by fishes and euphausiids. Pacific
sanddabs, Citharichthys sordidus, were the most
numerous prey fish found in his study. Kabata and
Forrester (1974) examined 753 arrowtooth flounder
collected off the west coast of Vancouver Island.
Their study showed that euphausiids, followed by
fish were the predominant foods taken by arrow-
tooth flounder. The most commonly found species
of fish were eulachon, Thaleichthys pacificus, and
Pacific herring, Clupea pallasii. Smith et al. (1978)
found that fish constituted 41.09% and euphausiids
37.22% by volume of the food of 236 arrowtooth
flounder collected from the northeast Gulf of Alaska.
Walleye pollock were most commonly consumed fish
prey. Moiseev (1953) found that Kamchatka flounder
fed almost exclusively on pollock and only occa-
sionally on herring and other fishes.
The type of prey eaten by a fish is strongly corre-
lated with the morphology of the alimentary tract
of the fish (De Groot 1971; Ebeling and Cailliet 1974;
Allen 1982). Structure of the digestive tract of
arrowtooth flounder and Kamchatka flounder are
very similar. Both have a very large terminal mouth
that is nearly symmetrical with a wide gape; teeth
are arrow-shaped and well developed on both sides
of the jaws; gill rakers are long and strongly dentate;
621
FISHERY BULLETIN: VOL. 84, NO. 3
£
E
en
c
>
300 r
250
200 -
150
100 -
50 -
Y = 0.39X-26.33
r-0.85
• •
• •
_ •
•
•
•
•
•
•
•
• •
•
• •
•
•
•
•
•
— v*^""'^ * *
'
•
■
1
■ i
150
200
250
300
350
400
450
500
Predator length (mm)
Figure 5.— Scatter plot of prey fish length consumed by Atheresthes species from the eastern Bering Sea in summer
1983.
and the esophagus and stomach are large with four
large pyloric caeca and the intestine is a simple loop.
All of these characteristics indicate that Atheresthes
species are fish feeders as predicted by using De
Groot's (1971) morphological criteria. He stated that
large gill rakers with teeth are indispensable to fish
feeders, since they prevent the prey, grasped alive,
from struggling out of the mouth. The high per-
centages of fish in the diet of the two Atheresthes
species obtained in this study would be expected on
the basis of the similarities in the digestive tracts
of the two species.
The results also indicate that Atheresthes species
feed up in the water column. According to Allen
(1982), flatfishes with large symmetrical mouths
(Atheresthes species) probably use sight to locate
prey. They are oriented up in the water column
when foraging. The presence of pelagic fish (T.
chalcogramma) and euphausiids or nektonic bentho-
pelagic crustaceans such as shrimps in the diets of
Atheresthes species supports Allen's generalizations
concerning correlations between morphology and
feeding behavior in flatfishes.
The trend of the feeding habits of Atheresthes
species with regard to predator length is toward
piscivory; that is, when the predators are bigger,
they take more fish (by weight) as food. Specimens
from the <200 mm size group were found to ingest
the greatest variety of prey items in comparison to
other size groups. Specimens >400 mm long preyed
mainly on other fishes, primarily on pollock.
However, euphausiids were of importance in the diet
of all size groups. One 460 mm arrowtooth flounder
was found to have 838 Thysanoessa inermis in its
stomach. Smith et al. (1978) also noted a change in
food habits with increasing length in the arrowtooth
flounder. In their study, specimens over 450 mm
long preyed exclusively on pollock and other
gadoids. Euphausiids were important food of the
arrowtooth flounder up to 350 mm long; however,
none were found among the stomach contents of
specimens larger than 350 mm.
Based on the results of this study and those of
Smith et al. (1978) and Gotshall (1969), it appears
that Atheresthes species are opportunistic feeders;
they feed on those prey items that are most
abundant— pollock and euphausiids in the Gulf of
Alaska and eastern Bering Sea and ocean shrimp
in northern California. In the eastern Bering Sea,
the estimated abundance of age-0 pollock in 1982
is between 100 billion and 1,300 billion and, based
on the results of the 1983 bottom trawl survey by
NWAFC, this 1982 year class is the largest observed
since the large 1978 year class (Traynor in press).
622
YANG and LIVINGSTON: FOOD HABITS AND DIET OF TWO CONGENERIC SPECIES
In spite of the high diet overlap between Kamchatka
flounder and arrowtooth flounder, there is probably
no competition for food between these two species
because they are exploiting abundant food sources.
Finally, although Kamchatka founder and arrow-
tooth flounder are genetically distinct, they can be
considered trophically equivalent on the basis of
their similar diets and high diet overlap.
LITERATURE CITED
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.
Cailliet, G. M., and J. P. Barry.
1979. Comparison of food array overlap measures useful in
fish feeding habits analysis. In S. J. Lipovsky and C. A.
Simenstad (editors), Gutshop '78, fish food habits studies;
Proceedings of the 2d Pacific Northwest Technical Work-
shop, p. 67-79. Univ. Wash., Div. Mar. Resour., Wash. Sea
Grant, WSG-WO-79-1.
De Groot, S. J.
1971. On the interrelationships between morphology of the
alimentary tract, food and feeding behavior in flatfishes
(Pisces: Pleuronectiformes). Neth. J. Sea Res. 5:121-196.
Ebeling, A. W., and G. M. Cailliet.
1974. Mouth size and predator strategy of midwater
fishes. Deep-Sea Res. 21:959-968.
Gotshall, D. W.
1969. Stomach contents of Pacific hake and arrowtooth
founder from northern California. Calif. Fish Game 55:75-
82.
Hart, J. L.
1973. Pacific fishes of Canada. Bull. Fish. Res. Board Can.
180, 740 p.
Kabata, Z., and C. R. Forrester.
1974. Atheresthes stomias (Jordan and Gilbert 1880) (Pisces:
Pleuronectiformes) and its eye parasite Phrixocephalus cin-
cinnatus Wilson 1908 (Copepoda; Lernaeoceridae) in
Canadian Pacific waters. J. Fish. Res. Board Can. 31:1589-
1595.
Langton, R. W.
1982. Diet overlap between Atlantic cod, Gadus morhua,
silver hake, Merluccius bilinearis, and fifteen other North-
west Atlantic finfish. Fish. Bull., U.S. 80:745-759.
Linton, L. R., R. W. Davies, and F. J. Wrona.
1981. Resource utilization indices: an assessment. J. Anim.
Ecol. 50:283-292.
Moiseev, P. A.
1953. Treska i Kambaly dalnevestochnykh morei (Cod and
flounders of Far-Eastern seas). [In Russ.] Izv. Tikhook-
ean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr. 40:1-287.
(Transl. by Transl. Bur. Can. Dep. Seer. State, 576 p.,
available as Fish. Res. Board Can. Transl. Ser. 119.)
Norman, J. R.
1934. A systematic monograph of the flatfishes (Hetero-
somata). Vol. I.: Psettodidae, Bothidae, Pleuronectidae.
Trustees Br. Mus., Lond., 459 p. (Available from Johnson
Reprint, N.Y., 1966.)
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.
Ranck, C, F. Utter, G. Milner, and G. B. Smith.
1986. Genetic confirmation of specific distinction of arrow-
tooth flounder, Atheresthes stomias, and Kamchatka
flounder, A. evermanni. Fish. Bull., U.S. 84:222-226.
Schoener, T. W.
1970. Non-synchronous spatial overlap of lizards in patchy
habitats. Ecology 51:408-418.
Shuntov, V. P.
1970. Sezonnoe respredelenie chernogo i strelozubykh
paltusov v Beringovum more (Seasonal distribution of black
and arrow-tooth halibuts in the Bering Sea). [In Russ.]
Tr. Vses. Nauchno-Issled. Inst. Morsk. Rybn. Khoz,
Okeanogr. 70 (Izv. Tikhookean. Nauchno-Issled. Inst. Rybn.
Khoz. Okeanogr. 72):391-401. [Transl. by Isr. Program Sci.
Transl., 1972, In P. A. Moiseev (editor), Soviet fisheries in-
vestigations in the northeastern Pacific, Part 5, p. 397-408.
Available from U.S. Dep. Commer., Natl. Tech. Inf. Serv.,
Springfield, VA, as TT 71-50127.]
Smith, G. B., and R. Bakkala.
1982. Demersal fish resources of the eastern Bering Sea:
spring 1976. U.S. Dep. Commer., NOAA Tech. Rep. NMFS
SSRF-754, 129 p.
Smith, R. L., A. C. Paulson, and J. R. Rose.
1978. Food and feeding relationships in the benthic and
demersal fishes of the Gulf of Alaska and Bering Sea. In
Environmental assessment of the Alaskan Continental Shelf,
Final Rep., Biol. Stud. 1:33-107. U.S. Dep. Commer.,
NOAA, Environ. Res. Lab., Boulder, CO.
Traynor, J. J.
In press. Midwater abundance of walleye pollock in the
eastern Bering Sea, 1979 and 1982. Bull., Int. North. Pac.
Fish. Comm.
WlLLIMOVSKY, N. J., A. PEDEN, AND J. PEPPAR.
1967. Systematics of six demersal fishes of the North Pacific
Ocean. Fish. Res. Board Can., Tech. Rep. 34, 95 p.
623
ECOLOGY OF CERIANTHARIA (COELENTERATA, ANTHOZOA) OF
THE NORTHWEST ATLANTIC FROM CAPE HATTERAS TO NOVA SCOTIA
Andrew N. Shepard,1 Roger B. Theroux,2 Richard A. Cooper,1
and Joseph R. Uzmann2
ABSTRACT
Ceriantharia, tube dwelling anthozoans, were collected in grab samples and documented by direct obser-
vations and photographs from research submersibles on the continental shelf and slope off the northeast
United States coast (Cape Hatteras to Nova Scotia). Two species [{Cerianthus borealis Verrill and Cerian-
theopsis americanus (Agassiz)] were identified from grab samples and four species, probably including
C. borealis, were observed from submersibles.
Ceriantharia distribution in relation to latitude, depth, temperature, and sediments was examined.
They occurred throughout the study area, abundantly at depths of 0 to 500 m and less abundantly from
900 to 2,400 m. Ceriantharia habitats displayed an extreme range in bottom water temperature (sum-
mer maximum minus winter minimum) of from 8° to 16°C, and had every sediment type, except 100%
gravel and coarse shifting sand. Geographic and bathymetric zonation is attributed primarily to tem-
perature and secondarily to food supply and substrate type.
Ceriantharia distribution patterns, in submarine canyon heads at depths of <400 m, were determined
from photographic transects run with submersibles; observed patchiness may be related to local differences
in food supply, sediments, and microtopography.
The motile megafauna associated with Ceriantharia "forest" areas and the infauna and epifauna
inhabiting ceriantharian tubes were evidence to show that tubes may enhance local species diversity and
abundance in featureless soft-bottom areas by 1) attracting motile species seeking cover and 2), acting
as a stable, elevated substrate for tubiculous and suspension feeding macrofauna.
The possibility of exploitation of energy reserves
beneath the northwest Atlantic outer continental
shelf and slope has prompted many new studies and
the reexamination of past investigations for baseline
information on the region's seafloor communities.
Research submersible studies of potential oil lease
tracts identified "indicator species" for assessing
environmental changes owing to drilling activities.
We considered Ceriantharia suitable for this purpose
because they were abundant, passive suspension
feeders, and nonmobile. Literature searches re-
vealed that very little has been published on the
Ceriantharia species occurring from Cape Hatteras
to Nova Scotia. This is surprising in light of the
group's significant contribution to the benthic bio-
mass of the region (Wigley and Theroux 1981) and
the important functional role [the effect a species
has on the distribution and abundance of other
residents (Sutherland 1978)] Ceriantharia may have
in structuring communities inhabiting featureless
soft-bottom substrate (O'Connor et al. 1977).
Woods Hole Laboratory, Northeast Fisheries
Center (NEFC), National Marine Fisheries Service
(NMFS), personnel have reported on the general
composition and distribution of invertebrate fauna
of the New England and Mid- Atlantic Bight con-
tinental shelf and slope (e.g., Wigley and Theroux
1981; Theroux and Wigley 19843; Cooper et al, in
press). Data on Ceriantharia were collected during
ecological studies pertaining to various kinds of
demersal fishes and benthic invertebrates: 1) a grab
sample survey (Fig. 1) done from 1955 to 1969
(Shepard and Theroux 19834), and 2) observations,
photographs, and limited sample collections from
research submersible studies. Dredge and trawl data
were available (Shepard and Theroux fn. 4), but not
analyzed since deep burrowing Ceriantharia (some-
'NOAA National Undersea Research Program, University of
Connecticut, Avery Point, Groton, CT 06340.
2Northeast Fisheries Center Woods Hole Laboratory, National
Marine Fisheries Service, NOAA, Woods Hole, MA 02543.
3Theroux, R. B., and R. L. Wigley. 1984. Quantitative com-
position and distribution of macrobenthic invertebrate fauna of the
New England Region. Unpubl. Manuscr. Northeast Fisheries
Center Woods Hole Laboratory, National Marine Fisheries Ser-
vice, NOAA, Woods Hole, MA 02543.
"Shepard, A. N., and R. B. Theroux. 1983. Distribution of
Cerianthids (Coelenterata, Anthozoa, Ceriantharia) on the U.S.
East Coast Continental Margin, 1955-1969: Collection data and
environmental measurements. Lab Ref. Doc. 83-12, 24 p. North-
east Fisheries Center Woods Hole Laboratory, National Marine
Fisheries Service, NOAA, Woods Hole, MA 02543.
Manuscript accepted September 1985.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
625
H i 1 1
FISHERY BULLETIN: VOL. 84, NO. 3
45°
-40°
ATLANTIC
OCEAN
Figure 1. -Chart of the northwest Atlantic from lat. 35° to 45°N (Cape Hatteras to Nova Scotia) showing stations where grab
samples of macrobenthic invertebrates were obtained, and the location of submarine canyons visited with research submersibles
(1 fm = 1.83 m).
times more than 1 m; Sebens5) may be poorly
sampled by dragged collection gear.
BK. P. Sebens, Maritime Studies Center, Northeastern Univer-
sity, Nahant, MA 01908, pers. commun. February 1985.
The objectives of this study are to describe 1) the
Ceriantharia species encountered, 2) their general
distribution in relation to latitude, depth, tempera-
ture, and sediments, 3) their local distribution pat-
626
SHEPARD ET AL.: ECOLOGY OF CERIANTHARIA
terns, and 4) how they interact with other benthic
species.
CERIANTHARIA
Ceriantharians represent a small, incompletely
described order of Anthozoa. Species identification
is difficult, and many species probably remain
undescribed since twice as many larval forms as
adults are known (Hartog 1977; Hartog6). Two
northwest Atlantic species have been identified;
Cerianthus borealis Verrill (1873) (see also Parker
1900; Kingsley 1904; Widersten 1976) and Cerian-
theopsis americanus (Agassiz 1859) (see also Ver-
rill 1864; McMurrich 1890; Parker 1900; Carlgren
1912; Field 1949; Widersten 1976). Two other un-
identified species have been found on the continental
slope (Grassle et al. 1975; Hecker et al. 1980; Valen-
tine et al. 1980; Sebens in press). Table 1 sum-
marizes the geographic and bathymetric ranges of
the above four species.
Ceriantharia live in permanent semirigid tubes
composed of a type of cnidae peculiar to the Order
(called ptychocysts by Mariscal et al. 1977), mucus,
and adhering substrate debris (Emig et al. 1972).
The feltlike tube is usually deep purple in coloration
and distinct enough to be used alone as evidence of
Ceriantharia presence. New England bottom trawl
fishermen are familiar with nets fouled with cerian-
tharian tubes (Rogers 1979). In contrast to other
burrowing anemones which have a single whorl of
tentacles, Ceriantharia have two distinct whorls
(marginal and oral tentacles) which remain outside
the tube during feeding and rapidly retract into the
tube when disturbed.
Ceriantharia are protandric hermaphrodites;
gametes are produced in the mesenteries and fer-
tilization is external. The larvae are pelagic and
duration of the planktonic stage is variable (Carlgren
1912; Hyman 1940; Robson 1966; TRIGOM-PARC
1974). Adults are capable of oral disc regeneration
by budding (Hyman 1940; Frey 1970). Asexual
reproduction has been described for at least one
species, Aracnanthus oligopodus (Cerfontaine 1909).
Ceriantharia are carnivorous passive suspension
or impingement feeders (Emig et al. 1972; Carac-
ciola and Steimle 1983). Digestion may begin in the
tentacles, and larger particles are primarily taken
up in the endoderm of sterile septa (Tiffon and
Daireaux 1974). Fish species inhabiting the region,
including cod, haddock, flounder, scup, and skate
are known predators of whole juvenile Ceriantharia
(Bowman and Michaels7) and may graze the tenta-
cles of adults (TRIGOM-PARC 1974). Off the U.S.
west coast, a nudibranch, Dendronotus iris Cooper,
preys on adult Ceriantharia (Wobber 1970).
Previous documentation of Ceriantharia in the
northwest Atlantic has come from grab samples
(Sanders 1956; Wigley 1968; Pearce 1972; Pearce
et al. 1976; Pearce et al. 1981; Reid et al. 1981;
Wigley and Theroux 1981; Caracciola and Steimle
1983) and submersibles (Grassle et al. 1975; Rowe
et al. 1975; Hecker et al. 1980; Valentine et al. 1980).
However, no studies in the region report exclusive-
ly on ceriantharian ecology.
6J. C. den Hartog, Curator of Coelenterata, Rijksmuseum van
Natuurlijke Historie, Postbus 9517, 2300 RA Leiden, Netherlands,
pers. commun. March 1983.
7Bowman, R., and W. Michaels. 1983. Unpubl. data. Food
Habits Program, Northeast Fisheries Center Woods Hole Labor-
atory, National Marine Fisheries Service, NOAA, Woods Hole, MA
02543.
Table 1. — Morphologic descriptions and geographic and bathymetric ranges of previously
described Ceriantharia species inhabiting the study area.
Species
General morphologic
description
Geographic range
Bathymetric
range (m)
Ceriantheopsis
americanus
see Verrill 1864
Cape Cod to Florida1
20-370
Cerianthus
borealis
see Verrill 1873
Arctic to Cape Hatteras1
10-4500
Unidentified
species I5
small (<5 cm contracted),
dark brown tentacles,
tube flush to seafloor.5
Continental slope off
New England
5'6'7>1,000
Cerianthid A8
larger than unidentified
species I, uniformly dark
tentacles, tube flush to
seafloor5
Continental slope off
New England
5,6,7,8>1500
1 Parker 1900.
2Field 1949.
3Pearce et al. 1981.
"Miner 1950, p. 196.
5Sebens in press.
6Grassle et al. 1975.
7Hecker et al. 1980.
Valentine et al. 1980.
627
FISHERY BULLETIN: VOL. 84, NO. 3
METHODS
Grab sample methodology (gear description, sam-
ple processing, data reduction, bathymetry, tem-
perature, and sediments) is reported in Wigley and
Theroux (1981). A chi-square (x2) test, employing
contingency tables (Richmond 1964), was used to
assess ceriantharian occurrence at grab sample sta-
tions (relation to latitude, depth, bottom water
temperature, and sediment type).
Table 2 lists the submersibles used and sampling
gear employed by each. Quantitative data were ob-
tained with externally mounted 35 mm camera-
strobe systems. Qualitative ecological and behavioral
information was acquired with 35 mm hand-held
cameras, audio tapes, and video tapes made with a
hand-held or externally mounted video camera. In
situ faunal and sediment collections were made with
the submersibles' manipulator arms. Only those
dives performed to assess the distribution of mega-
benthos and associated habitat types were analyzed.
The externally mounted 35 mm camera systems
used on Nekton Gamma, Johnson-Sea-Link, and
Alvin were quantitatively calibrated, assessing 3.6
m2, 7.0 m2, and 15.0 m2 of ocean floor per photo-
graphic frame, respectively (Bland et al. 1976;
Cooper and Uzmann 19818).
Photographs were read on either a light table with
a hand-held magnifying glass or motorized micro-
film reader with a 36 x 36 cm screen and 15 x
magnification lens. Each photograph was time-
annotated, thus allowing correlation with depth,
8Cooper, R. A., and J. R. Uzmann. 1981. Georges Bank and
Submarine Canyon living resources and habitat baselines in oil and
gas drilling areas. Northeast Monitoring Program Annual Report
for FY 80. Unpubl. manuscr., 34 p. Northeast Fisheries Center
Woods Hole Laboratory, National Marine Fisheries Service,
NOAA, Woods Hole, MA 02543.
temperature, slope angle, substrate-habitat type,
and current speed and direction documented on
hand-held audio recorders during the dives.
RESULTS
Species Identification
Ceriantharia occurred at 229 of the 1,295 grab
sample stations; 990 anemones were caught at 139
stations, whole tubes only at 29 stations, and tube
fragments at 61 stations (Fig. 2). Two species, Ceri-
antheopsis americanus and Cerianthus borealis,
were identified from grab samples (at four stations),
the remaining anemones were identified only as
Ceriantharia. The mean blotted wet weight of the
990 anemones was 5.0 g (95% C.L. = ±3.6); how-
ever, more than 90% weighed less than the mean.
Ceriantharia occurred at 82% of the submersible
dive sites (Appendix Tables 1, 2) and at every ma-
jor geographic feature visited (Fig. 2, Table 3). Sub-
mersible samples have not yet yielded anemones
suitable for identification to the species level. Figure
3 shows three of the four species (Cerianthids A, B,
C, and D) photographed from submersibles, and
Table 3 classifies the species by morphological
features apparent in photographs.
The minimum gross Ceriantharia size (height
above seafloor or width of exposed tentacle crown
and/or tube) visible in photographs was about 5 cm.
It was not unusual to see large Cerianthid B or C
tubes 20 cm above the seafloor. Based on laboratory
examination of 61 anemones and a few specimens
which were photographed in situ and then collected
with the manipulator arm, a gross size of 5 cm cor-
responds to an anemone wet weight of about 16 g
(3 times the mean weight of anemones captured with
grab samplers).
Table 2.— Submersible, cruise year, and gear used for data col-
lection. PC8 = Perry Model C8, NG = Nekton Gamma, AL =
Alvin, and JSL = Johnson-Sea-Link.
In situ
Submersible/
Audio
Video
35
mm
photographs
collections
of fauna/
year
tapes
tapes
Hand-held
External
substrate
PC8/1971
X
X
NG/1973
X
X
X
NG/1974
X
X
X
NG/1979
X
X
X
AL/1975
X
X
X
X
AL/1976
X
X
X
AL/1978
X
X
X
AL/1980
X
X
X
X
JSL/1980
X
X
X
X
JSL/1981
X
X
X
X
Relation to Latitude
Ceriantharia occurrence at grab sample stations
was not independent of latitude (x2, P < 0.05). Oc-
currence was highest in three areas: off Chesapeake
Bay Gat. 37° to 38°N); south of Cape Cod in the zone
also including the southern half of Georges Bank
(lat. 40° to 41°N); and on the shelf off Nova Scotia
(lat. 44° to 45 °N) (Fig. 4).
From submersibles, Cerianthid B was the only
species seen on Georges Bank, or north of 41 °N
[Wilkinson Basin (Gulf of Maine) and Corsair
Canyon]; Cerianthids A, C, and D were all seen in
canyons or on the slope south of Georges Bank
(Table 3).
628
SHEPARD ET AL.: ECOLOGY OF CERIANTHARIA
H 1 1 1 i
TLANTIC
OCEAN
O GRAB SAMPLE STATIONS
□ SUBMERSIBLE DIVE(S)
■/OOfm
Figure 2.— Chart showing the submersible dive(s) sites and grab sample stations containing Ceriantharia. Symbols for submersible
dive(s) sites often circumscribe more than one dive, since at this scale some dives were too close together to distinguish with separate
symbols (1 fm = 1.83 m).
Relation to Bathymetry
In grab samples, Ceriantharia were found at
depths from 6 to 2,329 m, but occurrence was not
independent of depth (x2, P < 0.05). Occurrence
was highest from 0 to 100 m, and no Ceriantharia
were caught from 501 to 900 m (Fig. 4).
Submersible dive depth range was 80 to 1,930 m
(Appendix Tables 1, 2). Cerianthids B, C, and D were
seen within the 80-400 m range, no species were
629
FISHERY BULLETIN: VOL. 84, NO. 3
Figure 3.— A, B, C, - black and white prints of 35 mm Ektachrome transparencies from a hand-held
camera; D - from externally mounted 35 mm brow camera. A. Alvin dive 838, axis of Oceanographer
Canyon, 1,740 m: Cerianthid A (dark anemones); white brittle stars, Ophiomusium sp.; sea urchins,
Echinus affinus; and a grenadier (Macrouridae) on a calcareous silt-sand substrate. B. Nekton Gamma
1974 dive 30, head of Lydonia Canyon, 300 m: Cerianthid B with a blackbelly rosefish, Helicolenus dac-
630
SHEPARD ET AL.: ECOLOGY OF CERIANTHARIA
tylopterus, at its tube base, on silt-clay substrate. C. Nekton Gamma 1974 dive 30, 300 m: Cerianthid
B with a portunid crab, Bathynectes sp., at its tube base on silt-clay substrate. D. Nekton Gamma 1979
dive 3, head of Block Canyon, 150 m: Cerianthid C with tube epifauna (sponges and colonial white
anemones), and redfish, Sebastes sp., just visible near center of the photograph on a silt-clay substrate,
current direction was from left to right.
631
FISHERY BULLETIN: VOL. 84, NO. 3
Table 3.— Morphological features, apparent in photographs taken from submersibles, used to
distinguish between four Ceriantharia species seen, and the geographic areas and bathymetric
ranges in which they were found (cf. Fig. 3, Appendix Tables 1 and 2).
Species
Tube height
in relation
to seafloor
Above Flush
Characteristics of marg
Length Arrangement
nal tentacles
Coloration
Geo-
graphic
areas1
Depth
range
(m x 100)
A
X
unequal
multiplanar2
dark red,
black
6,8
16-19
B
X
unequal
multiplanar
pale purple,
pink, tan,
or brown
1-8, 10
1-4
C
X
equal
parabolic2
white with
purple marks
4,9
2-4
D
X
unequal
multiplanar
greenish
yellow
10
2-3
11 - Wilkinson Basin, Gulf of Maine; 2 - Georges Bank; 3 - Corsair Canyon; 4 - Lydonia Canyon; 5 - Gilbert
Canyon; 6 - Oceanographer Canyon; 7 - Hydrographer Canyon; 8 - Veatch Canyon; 9 - Block Canyon; 10 - Hud-
son Canyon.
2Used by Meyer (1980) to characterize feeding nets of other passive suspension feeders.
U
0
23
1
3
U 20
IS
IB
S
0
30
23
20
IS
10
S
0
3 5 9 16
DEPTH (M X IBB)
■
p
•
n
1
1
\\^
sAA
\V
,\v
4 8 12 16 20
TEMPERATURE RRNGE (AT.°C)
_ra.
1
p
1
^
s
^
^
s
2 3 4
SEDIMENT TYPE
observed at depths from 400 to 1,600 m, and Ceri-
anthid A was seen at depths from 1,600 to 1,930 m
(Table 3).
Relation to Bottom Water Temperature
Temperature observations were sparse for grab
sample stations, so, the extreme range of temper-
ature (A T), a commonly used measure of climatic
variability (MacArthur 1975), was used to compare
temperature with Ceriantharia distribution; A T
equals the difference between extreme annual
recorded temperatures (summer high minus winter
low), obtained from various published sources, and
measurements, made by the NEFC. Site ranges
were grouped for plotting: 0° to 3.9°C, 4° to 7.9°C,
8° to 11.9°C, 12° to 15.9°C, 16° to 19.9°C, and
>19.9°C. Temperature range changed significant-
ly with latitude and depth. Largest A T's generally
dominated shelf waters south of lat. 41°N, and in-
shore waters (Fig. 5).
Ceriantharia occurrence at grab sample stations
was not independent of temperature range (x2, P <
0.05); occurrence was highest on the continental
shelf where A T was from 8° to 15.9°C (Fig. 4).
All submersible dives were performed in July or
August. Bottom water temperatures (external
Figure 4.— Ceriantharia occurrence (% of grab sample stations)
in relation to latitude, depth, temperature range (AT = summer
high minus winter low), and sediment type. Depth stratum size
was determined by pooling, from shallow to deep, adjacent 100
m depth intervals until enough observations were available for a
chi-square test. Sediment type codes are 1 - gravel; 2 -
gravel/sand, silt, mud or clay; 3 - sand; 4 - silt/sand; 5 - silt/clay.
632
SHEPARD ET AL.: ECOLOGY OF CERIANTHARIA
Figure 5.— Distribution of extreme range in bot-
tom water temperature (summer maximum minus
winter minimum) in the Middle Atlantic Bight
(from Wigley and Theroux 1981) and New England
region (Theroux and Wigley, text footnote 3).
Cape Hatteras
633
FISHERY BULLETIN: VOL. 84, NO. 3
thermometer observations) decreased with depth;
temperatures ranged from 5° to 13 °C at depths
<500 m and declined gradually from 5°C at 500 m
to 3.5°C at 1,900 m (Appendix Tables 1, 2). Depth-
temperature profiles of three Alvin dives (Fig. 6)
indicate depths of 500 to 600 m were a transition
zone; deeper bottom water temperatures decreased
little with depth, in comparison to shallower tem-
peratures. Cerianthids B, C, and D were seen at
temperatures of 5.3° to 13.0°C, and Cerianthid A
was observed only in colder, deeper water, in the
narrow range of3.5°to3.9°C (Appendix Tables 1,
2).
0?
Q
X
Q.
U
O
10
12 •
TEMPERATURE (°C)
2 4 S 8 10
i i i i 1 1 r 1 i
* - #576
0 - #578
+ - #579
Figure 6.— Depth-temperature profiles constructed from obser-
vations (of external thermometers) made on the bottom during
three Alvin dives in Veatch Canyon. Temperature stabilized at
about 500-600 m.
Relation to Sediments
Ceriantharia occurrence at grab sample stations
was not independent of sediment type (x2, P <
0.05); they rarely inhabited 100% gravel sediments
(Fig. 4). However, when stations with 100% gravel
sediments were not included, occurrence was in-
dependent of sediment type (x2, P > 0.05). Al-
though occurrence in silt-clay sediments was lower
than in other unconsolidated sediments (Fig. 4), this
may be a result of the large proportion of silt-clay
sediment stations at depths >500 m, where Ceri-
antharia were scarcer; if only silt-clay sediments
from shallower than 500 m are analyzed, occurrence
is more than 20%.
Photographic transect profiles of submersible
dives (Appendix Table 2, depths <400 m) provided
information on Ceriantharia abundance with respect
to substrate, depth, temperature, transect direction,
and distance (Figure 7 shows one profile). Based on
the number of sightings in various substrata (Ap-
pendix Tables 1, 2) and the transect profiles, about
70% of the Ceriantharia inhabited silt-sand and silt-
clay sediments. However, they also commonly
occurred in rarer gravelly substrates (less than
about 50% gravel cover on sand or clay; only about
20% of the total seafloor viewed). They were not
seen in coarse sand sediments (usually rippled and/or
in dune formations).
The clay substrate observed from submersibles
was actually a semiconsolidated mud (Cooper et al.
in press); the term clay was used to differentiate it
from sand substrates, but clay may only be a minor
constituent.
Spatial Pattern
Ceriantharia density and biomass estimates from
grab sample data were determined for comparison
to other studies (e.g., Sanders 1956; Pearce et al.
1981; Reid et al. 1981; Caracciola and Steimle 1983).
However, because no replicate sampling was done
at over 90% of the stations, density and biomass
were not analyzed further. For stations with
anemones or whole tubes, mean density was 35.7
m"2 (N = 168, 95% C.L. = ±12.1, range = 1.7 to
1,370 m~2). Mean station biomass (anemone blotted
wet weight) was 48.6 g m~2 (N = 139, 95% C.L. =
±35.4).
On the quantitative submersible dives, Cerian-
tharia density ranged from 0 to 0.414 m~2 dive-1
(Appendix Table 2). The maximum density in one
photographic frame was 6.6 m~2. The photographic
transect profiles (Fig. 7) showed Ceriantharia
populations shallower than 400 m were spatially ag-
gregated. No quantitative information was available
for the Cerianthid A populations seen in the axes
of Oceanographer and Veatch Canyons.
The largest aggregation encountered (head of
Lydonia Canyon, Fig. 7) was over 0.5 km wide and
composed mostly of Cerianthid B, with some Cerian-
thid C individuals. The dives were run over a perma-
nent station marker (37 khz pinger) positioned on
a 14-15 m high knoll. Substrate atop the knoll was
gravel-sand, near the base and surrounding the knoll
was silt-sand. Approximately half of the Cerian-
tharia aggregation occupied the gravel-sand sedi-
ments. Ceriantharia were the dominant megafauna
in the area, other common megafauna were gala-
theid crabs, Munida iris Milne-Edwards, and
634
SHEPARD ET AL.: ECOLOGY OF CERIANTHARIA
IA
O
I
a.
o
x
<
cc
Id
IB
IA
SUBSTRATE
152 M
151 M
i i i i — i — T — r
200. 250.
PHOTO #
— i — i — i — r
400.
0.0
0.6*
TRANSECT LOCATION (KM)
1.2
Figure 7.— One example, from 1980 Johnson-Sea-Link dives 15 and 16 in Lydonia Canyon, of the photograph-by-photograph transect
profiles of Ceriantharia abundance constructed for quantitative submersible dives during which Ceriantharia density exceeded 0.1
m"2 dive"1, at depths of less than 400 m. Substrate codes: 1 - sand base, IA - silt veneer, IB - greater than 5% gravel cover.
A permanent station marker (37 khz pinger) was located at 0.6 km into the transect, as denoted by the asterisk.
asteroids on gravel-sand, and shell-less hermit crabs,
Catapagurus sp., on silt-sand. Galatheids were also
observed on silt-sand sediments, often near cerian-
tharian tubes. A qualitative observation made on
several submersible dives was that Ceriantharia
"forests" (aggregations) were often associated with
rises in seafloor topography.
Functional Role
Figure 8 (data from 1979 Nekton Gamma dive #3
in Block Canyon) shows Cerianthid C frequency of
occurrence and number of associated species (diver-
sity) plotted by photographic frame. The substrate
throughout the dive was a low-relief silt-clay, and
-i — i — i — i — | — i — n — | V i — i — | — i — i — i — | — i — i — i — | — i-
20 40 60 80 100 120 140 160
PHOTO n
Figure 8.— Cerianthid C abundance and diversity (number of species) of associated
fauna along a 1.0 km photographic transect from 1979 Nekton Gamma dive #3.
Each data point represents the sum of 5 adjacent photographic frames: species
diversity increased significantly in areas with Ceriantharia (Mann-Whitney test,
P < 0.01).
635
FISHERY BULLETIN: VOL. 84, NO. 3
the depth and temperature ranges were 137 to 183
m, and 13.0° to 10.7°C. Mean number of species was
significantly higher in photographs with Cerian-
tharia (Mann-Whitney test, P < 0.01): Three groups
of epifauna (hydroids, sponges, and small white
anemones; Fig. 3D) were attached to Ceriantharia
tubes only and not found on the surrounding sub-
strate. Also, blackbelly rosefish, Helicolenus dacty-
lopterus (De La Roche) (Fig. 3B), and redfish,
Sebastes sp. (Fig. 3D), abundances were higher in
the Cerianthid C patch (0.40/frame and 0.18/frame,
respectively) than in the adjacent area (0.03/frame
and 0.00/frame); about half of the fish were nestled
at tube bases.
At other dive locations, motile megafaunal species
often seen nestled near tubes included portunid
crabs (Bathynectes sp.) (Fig. 3C); jonah crabs, Cancer
sp.; pandalid shrimps, Pandalus sp.; American
lobsters, Homarus americanus Milne-Edwards;
hakes, Urophycis spp.; and greeneyes Chloropthal-
mus agassizii Bonaparte.
Two Cerianthid B tubes (50 m apart) and adjacent
sediments were collected with the grab sampler of
the submersible Johnson-Sea-Link, in the head of
Oceanographer Canyon at a depth of 293 m. The
tubes were separated from the adjacent sediments
immediately after the submersible surfaced. The
volume of each tube was less than the volume of ad-
jacent sediments (80% fine sand, <0.5 mm; 10%
coarse sand; 10% silt) (Appendix Table 3). After
preservation and staining, the macrofauna (>0.5
mm) were identified for each sample (Appendix
Table 3): Polychaetes were dominant and the three
most abundant polychaete species inhabiting the
Ceriantharia tubes were absent or scarce in the ad-
jacent sediments; Polycirrus eximius (Leily) (a
tentacle feeder which sweeps the water and sub-
stratum for food), Marphysa sp. (a jawed omnivore),
and a filter-feeder, Potamilla neglecta (Sars)
(Fauchald 1977; Fauchald and Jumars 1979).
DISCUSSION
Collection Gear
Gear differences largely account for the differ-
ences in Ceriantharia size and density estimates
from grab samples versus photographs. Due to
limitations in resolution, photographs provide valid
data only on larger epifauna (Emery et al. 1965;
Barham et al. 1967; Wigley and Emery 1967). How-
ever, since the estimated depth of penetration of a
0.1 m2 Smith-Mclntyre grab sampler, the gear used
most frequently in this study, is only 3 to 5 cm in
unconsolidated substrates (Smith and Mclntyre
1954), and large ceriantharian tubes often extend
much deeper than 5 cm below the seafloor (Sebens
fn. 5), making them difficult to dislodge, if the
primary objective is to sample large individuals and
document the associations between tubes and other
fauna, then photographs and direct observations are
more useful than grab samples.
Species Identification
Ceriantheopsis americanus and Cerianthus
borealis, identified from grab samples, occurred
within the geographic and bathymetric ranges noted
previously for these species (Table 1). Unfortunately,
many Ceriantharia samples were discarded, and
none of the available samples from depths greater
than 500 m contained anemones for taxonomic
identification.
The morphological features used to distinguish
between the four species seen from submersibles
(Table 3) may not individually be reliable; tentacle
coloration may vary noticeably within a species (Arai
1971; Uchida 1979). However, taken together, we
feel the features were consistent enough to indicate
we saw four species of adult Ceriantharia: C.
borealis (probably Cerianthid B), two unidentified
species (Cerianthids C and D) from depths shallower
than about 500 m, and another unidentified species
(Cerianthid A) living deeper down the continental
slope.
The conclusion that Cerianthid B is C. borealis is
based on the similarities between our descriptions
of Cerianthid B morphology and distribution (Table
3), and information from other studies on C. borealis
(Table 1; Gosner 1979). The only other previously
identified inhabitant of the study area, C. ameri-
canus, was probably not encountered on our sub-
mersible dives; the deepest record found for C.
americanus was about 70 m (Pearce et al. 1981),
whereas our shallowest submersible dive was to a
depth of 80 m.
Sebens (in press) described two unidentified Ceri-
antharia species which occur at depths >1,000 m in
the Northwest Atlantic: Unidentified Species II
(seen at depths >1,500 m) resembles Cerianthid A
(Table 3, Fig. 3A), Cerianthid A in Valentine et al.
(1980), and a photograph of unidentified Cerian-
tharia taken by Grassle et al. (1975) at depths of
1,550 to 1,830 m just south of New England. The
distinction Sebens (in press) makes between Uniden-
tified Species I (seen at depths of >1,000 m) and
Unidentified Species II (Cerianthid A) is that Species
II is smaller (Table 1). Grassle et al. (1975) and
636
SHEPARD ET AL.: ECOLOGY OF CERIANTHARIA
Hecker et al. (1980) also reported seeing small
unidentified Ceriantharia at about 1,300 and 1,000
m, respectively. We saw (from submersibles) no
Ceriantharia from 1,000 to 1,600 m for comparison.
In addition to the six documented species above,
other Ceriantharia sighted in or near the region in-
clude two possible species photographed by Hecker9:
one at depths of 1,800 to 2,800 m (from Lydonia
Canyon to Cape Lookout, NC), which resembles a
stout black Cerianthid B, and another resembling
Cerianthid A (except its tube extends above the
seafloor) at depths of 500 to 1,000 m off Cape Hat-
teras. Rowe and Menzies (1969) photographed
Ceriantharia on the continental slope (at depths of
400 to 3,000 m) south of Cape Hatteras (about lat.
34 °N) which they guessed to be Ceriantheomorphe
brasiliensis Carlgren. However, they presented no
photographs for comparison and collected no
voucher specimens. The C. brasiliensis specimens
identified by Carlgren (1931) were from Brazil,
South America, and its resemblance to other slope
species is uncertain. Submersible dive time devoted
to in situ documentation and collection of specimens
is obviously needed in order to identify the deep-
water species10.
Relation to Latitude
North of Cape Cod and Georges Bank (lat. 42° to
44 °N) the continental shelf is dominated by the Gulf
of Maine, a feature unlike the rest of the shelf in
the region because of its topographic irregularity
and because it reaches depths of more than 100 m
closer to shore. The lack of tidal mixing below 100
m over much of the gulf, and the fact that the prin-
cipal source of its bottom water is thermally stable
continental slope water introduced through the
Northeast Channel, results in water temperature
stratification which keeps the gulf bottom water
temperatures virtually constant throughout the year
(TRIGOM-PARC 1974; Rowe et al. 1975; Ingham et
al. 1982, p. 43). The narrow extreme range of bot-
tom water temperature (A T) dominant from lat. 42°
to 43°N (Fig. 5) may account for low Ceriantharia
occurrence at grab sample stations there (Fig. 4),
while peaks in occurrence are evident at lat. 40° to
41 °N (shelf just south of Cape Cod, including south-
ern Georges Bank), and from 44° to 45°N (shelf off
9B. Hecker, Lamont-Doherty Geological Observatory, Columbia
University, Palisades, NY 10964, pers. commun. October 1984.
10For all photographed, but unidentified slope species, we know
of only one voucher specimen (of Unidentified Species I), present-
ly located at the Harvard Museum of Comparative Zoology, Cam-
bridge, MA.
Nova Scotia) may be associated with more favorable
intermediate temperature ranges which prevail
there (8° to 15.9°C). High Ceriantharia occurrence
at grab sample stations between 37° to 38 °N is in
part due to high occurrence at stations in the lower
half of Chesapeake Bay; occurrence was 56% at nine
Bay Stations and 23% at 52 shelf/slope stations.
However, our data is too sparse and inconclusive to
make a bay versus non-bay comparison, or explain
the high occurrence at shelf stations in this area.
According to Gosner (1971), the continental
margin from Cape Hatteras to Nova Scotia is
divided into two faunal provinces with respect to
benthic invertebrates: a Boreal (cold-temperate)
province north of Cape Cod, and a Virginian (warm-
temperate) province of Cape Cod, MA. Theroux (in
press) considers the situation to be more complex
and to depend on the species considered, but agrees
that Cape Cod and Georges Bank are the beginning
of a rapid transition from cold to warm temperate
fauna, and suggests that the transition is associated
with Georges Bank and Nantucket Shoals thermal
fronts (Fig. 5; Ingham et al. 1982, p. 40-41).
Using Gosner's (1971) faunal province descrip-
tions, our submersible data indicate that, in addi-
tion to C. americanus, at least two other warm-
temperate species inhabit the northwest Atlantic
continental shelf (Cerianthids C and D). The only
cold-temperate shelf species, Cerianthid B (probably
C. borealis) ranges south to Cape Hatteras (Tables
1, 3). The last species we saw (Cerianthid A) is
bathyal.
Relation to Bathymetry
Bathymetric zonation of benthic fauna has been
previously described for the continental shelf-slope
region of the northwest Atlantic (Wigley and Emery
1967; Rowe and Menzies 1969; Sanders and Hessler
1969; Rowe 1972; Grassle et al. 1975; Haedrich et
al. 1975, 1980; Hecker et al. 1980; Valentine et al.
1980; Wigley and Theroux 1981). Rowe et al. (1982)
cautioned, "'zones' that previous investigations
have described apparently are a function both of the
animal groups studied and distribution of samples
with depth". Thus, our discussion of Ceriantharia
zonation is limited to depths <2,000 m, since below
that depth there were no submersible data to sup-
port the grab sample data.
Ceriantharia distribution, as determined from the
grab sample data (Fig. 4), our submersible obser-
vations (Table 3), and data from other investigations
(Table 1) imply boundaries (defined here as depths
characterized by distinct changes in the benthic com-
637
FISHERY BULLETIN: VOL. 84, NO. 3
munity's species composition) to Ceriantharia
distribution exist at about 500, 900, and 1,600 m.
Our submersible data indicate that shelf species
were confined to depths of less than about 400 m,
and the bathyal species (Cerianthid A) was seen
between 1,600 and 2,000 m. Published reports in-
dicate another unidentified species lives deeper than
about 1,000 m (Grassle et al. 1975; Hecker et al.
1980; Sebens in press). Similar depth zonation of
slope fauna inhabiting the study area have been
reported for isopods (Menzies et al. 1973), demer-
sal fishes (Musick11), and megafauna captured in
trawls (Haedrich et al. 1980). Some environmental
factors, suggested as causes for observed distribu-
tions, are temperature, sedimentation rates, and
substrate types (summarized by Haedrich et al.
1975, 1980).
The depth interval between about 400 and 600 m
on the continental slope south of New England is
a temperature transition zone; shallower bottom
waters experience larger seasonal temperature
variations than stable deeper waters (Sanders and
Hessler 1969; Haedrich et al. 1975). Depth-temper-
ature profiles (Fig. 6) made on A Ivin dives in Veatch
Canyon showed larger depth related temperature
variations also occurred shallower than 500 to 600
m. The shelf species (Cerianthids B, C, and D) may
not be able to tolerate and/or thrive in the cold stable
conditions below 500 m.
The Cerianthid A population, we saw deeper than
1,600 m in the axis of Oceanographer Canyon, in-
habited sediments high in biogenic carbonates;
canyon axes may act as settling basins for suspended
matter being funneled downcanyon (Valentine et al.
1980). Rowe and Menzies (1969) attributed increases
in suspension-feeder concentration, in photographs
from the upper slope (200-800 m) and at the slope
base (3,000 m) off North Carolina, to increased
detritus accumulation resulting from downslope
movement and concentration by the prevailing bot-
tom currents. Haedrich et al. (1980) stated, in
reference to the depth zonation of megabenthic
fauna on the slope off southern New England, that
"zonation must result to some degree from vary-
ing strategies that promote success along a food
resource gradient".
Haedrich et al. (1975) suggested boundaries to
zones of larger epifauna, at about 400 and 1,000 m
nMusick, J. A. 1976. Community structure of fishes on the
continental slope and rise off the Middle Atlantic Coast of the
U.S. Manuscript presented at Joint Oceanographic Assembly,
Edinburgh, September. (Copies available from: J. A. Musick,
Virginia Institute of Marine Science, Gloucester Point, VA 23062,
USA).
on the continental slope south of New England,
result from physical changes in the slope environ-
ment. Macllvaine (1973, p. 30-70) reported on the
physical environment in the same area (sediment
type, suspended sediments, and slope gradient). The
zone between 400 and 1,000 m consists largely of
homogeneous silt-sand substrate, near-bottom sus-
pended sediments at 520 m were 50 to 60 \xglh
(about 25% organics), and the slope gradient is about
1.4°. Deeper than about 1,000 m there are more
variable sediment features (stiff clayey silt sedi-
ments which are smooth or hummocky, talus slopes,
and rock outcrops), suspended sediments were 20
^g/L (about 45% organics) at 1,000 m and 80 /ig/L
(about 80% organics) at 1,670 m, and the slope
gradient is steeper (7.6°).
Suspension feeders rely on current velocity and
nutrient load for their food supply. Substrate vari-
ability deeper than 1,000 m may enhance Cerian-
tharia occurrence down to 2,000 m: Features such
as hummocks may act as perches for suspension
feeders, placing them up higher where current is
swifter and their food supply is replenished more
rapidly (Hughes 1975; Dyer 1980; Sebens 1984).
Higher suspended sediments and percentage of
organics may further enhance Ceriantharia occur-
rence below 1,600 m, as compared with 1,000 or 520
m. The lesser slope gradient between 400 and 1,000
m probably results in lower near bottom current
velocities; near the shelf-slope break in Ocean-
ographer Canyon, bottom currents are swifter at
105 to 300 m than at 650 m, due primarily to a dif-
ference in slope gradient (Valentine in press). Thus,
increased slope gradient may enhance Ceriantharia
occurrence below 1,000 m.
Other mechanisms may affect ceriantharian depth
zonation such as the direct effects of pressure
(Siebenallar and Somero 1978), or predators (Paine
1966; Rex 1976); however, data were not available
to evaluate these factors.
Submarine canyons received particular attention
during submersible dive activities because of the
potential entrainment of discharges from oil explora-
tion activities into productive canyon environments
(Cooper and Uzmann fn. 8). Bathymetric zonation
of slope fauna may be altered and/or species abun-
dance enhanced by submarine canyons (Rowe 1971;
Haedrich et al. 1975). The conduitlike nature and
substrate heterogeneity of canyons have both been
implied as explanations for observed faunal enrich-
ment in canyons as opposed to adjacent noncanyon
slope areas (Rowe and Menzies 1969; Rowe 1971,
1972; Haedrich et al. 1975; Hecker et al. 1980;
Valentine et al. 1980; Rowe et al. 1982). Although
638
SHEPARD ET AL.: ECOLOGY OF CERIANTHARIA
we had no adjacent slope dives to compare with the
canyon dives, Ceriantharia were common in canyons
and have been suggested to be canyon "indicator"
species (Rowe 1972). In the future, we hope a
canyon-slope comparison of Ceriantharia species'
diversity and abundance will be made.
Relation to Bottom Water Temperature
Wigley and Theroux (1981) found that total macro-
faunal density in the Middle Atlantic Bight generally
increased directly with increasing temperature
range (A T). Ceriantharia occurrence at grab sam-
ple stations followed this trend until A T reached
15.9°C, after which it decreased (Fig. 4). Why an
intermediate temperature range may be favorable
to Ceriantharia is unknown. Wide ranges might en-
tail harmful extremes of temperature, while nar-
rower ones may be too constant at an unfavorable
level, or larval stages may benefit from some degree
of fluctuation for maximal development ( Andrewar-
tha and Birch 1954, p. 129-205). Information on how
temperature affects ceriantharian metabolism,
activity patterns, and development is lacking.
Marine organism distributions are largely con-
trolled by temperature (Hutchins 1947; Crisp 1965;
Gosner 1971). The most obvious effect of tempera-
ture on invertebrate distributions is exclusion of
species from areas with unsuitable thermal regimes
(Kinne 1970). Submersible data on ceriantharian
geographic and bathymetric distribution demon-
strate allopatric speciation which we believe is
primarily a response to temperature.
Relation to Sediments
The presence of silt is characteristic of deposi-
tional areas which may be favorable to suspension
feeders (Rowe and Menzies 1969). Wigley (1968)
described Ceriantharia as common inhabitants of
silty-sand sediments on Georges Bank. Through
resuspension, surficial deposits are potential food
for Ceriantharia (Rhoads 1974). In addition to low
deposition, substrate instability may account for the
scarcity of Ceriantharia in 100% gravel and rippled
coarse sand substrate. Shifting substrates, such as
the 100% gravel sediments at grab sample stations
or the rippled sand dunes observed from submer-
sibles, may harm suspension feeders through
clogging of feeding apparatus, or the burial of lar-
vae (Sanders 1956; Ross 1968; Rhoads and Young
1970; Rhoads 1974).
However, Ceriantharia were generally cosmo-
politan with respect to substrate (Fig. 4; Appendix
Tables 1, 2). They are well adapted to withstand
strong currents, sediment movement, and extreme
deposition of fine material because their tubes pro-
vide firm anchorage (Frey 1970) and protection
against clogging or burial (Pearce 1972). Pearce et
al. (1976) found Ceriantharia were dominant macro-
fauna in fine carbon-rich sediments stressful to other
benthic species, near New York Bight sewage sludge
disposal sites.
Just as 100% gravel substrate is unfavorable for
burrowing, a gravel veneer might also be expected
to limit space available for burrowing. However, on
submersible dives, Ceriantharia were frequently
seen in gravel-covered areas (less than about 50%
gravel cover). These deposits, probably Pleistocene
ice-rafted glacial debris, are exposed in areas which
usually experience higher currents than adjacent
areas (Valentine et al. 1980; Valentine in press), a
favorable consideration for suspension feeders.
Spatial Pattern
Local conditions of food supply, substrate, or
micro topography, may enhance Ceriantharia aggre-
gation (Fig. 7). Local differences in food supply may
allow Ceriantharia to survive in aggregations.
Grassle et al. (1975) observed that strongly clumped
suspension-feeders were able to maintain aggrega-
tions because their food supply was continually
renewed. Unusually high Ceriantharia abundances
near a sewage sludge/dredge spoil disposal area may
have occurred owing to the increased amounts of
organic matter (Pearce et al. 1976).
Grassle et al. (1975) found Ceriantharia, similar
to Cerianthid A, more randomly distributed on the
continental slope, south of Cape Cod (depth of 1,465
to 1,830 m, homogeneous sandy silt-clay substrate).
In comparison, substrata in canyon heads where
aggregations were observed from submersibles are
heterogeneous (Hecker et al. 1980; Valentine et al.
1980). Our grab samples showed the same contrast
between heterogeneous substrata shallower than
500 m and homogeneous silt-sands and clays down-
slope (Shepard and Theroux fn. 4). Since inver-
tebrates are capable of substrate selectivity (Thor-
son 1966; Gray 1974), a variable substrate may be
characterized by patchy inhabitant distributions
(Hecker et al. 1980).
The Cerianthid B aggregation in Lydonia Canyon
(Fig. 7), located on a knoll, may benefit from
elevated positioning and swifter currents (Hughes
1975; Sebens 1984), thus aggregations may also
form in response to local changes in surface
elevation.
639
FISHERY BULLETIN: VOL. 84, NO. 3
Functional Role
An increase in structural complexity of the sub-
strate vertically and/or horizontally increases the
number of microhabitats, and if the appropriate
colonizers and mortality sources are present, within-
habitat diversity will likely be increased (Steimle and
Stone 1973; Abele 1974; Hughes 1975; Woodin 1976,
1978; Connell 1978; Suchanek 1979; Hulbert et al.
1982). Ceriantharia tubes may increase species
diversity and abundance on featureless soft bottom
areas by 1) attracting motile megafauna seeking
refuge near tubes and 2) serving as a favorable
substrate for epifauna and infauna, particularly
suspension-feeders and tubiculous species.
By acting as a three-dimensional refuge, the tubes
may ease predation pressure on smaller motile
species (Ware 1972; Whoriskey 1983). Demersal fish
and crustaceans similar to those we observed have
been noted by others in association with Cerian-
tharia (Uzmann et al. 1977; Hecker et al. 1980;
Valentine et al. 1980). The species most commonly
observed near tubes, Helicolenus dactylopterus,
Sebastes sp., and Bathynectes sp., characteristical-
ly exhibit thigmotactic behavior.
Associations similar to the ones we found between
suspension feeders and Ceriantharia tubes in Block
Canyon (Figs. 3D, 8), and polychaetes and tubes
from Oceanographer Canyon (Appendix Table 3),
have been recorded for Ceriantharia and polychaetes
(Kingsley 1904; O'Connor et al. 1977), phoronids
(Ponder 1971; Emig et al. 1972; Hartog 1977), and
bivalves (Ponder 1971). These associations have
been alternately referred to as commensalism or in-
quilinism; we prefer the latter definition as it high-
lights the role of the ceriantharian tube. Emig et
al. (1972) speculated that Cerianthus maua Carlgren
tentacles may act as baffles, causing waterborne
food particles to settle out, and become available to
suspension feeders (Phoronis australis Haswell) in-
habiting the C. maua tubes, in which case the term
commensalism may be more appropriate. However,
Emig et al. also stated that increased food supply
is probably a secondary benefit to the phoronids and
that the suitability of the tube as a settlement sur-
face for larvae motivates the association. O'Connor
et al. (1977) studied a Pachycerianthus multiplicatus
Carlgren population inhabiting deposit substrates
(85% silt-clay, 15% sand) off Ireland and suggested
tubes were prime settlement surface for the larvae
of inquiline filter-feeding polychaetes, Myxicola in-
fundibulum (Renier). The associates (sponges,
hydroids, and colonial anemones) of Ceriantharia
tubes in Block Canyon are generally nonmotile so
they probably had to arrive on the tubes as larvae.
More unstable substrate surrounding the tubes may
be less suitable as a settlement surface for larvae
of suspension feeders (Rhoads and Young 1970,
1971; Rhoads 1974).
The vertical aspect of Ceriantharia tubes may
enhance diversity and abundance by 1) allowing ver-
tical stratification of trophic types (MacArthur and
Levins 1964; Hughes 1975; Schoener 1975; Ausich
and Bottjer 1982), and 2) affording inhabitants, such
as the filter feeder Potamilla neglecta, elevated feed-
ing stations where clogging by resuspended sedi-
ments is less likely, and current velocities tend to
be greater (Dyer 1980), thus the food supply is more
rapidly renewed (Hughes 1975; Sebens 1984).
The stable nature of the tubes may serve species
behaviorally inclined to attach themselves to firm
substrate. The three species of polychaetes, Poly-
cirrus eximius, Marphysa sp., and Potamilla neglec-
ta, most abundant on ceriantharian tubes caught in
Oceanographer Canyon, but rarely found in the ad-
jacent sediments (Appendix Table 3), usually attach
their tubes to solid surfaces such as stones, algae,
or hydroids (Gosner 1971; Fauchald and Jumars
1979).
Infaunal species may also gain relief from preda-
tion pressure by inhabiting ceriantharian tubes. The
feltlike tubes are generally more consolidated that
the sediments surrounding them, thus more difficult
to graze. Ponder (1971) viewed protection as the
principal benefit to a leptonid bivalve, Montacutona
ceriantha Ponder, inquiline with Cerianthus sp. in
Japanese waters. Protection may be enhanced for
tubiculous infauna since their retraction may be
stimulated by a similar response to disturbance by
the host ceriantharian (Emig et al. 1972).
Ceriantharia tubes may serve as a preferential
food source for some infauna. O'Connor et al. (1977)
noted sipunculids, Golfingia elongata (Keferstein),
inquiline with Pachycerianthus multiplicatus had
tube remains in their guts. Scavengers, such as Mar-
physa sanguinea may benefit from the inquilinism
for this reason.
Ceriantharia may also negatively affect the in-
fauna in sediments adjacent to the tubes; large
motile species, attracted to the tubes for shelter,
might selectively graze near tubes. We hope to in-
vestigate Ceriantharia "forest" communities more
thoroughly on future submersible cruises: Substrate
collections taken away from tubes will further define
their functional role. We believe Ceriantharia influ-
ence the ecology of the northwest Atlantic contin-
ental shelf and slope more than has been revealed
from data collected by conventional surface tech-
640
SHEPARD ET AL.: ECOLOGY OF CERIANTHARIA
niques alone; methods inadequate for collecting
deep-burrowing adults, and providing information
on behavioral and spatial relationships between
Ceriantharia and other community residents.
ACKNOWLEDGMENTS
Funding for submersible time was provided by
NOAA's Office of Undersea Research, Washington,
D.C. Ann Frame, NMFS Sandy Hook Laboratory,
NJ, identified invertebrate specimens. We thank
Kenneth Sebens and J. C. den Hartog for critically
reviewing the manuscript. Alan Hulbert and Michael
Pennington provided advice on data analysis. Han-
nah Goodale, Jean Klemm, and Connie Fontaine
typed the various drafts of the manuscript. Special
thanks to the submersible and ship crews who made
the data collection possible: R/V Johnson (JSL), R/V
Atlantic Twin (Nekton), and R/V Lulu (Alvin).
We dedicate this effort to the memory of John
Lamont, whose talents, patience, and humor made
our daily burdens easier to bear.
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643
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646
CARTILAGE AND BONE DEVELOPMENT IN SCOMBROID FISHES
Thomas Potthoff, Sharon Kelley, and Joaquin C. Javech1
ABSTRACT
Early development of cartilage and bone was examined in representative species of the scombroid fish
families Scombrolabracidae, Gempylidae, Trichiuridae, Scombridae, Istiophoridae, and Xiphiidae from
cleared and stained larval size series. Development of the dorsal and anal fins and their pterygiophore
supports, development of the neural and haemal spines and hypural complex, and ossification of the
vertebrae were studied. The first appearance and location of these skeletal elements in cartilage were
noted, and then the direction of new additions was observed. Direction of ossification of these elements
was also noted. There were three major kinds of verebral column development: The first was shared
by Scombrolabracidae, Scombridae in part - Scombrini, Scomberomorini, and Thunnini; the second was
shared by Gempylidae, Sarda (Scombridae in part - Sardini), Istiophoridae, and Xiphiidae; the third kind
was found in Trichiurus (Trichiuridae). Saddle-shaped ossifications of the vertebrae were found only
in the Scombrolabracidae, and Gempylidae, and Scombridae. Four major kinds of fin and pterygiophore
development were observed in the scombroid families: Scombrolabracidae and Scombridae in part - Scom-
brini shared one kind; Gempylidae, Trichiuridae, and Scombridae in part - Scomberomorini, Sardini, and
Thunnini shared another kind, which had some variations for different taxa; Istiophoridae had the third
kind; and Xiphiidae had the fourth kind. Initial ossification of the vertebral column started in one place
mScombrolabrax, Gempylidae, Trichiurus, and Xiphias, in two places in Scomber omorus, Sarda, Thun-
nus, and Istiophorus, and in four places in Scomber and Acanthocybium. From our investigation, we
are just beginning to learn about developmental characters and we cannot interpret their full meaning
until more developmental work has been accomplished; we can only state that billfish (Istiophoridae,
Xiphiidae) are very different from all other scombroids studied and that Scombrolabrax shows affinity
with the scombroids.
In this paper we describe development of selected
osteological features of families in the suborder
Scombroidei. We believe that this ontogenetic data
will be useful in future taxonomic studies to aid in
establishing familial relationships. Under current
classification the scombroids comprise various num-
bers of families. Greenwood et al. (1966) recognized
six families in the suborder Scombroidei: Scom-
bridae, Gempylidae, Trichiuridae, Istiophoridae,
Xiphiidae, and Luvaridae. Gosline (1968), Potthoff
et al. (1980), and Collette et al. (1984) included the
family Scombrolabracidae in the Scombroidei, but
Johnson (in press) removed it recently. Collette et
al. (1984), Leis and Richards (1984), and Tyler et
al.2 removed the Luvaridae from the Scombroidei.
For this study we examined ontogenetic series of
representative genera of the families Scombrola-
bracidae, Gempylidae, Trichiuridae, Scombridae
(four tribes), Istiophoridae, and Xiphiidae.
Southeast Fisheries Center Miami Laboratory, National Marine
Fisheries Service, NOAA, 75 Virginia Beach Drive, Miami, FL
33149.
2Tyler, J. C, G. D. Johnson, I. Nakamura, and B. B. Collette.
Osteology and relationships of the oceanic fish Luvarus imperialis
(Luvaridae): an acanthuroid not a scombroid. Unpubl. manuscr.
National Museum of Natural History, Wash., DC 20560.
Research on the larvae and young stages of scom-
broids, particularly tunas (Richards and Klawe 1972)
has been extensive. In general, most papers deal
with the external description of the larvae and
juveniles (Okiyama and Ueyanagi 1978); few exist
that address the internal morphology and develop-
ment of scombroids and those are mostly on scom-
brids. Kramer (1960) described bone development
in the mackerel (Pneumatophorus diego = Scomber
japonicus). Potthoff and Richards (1970), Matsu-
moto et al. (1972), and Richards and Potthoff (1974)
published osteological characters for juvenile scom-
brids. Cartilage and bone development were de-
scribed in Thunnus atlanticus (Potthoff 1975), Scom-
brolabrax heterolepis (Potthoff et al. 1980), and
Xiphias gladius (Potthoff and Kelley 1982). Kohno
et al. (1984) described fin and cartilaginous fin sup-
port development in Scomber japonicus. To our
knowledge no developmental studies of cartilage and
bone have been made for the scombroid families
Istiophoridae and Gempylidae, although a part of
the research presented here was published in Col-
lette et al. (1984). Since Collette et al. (1984), we
have conducted additional research and have dis-
covered several errors in our published observations.
We have added developmental series of Scomber
Manuscript accepted February 1986.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
647
FISHERY BULLETIN: VOL. 84, NO. 3
spp., Scomberomorus spp., Acanthocybium solanderi
and Sarda sarda (Scombridae), Trichiurus lepturus
(Trichiuridae), and Makaira nigricans (Istiophor-
idae). We examined numerous juvenile and adult
Trichiuridae; our findings are incorporated here. In
table 161 of Collette et al. (1984), observations from
the gempylid Diplospinus multistriatus were er-
roneously listed under Trichiuridae. In this paper
we have revised and corrected that table and incor-
porated all our new findings (Tables 1, 2).
Table 1 .—Developmental and osteological features and counts
Gempylidae
Trichiruidae
Scombridae
Scombrolabracidae
(Scombrolabrax)
without
tail and
pelvic fin,
Trichiurus
with tail and
pelvic fin,
Benthodesmus
Evoxymetapon
Lepidopus
Scombrini
(Scomber)
Predorsal bones:
present or absent
absent
present or
or absent2
number
0
0 or 1
First anteriormost dorsal
pterygiophore:
supports number of
2
2
fin spines
inserts in interneural
space number
3
2
First anteriormost anal
pterygiophore:
supports number of
3
32or 3
spines or rays
Middle radials:
present or absent
present
present5
Dorsal and anal stay:
present or absent
present
present
ossifies to one or two
one part
one or
parts
two parts6
posteriorly bifurcated
nonbifurcated
bifurcated
or nonbifurcated
Pelvic fin:
spine, ray count
l,5
l,5;l,4;l,2;
M;l
Preural centrum 3:
neural spine with or
without cartilage tip
with
with
haemal spine autogenous
autogenous
autogenous
or nonautogenous
Vertebrae inclusive of
urostyle supporting
caudal rays:
number
3
3
Number of vertebrae:
precaudal + caudal =
13 + 17 = 30
usually more
total
precaudal,
fewer caudal
total 31-67
Epurals:
number
3
73
Anterior epural fused with
neural arch of Pu2
No
No
absent
present
not determined
40 + 126 = 166
absent
0
43
present
present
one part
nonbifurcated
l,1;l,2
with
ontogenetically
fused
fewer
precaudal,
more caudal,
total 99-192
1 (ontogenetic
fusion from 2)
No
absent
0
present
present
one part
bifurcated
l,5
with
autogenous
13,14 +
17,18 =
31
No
1Data from Fritzsche and Johnson (1980) and G. D. Johnson (text footnote).
2Ruvettus, Thyrsitops and Tongaichthys have one predorsal bone.
3Rexea and Thyrsites (Leionura) have two spines, Nealotus ontogenetically has three spines but second spine fuses to basipterygium during devel-
opment.
4Two of these spines are extreme vestiges.
648
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
METHODS
Scombroid larvae were cleared and stained for
cartilage and bone (Potthoff 1984) and subsequent-
ly measured in millimeters with a calibrated ocular
micrometer under a binocular microscope. Noto-
chord length (NL) was measured on preflexion and
flexion stage larvae from the anterior tip of the up-
per jaw to the posterior tip of the notochord. Stan-
dard length (SL) was measured from the anterior
for the scombroid families and Morone, a primitive perciform fish.
Scombridae—
■Continued
Scomberomorini
(Scomberomorus)
Scomberomorini
(Acanthocybium)
Sardini
(Sarda)
Thunnini
(Thunnus)
Istiophoridae
(Istiophorus)
Xiphiidae
(Xiphias)
Percichthyidae
(Moroney
absent
0
absent
0
absent
0
absent
0
absent
0
absent
0
present
3
2
2
2
2
3
1 to 3,
mostly 2
3
3
3
2
3
1
2
3
3
not known
3
3
2
1 to 3,
3
mostly 2
present
present
present
present
present
absent
present
present
one part
nonbifurcated
present
one part
slightly
bifurcated
present
one part
bifurcated
present
one part
bifurcated
present
one part
bifurcated,
sometimes
non-
bifurcated
present
one part
non-
bifurcated
present
one part
nonbifurcated
l,5
l,5
l,5
l,5
l,2
l,5
with
with
with
with
with
without
with
autogenous
autogenous
autogenous
autogenous
autogenous
non-
autogenous
autogenous
4,5
(16-22) +
(24-32) =
(41-53)
(30-32) +
(31-33) =
(62-64)
26
+
25 =
51
fewer
precaudal,
more caudal,
total 39-41
12
11
+
+
12 = 24
13 = 24
15 + 11 =26
16 + 10 = 26
12 + 13 = 25
11 + 14 = 25
2
2
2
2
3
3
3
No
No
No
Yes
No
No
No
5Neoepinnula lacks middle radials.
6Lepidocybium, Rexea, Diplospinus, Paradiplospinus, Tongaichthys, and Gempylus have a one-part stay, all other gempylids have a two-part stay.
7Diplospinus ontogenetically usually has three epurals, posterior two epurals are fused to one in adults, but some Diplospinus develop only two
epurals.
649
FISHERY BULLETIN: VOL. 84, NO. 3
Table 1 .—Continued.
Scombrolabracidae
(Scombrolabrax) Gempylidae
Trichiuridae
Scombridae
with tail and
without
pelvic fin,
tail and
Benthodesmus
pelvic fin,
Evoxymetapon
Scombrini
Trichiurus
Lepidopus
(Scomber)
Uroneural:
number
2
2
Hypural 5:
present or absent
present
present
fused or separate
separate
separate
Ontogenetic hypural fusion:
fusion of hypurals 1 & 2
to ventral plate is in
cartilaginous or
no fusion
if present,
ossified state
ossified
fusion of hypurals 3 & 4
to dorsal plate is in
cartilaginous or
no fusion
If present,
ossified state
ossified
Procurrent spur (Johnson
1975):
present or absent
present
present,
reduced or
absent
Stay on 4th pharyngo-
branchial (G. D. Johnson,
text footnote):
present or absent
absent
absent
absent
present
not known
fused to
uroneural
proximally
not known cartilaginous
not known
absent
cartilaginous
or ossified
absent
absent
absent
present
Table 2.— Developmental features for the scombroid
Neural and haemal arches and
spines, parapophyses and
hypural parts initially develop
in the following places on the
notochord by the following se-
quence. Addition is in a given
direction.
Developing pterygiophores
and fin spines and rays are
added in a direction.
Scombrolabracidae
(Scombrolabrax)
Gempylidae
(Gempylus,
Nesiarchus,
Diplospinus)
1.
2.
3.
Anterodorsad, posteriorly.
Posteroventrad, posteriorly
and anteriorly.
Ventrad at center, posteri-
orly and anteriorly.
Dorsad at center, posterior-
ly and anteriorly.
Anterodorsad, posteriorly.
Posteroventrad, posteriorly
and anteriorly.
Ventrad at center, posteri-
orly and anteriorly.
First dorsal: anteriorly and
posteriorly. Second dorsal: an-
teriorly and posteriorly. Anal:
anteriorly and posteriorly.
First dorsal: posteriorly. Sec-
ond dorsal: anteriorly and
posteriorly. Anal: anteriorly
and posteriorly.
Trichiuridae
(Trichiurus)
1. Anterodorsad, posteriorly.
2. Ventrad at center, posteri-
orly and anteriorly.
Entire dorsal and anal: poste-
riorly.
650
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
Scombridae — Continued
Scomberomorini Scomberomorini Sardini Thunnini Istiophoridae Xiphiidae Percichthyidae
(Scomberomorus) (Acanthocybium) (Sarda) (Thunnus) (Istiophorus) (Xiphias) (Moroney
1 111112
present
present
present
present
absent
separate
fused to
uroneural
proximally
separate
separate
cartilaginous
cartilaginous
cartilaginous
cartilaginous
cartilaginous
or ossified
cartilaginous
cartilaginous
cartilaginous
cartilaginous
cartilaginous
or ossified
or ossified
or ossified
present
separate
present
separate
ossified
ossifed
no fusion
no fusion
absent
absent
absent
absent
absent
absent
present
present
present
present
present
present
present
absent
families and Morone, a primitive perciform fish.
Sequence of fin and associ-
ated pterygiophore develop-
ment.
First anteriormost dorsal and
anal pterygiophore develop
from one or two pieces of carti-
lage.
Number of initial places of
ossification along vertebral
column; centra develop from
saddle-shaped ossifications at
bases of neural and haemal
arches.
1. Second dorsal and anal
concurrently.
2. First dorsal. First dorsal
separated from second
dorsal during part of devel-
opment.
Dorsal from one piece, anal
from two pieces.
1;Yes
1 . First dorsal.
2. Second dorsal and anal
concurrently. First dorsal
separated from second
dorsal during part of devel-
opment.
1 . All dorsal rays and pteryg-
iophores dorsoanterior to
anal fin.
2. All dorsal rays and pteryg-
iophores opposite future
anterior portion of anal fin.
3. All anal rays and pterygio-
phores.
Dorsal from one piece, anal
from two pieces.
Dorsal and anal from one
piece.
1;Yes
1;No
651
FISHERY BULLETIN: VOL. 84, NO. 3
Table 2.— Continued.
Neural and haemal arches and
spines, parapophyses and
hypural parts initially develop
in the following places on the
notochord by the following se-
quence. Addition is in a given
direction.
Developing pterygiophores
and fin spines and rays are
added in a direction.
Scombridae,
Scombrini
(Scomber)
Scombridae,
Scomberomorini
(Scomberomorus)
Scombridae,
Scomberomorini
(Acanthocybium)
1
Posteroventrad, posteriorly
and anteriorly.
Ventrad at center, posteri-
orly and anteriorly.
Dorsad at center, posterior-
ly and anteriorly.
Anterodorsad, posteriorly.
Anterodorsad, posteriorly.
Posteroventrad, posteriorly
and anteriorly.
Ventrad at center, posteri-
orly and anteriorly.
Dorsad at center, posterior-
ly and anteriorly.
Not entirely known. Smallest
specimen available had al-
ready two centers of initial
development: anterodorsad
and posteroventrad.
First dorsal: pterygiophores
anteriorly and posteriorly.
Spines: one anteriorly, rest
posteriorly. Second dorsal: an-
teriorly and posteriorly. Anal:
anteriorly and posteriorly.
First dorsal: posteriorly. Sec-
ond dorsal: anteriorly and pos-
teriorly. Anal: anteriorly and
posteriorly.
First dorsal: probably posteri-
orly. Second dorsal: anteriorly
and posteriorly. Anal: anterior-
ly and posteriorly.
Scombridae,
Sardini
(Sarda)
Scombridae,
Thunnini
(Thunnus)
Istiophoridae
(Istiophorus)
Xiphiidae
(Xiphias)
1. Anterodorsad, posteriorly.
2. Posteroventrad, posteriorly
and anteriorly.
3. Ventrad at center, posteri-
orly and anteriorly.
1. Anterodorsad, posteriorly.
2. Posteroventrad, posteriorly
and anteriorly.
3. Ventrad at center, posteri-
orly and anteriorly.
4. Dorsad at center, posterior-
ly and anteriorly.
1. Anterodorsad, posteriorly.
2. Posteroventrad, posteriorly
and anteriorly.
3. Ventrad at center, haemal
spines posteriorly, para-
pophyses anteriorly.
1 . Anterodorsad, posteriorly.
2. Posteroventrad, posteriorly
and anteriorly.
3. Ventrad at center, posteri-
orly and anteriorly.
First dorsal: pterygiophores
posteriorly. Spines: first one
anteriorly, rest posteriorly.
Second dorsal: probably ante-
riorly and posteriorly. Anal:
anteriorly and posteriorly.
First dorsal: pterygiophores
posteriorly. Spines: first one
anteriorly, rest posteriorly.
Second dorsal: anteriorly and
posteriorly. Anal: some ante-
riorly, most posteriorly.
Entire dorsal: very few anteri-
orly, most posteriorly. Anal:
very few anteriorly, most pos-
teriorly.
Entire dorsal: anteriorly and
posteriorly. Anal: very few an-
teriorly, most posteriorly.
Percichthyidae
(Moroney
Anterodorsad, posteriorly.
Ventrad at center, posteriorly
and anteriorly. Posteroven-
trad, posteriorly and anterior-
ly. Initial sequence not known,
not known if neural arches and
spines develop initially at
center.
First dorsal: anteriorly and
posteriorly. Second dorsal: an-
teriorly and posteriorly. Anal:
anteriorly and posteriorly.
'Data from Fritzsche and Johnson (1980) and G. D. Johnson (text footnote 3).
652
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
Sequence of fin and associ-
ated pterygiophore develop-
ment.
First anteriormost dorsal and
anal pterygiophore develop
from one or two pieces of carti-
lage.
Number of initial places of
ossification along vertebral
column; centra develop from
saddle-shaped ossifications at
bases of neural and haemal
arches.
1. Second dorsal and anal Dorsal
concurrently. piece.
2. First dorsal.
and anal from one 4;Yes
1. First dorsal.
2. Second dorsal and anal
concurrently. First dorsal
separated from second
dorsal during part of devel-
opment.
Dorsal from one piece, anal
from two pieces.
2;Yes
First dorsal.
Second dorsal and anal
concurrently. First dorsal
separated from second
dorsal during part of devel-
opment.
First dorsal.
Second dorsal and anal
concurrently. Not known if
first dorsal is separated
from second dorsal during
part of development.
First dorsal.
Second dorsal and anal al-
most concurrently. First
dorsal separated from sec-
ond dorsal during part of
development.
Dorsal probably from one 4;Not known
piece, anal not known.
Dorsal from one piece, anal 2?;Yes
probably from two pieces.
Dorsal from one piece, anal 2;Yes
from two pieces.
1. First dorsal.
2. Second dorsal and anal
concurrently. First dorsal
not separated from second
dorsal during development.
Dorsal from one piece, anal
from two pieces.
2;No
1.
Second dorsal and anal
concurrently.
First dorsal. First dorsal
and first anal nor separated
from second dorsal and
second anal during devel-
opment.
Second dorsal and anal
concurrently.
First dorsal. Separation or
continuity of first and sec-
ond dorsals not known.
Variable, dorsal and anal may 1;No
develop from one or two
pieces.
Dorsal and anal from two ? ; N o
pieces.
653
FISHERY BULLETIN: VOL. 84, NO. 3
tip of the upper jaw to the posterior margin of the
hypural bones. Xiphias larvae were measured from
the anterior margin of the eye to the posterior tip
of the notochord for eye notochord length (ENL) or
from the anterior margin of the eye to the posterior
margin of the hypural bones for eye standard length
(ESL).
FAMILY SCOMBROLABRACIDAE
Figure 1
Thirty Scombrolabrax heterolepis larvae (2.9-10.4
mm NL or SL) were available.
Development of the vertebral column initially
started in four places on the notochord: 1) antero-
dorsad (neural arches and spines of future centra
1-3), 2) posteroventrad (parhypural, hypurals), 3)
ventrad at the center (haemal arches and spines on
future centra 16-21), and 4) dorsad at the center
(neural arches and spines on future centra 12-28).
The anterior neural spines were added in a posterior
direction whereas the neural and haemal spines at
the center of the body were added anteriorly and
posteriorly. The two areas of neural spine develop-
ment coalesced around the eighth neural spine
anteriorly and just anterior to the hypural complex
posteriorly. The hypurals were added in a posterior
direction, but the parhypural and the two autoge-
nous haemal spines were added anteriorly (Table 2).
Ossification of the vertebral column in Scombrola-
brax initially started in one place with the ante-
riormost neural arches and spines and proceeded in
a posterior direction. The hypural complex was the
last along the vertebral column to start ossifying.
Vertebrae first ossified by forming saddles of bone
dorsad and ventrad around the notochord. As ossi-
fication proceeded the saddles merged laterally
forming an hourglass-shaped vertebra in the lateral
view.
Cartilaginous second dorsal and anal fin pterygio-
phores developed first simultaneously above inter-
neural spaces 15-17 and below interhaemal spaces
16-19 before the anterior neural arches and spines
had coalesced. The addition of cartilaginous second
dorsal and anal fin pterygiophores was in an ante-
rior and posterior direction. First dorsal fin pteryg-
iophores appeared second above interneural spaces
4-7, to which pterygiophores were added anterior-
ly and posteriorly, terminating anteriorly in the
third interneural space and joining with the second
dorsal fin pterygiophores posteriorly. Dorsal and
anal fin rays and spines developed in the same se-
quence as their corresponding pterygiophores, but
a little later (Table 2).
Scombrolabrax heterolepis does not develop pre-
dorsal bones. The first dorsal pterygiophore orig-
inated from one piece of cartilage and inserted in
the third interneural space supporting two fin spines
(one supernumerary spine). The first anal pterygio-
phore developed from two pieces of cartilage and
supported three spines (two supernumerary spines).
The posteriormost five or six dorsal and anal pte-
rygiophores had middle radials. The last dorsal and
anal pterygiophore supported a double ray and had
a nonbifurcated stay (Table 1).
In S. heterolepis, first caudal development of the
cartilaginous parhypural and hypurals 1 and 2 was
concurrent with the anterior development of the
neural spines and the central appearance of haemal
spines. The hypural complex development was
described by Potthoff et al. (1980). Scombrolabrax
heterolepis had the basic perciform caudal skeleton
(Gosline 1968), with no hypural fusion observed in
adults. The neural and haemal elements of preural
centra 2 and 3 supported the procurrent caudal rays.
A procurrent spur was present on the posteriormost
ventral secondary caudal ray with a basally fore-
shortened ray anterior to it (Johnson 1975) (Table 1).
FAMILY GEMPYLIDAE
Figures 2-4
One hundred and ten gempylids in 11 genera were
available: 33 Gempylus serpens (3.7-9.9, 160 mm NL
or SL), 2SNesiarchus nasutus, (2.6-10.2, 55, 242 mm
NL or SL), 7 Neoepinnula orientalis (3.3-7.1, 112
mm NL or SL), 11 Nealotus tripes (3.4-11.9, 24-140
mm NL or SL), 5 Lepidocybium flavobrunneum
(5.5-35.3 mm NL or SL), 5 Promethichthys prome-
theus (26.4-161 mm SL), 2 Rexea sp. (132, 155 mm
SL), 2 Ruvettus pretiosus (209, 212 mm SL), 1
Thyrsitops lepidopoides (160 mm SL), 16
Diplospinus multistriatus (3.4-13.5 mm NL or SL),
5 Thyrsites atun (= Leionura, 83-254 mm SL). Of
these, G. serpens, D. multistriatus, and TV. nasutus
yielded complete developmental series.
Development of the vertebral column initially
started in three places on the notochord: 1) antero-
dorsad (neural arches and spines on future centra
1-6); 2) posteroventrad (hypurals); and 3) ventrad
at the center (anterior haemal arches and posterior
parapophyses). The neural arches and spines were
Figure 1.— Schematic representation of vertebral column, dorsa
and anal fin, pterygiophore, and hypural development in Scorn
brolabrax heterolepis, Scombrolabracidae. Cartilage, white; ossi
fying, stippled. Scale represents interneural and interhaemal spac<
number and vertebra number.
654
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
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655
FISHERY BULLETIN: VOL. 84, NO. 3
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Figure 2.— Schematic representation of vertebral column, dorsal and anal fin, pterygiophore, and hypural development in Gempylus
serpens, Gempylidae. Cartilage, white; ossifying, stippled. Scale represents interneural and interhaemal space number and vertebra
number.
added in a posterior direction. Haemal arches and
spines developed only when the neural spines
reached the caudal area, and they were added in a
posterior direction. Parapophyses were added ante-
riorly. The hypurals were added posteriorly, the par-
hypural and the autogenous haemal spines were
added anteriorly (Table 2). Ossification of the verte-
bral column in the gempylid genera examined by us
initially started in one place and was similar to the
ossification in Scombrolabrax, except in Diplospinus
the vertebral column was ossified to preural centrum
6 when the urostyle and the hypurals initially started
to ossify. Saddle-shaped vertebral ossifications were
observed in all gempylids examined, similar to those
described for Scombrolabrax.
Gempylids developed first dorsal fin pterygio-
phores and fin spines first, after only a few carti-
laginous neural spines had developed. Development
of first dorsal fin pterygiophores and spines was in
a posterior direction. During early development the
neural spines were anterior to the first dordal fin
pterygiophores and fin spines, but later they
developed faster and were posterior to the pterygio-
phores. Pterygiophores of the second dorsal and anal
fins developed before the developing first dorsal fin
pterygiophores and had joined with the second dor-
656
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
2 4 6 8 10 12 14 16 18
-i — i — i — r
20
~~l —
22
— I-
24
26
28
30
32
34
36
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r
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i — r
~T
T
T"
T
T
3 6 mm NL
^Mmm^
4 0 mm NL
<?
2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34
Figure 3.— Schematic representation of vertebral column, dorsal and anal fin, pterygiophore, and hypural development in Nesiar-
chus yiasutus, Gempylidae. Cartilage, white; ossifying, stippled. Scale represents interneural and interhaemal space number and vertebra
number.
sal fin pterygiophores. Addition of second dorsal and
anal pterygiophores was then in an anterior and
posterior direction. The same development was
observed for the second dorsal and anal fin rays and
anal spines at slightly greater size (Table 2).
Most gempylid genera lack predorsal bones, ex-
cept Tongaichthys (Nakamura and Fujii 1983),
Ruvettus (Potthoff s pers. obs.), and Thyrsitops
(Sato 1983) which have one predorsal bone. The first
dorsal pterygiophore originated from one piece of
cartilage and inserted in the second interneural
space supporting two fin spines (one supernumerary
spine). In three Atlantic Lepidocybium, the first dor-
sal pterygiophore inserted in the second interneural
space, but in two Pacific specimens it was found in
the third space. The first anal pterygiophore was
considerably larger than the following pterygio-
phores and presumably developed from two pieces
of cartilage. It supported three anal spines (two
supernumerary spines) except in adults of Rexea,
657
FISHERY BULLETIN: VOL. 84, NO. 3
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POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
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Thyrsites (Leionura), and Nealotus where only two
spines were supported (one supernumerary). Lar-
vae of Nealotus have three spines associated with
the first anal pterygiophore, but in juveniles the sec-
ond anal spine was fusing to the posterior process
of the pterygiophore. No evidence of a similar fu-
sion was observed in Rexea or Thyrsites (Leionura).
Gempylids had middle radials in one to six posterior-
most dorsal and anal pterygiophores (except Neo-
epinnula lacked middle radials). A double ray, and
a two-part posteriorly bifurcated stay was associated
with the last dorsal and anal pterygiophore in ap-
proximately one half of the genera. Lepidocybium,
Gempylus, Diplospinus, Paradiplospinus, Tongaich-
thys, and Rexea had a one-part posteriorly bifurcated
stay (Table 1).
First caudal development of the cartilaginous
parhypural and hypurals 1 and 2 was concurrent
with anterior development of a few neural spines
and some first dorsal fin pterygiophores and fin
spines. The gempylid genera studied by us developed
all parts found in basic perciform caudal skeletons
(Gosline 1968), even the smaller second uroneural.
Caudal parts then fuse differently in the various
genera of adults (Matsubara and Iwai 1958). The
neural and haemal elements of preural centra 2 and
3 supported the procurrent caudal rays. In the gem-
pylids the procurrent spur on the posteriormost ven-
tral secondary caudal ray may be present, reduced,
or absent. Johnson (1975) examined two species in
which it was absent (Table 1).
FAMILY TRICHIURIDAE
Figures 5-8
Seventy-three trichiurids in four genera were
available: 61 Trichiurus (4.5-26, 300, 303, 510 mm
TL), 8 Benthodesmus (4.5, 12 mm NL, 65-120, 541,
545 mm SL), 3 Evoxymetapon (210-550 mm SL), 1
Lepidopus (280 mm SL). Only Trichiurus yielded
a complete developmental series.
Development of the vertebral column in Trichi-
urus initially started in two places on the noto-
chord: 1) anterodorsad (neural arch and spine on
future centrum 1), and 2) ventrad at the center (an-
terior haemal arches and posterior parapophyses).
Cartilaginous neural arches and spines were added
in a posterior direction. Haemal arches and spines
developed when the neural spines reached the ante-
rior future caudal vertebrae. Addition of haemal
arches and spines was also in a posterior direction
(Table 2). Trichiurus lacked a caudal complex. Ossi-
fication of the vertebral column started initially in
one place, with the anteriormost neural spines and
659
FISHERY BULLETIN: VOL. 84, NO. 3
2 4 6 8 10 12 14 36 38 40 42 44
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108 110 112 114 116 118 164 166
i i i i 1 1 1 1 1 1 1 i 1 1
?
YTffimr""
4 5 mm SL
5 0 mm SL
Z\
6 0 mm SL
, — — - — -—
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'ffwmr^
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nfTTTTTTTTTTTT'
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6 8 10 12 14
16 0 mm SL
_i i i i i i i i i i i i i i i i i i i i i i i p
36 38 40 42 44 108 110 112 114 116 118 164 166
Figure 5.— Schematic representation of vertebral column, dorsal and anal fin, pterygiophore, and hypural development in Trichiurus
lepturus, Trichiuridae. Cartilage, white; ossifying, stippled. Scale represents interneural and interhaemal space number and vertebra
number.
660
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
Figure 6.— Left lateral view of the anteriormost three dorsal pterygiophores inserting in the interneural
spaces 2-4 from a juvenile Trichiurus lepturus 510 mm TL. D, distal radial; Ns, neural spine; P, proximal
radial; R, ray or spine; X, a new pterygiophore element of unknown homology. Cartilage, white; bone,
stippled.
arches and proceeded in a posterior direction.
Saddle-shaped ossifications of the vertebrae as seen
in Scombrolabrocidae, Gempylidae, and Scombridae
were not observed in Trichiurus, instead vertebral
ossification started laterally on both sides of the
notochord as a thin strip of bone. During further
development the lateral strip elongated dorsad
and ventrad joining the strip from the opposite
side and forming a ring of bone around the noto-
chord.
Trichiurus first developed two of the three ante-
rior dorsal fin spines. Next the first dorsal pteryg-
iophore developed. Then dorsal pterygiophores, the
third dorsal fin spine, and the dorsal fin rays were
added in a posterior direction, with the pterygio-
phore development being slightly posterior to the
ray development and considerably posterior to the
neural arch and spine development. The single large
anal spine developed first after dorsal fin ray and
pterygiophore development had dorsally passed the
anterior portion of the anal fin fold. Next, the large
first anal fin pterygiophore and some haemal arches
and spines developed. Further development con-
sisted of the addition of anal fin rays, pterygio-
phores, and haemal arches and spines in a posterior
direction. The haemal arches and spines and the anal
fin rays developed slightly anterior to the anal pte-
rygiophores. The anal pterygiophores were slightly
anterior to the dorsal fin ray and pterygiophore
development (Table 2).
Trichiurus lacked predorsal bones. The first dor-
sal pterygiophore supported two fin spines (one
supernumerary) and originated from one piece of
cartilage. In larvae the first dorsal pterygiophore
inserted between the split neural arch and spine of
the first centrum, thus inserting into the first and
second interneural spaces. However, in adults the
first dorsal pterygiophore inserted into the second
interneural space. All following interneural and
interhaemal spaces accommodated one pterygio-
phore per space. The first anal pterygiophore was
larger than the following pterygiophores, but it
developed from one piece of cartilage and sup-
ported one supernumerary spine and one ray (Table
1).
The pterygiophores in Trichiurus and probably
in most if not all species of the Trichiuridae are
anatomically different from those of other scom-
661
FISHERY BULLETIN: VOL. 84, NO. 3
Figure 7.— Two dorsal fin pterygiophores from Trichiurus lepturus 510 mm TL, taken directly from
opposite the anterior portion of the anal fin. A, left lateral view of the pterygiophores and rays; the
left side of the posterior ray has been removed. Cartilage, white; ossifying, stippled. B, dorsal view
of one of the two pterygiophores; unfused parts have been disarticulated. C, dorsal view of
pterygiophore in B, unfused parts have been left articulated. For abbreviations see Figure 6.
broids (G. D. Johnson3). The anteriormost two dor-
sal pterygiophores supported three spines, which
were the only dorsal fin spines and which had ser-
rations in larvae and juveniles, but were smooth in
adults. The anterior two pterygiophores had two
parts each and supported fin spines. The 3d-127th
pterygiophores had three parts and supported fin
3G. David Johnson, Curator (Fishes), Smithsonian Institution,
National Museum of Natural History, Wash., DC 20560, pers. com-
mun. 1985.
rays, the distal parts being located between the
bifurcate bases of the rays. These distal parts were
not homologous with distal radials and are labeled
"X" in Figures 6-8. The 128th-130th pterygiophores
had four parts, and the last three pterygiophores
(131st-133d) had become vestigial having a variable
number of parts, usually from two to four. Anal fin
pterygiophores were anatomically similar to the dor-
sal fin pterygiophores. The first anal fin spine was
large and serrated in larvae and juveniles but
became small and smooth in adults. Trichiurus lar-
662
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
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vae and juveniles developed an anal fin in which the
rays were of the same length as those in the dorsal
fin, but the anal rays became very short and vestigial
in adults. In adult Trichiurus the posterior end of
the dorsal fin was anterior to the posterior end of
the anal fin. Other trichiurids (Benthodesmus, Evox-
ymetapon, Lepidopus) examined by us had pte-
rygiophore arrangements similar to Trichiurus.
FAMILY SCOMBRIDAE
The family is a very speciose group which is
divided into two subfamilies (Collette et al. 1984).
For the monotypic Gasterochismatinae, larvae were
not obtainable, but one or more species for each of
the four tribes of the Scombrinae was studied.
Tribe Scombrini
Figure 9
Twenty-two Scomber japonicus (4.4 mm NL - 9.6
mm SL, 100, 103 mm SL) and 12 S. scombrus (5.7
mm NL - 8.2 mm SL) were used in this study. Many
more Scomber smaller than 5.5 mm NL were avail-
able but showed no cartilage development along the
notochord. In addition, developmental studies on
Scomber by Kramer (1960) and Kohno et al. (1984)
were consulted.
Development of the vertebral column in Scomber
initially started in four places on the notochord: 1)
posteroventrad (parhypural, hypurals 1 and 2), 2)
ventrad at the center (anterior haemal arches and
spines), 3) dorsad at the center (neural arches and
spines above developing haemal arches and spines),
and 4) anterodorsad (neural arches and spines of
future centra 1-3). The anterior neural spines were
added posteriorly, the neural spines at the center
of the notochord were added anteriorly and poste-
riorly, the haemal spines were added posteriorly, but
the parapophyses were added anteriorly. The hypu-
rals were added in a posterior direction, but the two
autogenous haemal spines were added anteriorly.
The dorsal and ventral areas of development co-
alesced completing the cartilaginous ontogeny of the
vertebral column. Ossification of the vertebral
column (neural and haemal spines, vertebrae, and
hypural complex) initially started in four places:
1) dorsoanteriorly (anteriormost neural arches and
spines), 2) ventrad at the center (anterior haemal
arches and spines and posterior parapophyses), 3)
posteriorly (hypural complex), and 4) dorsad at the
center (neural arches and spines). The four initial
areas of ossification coalesced as ossification pro-
gressed. Vertebrae in Scomber initially had saddle-
663
FISHERY BULLETIN: VOL. 84, NO. 3
I 3 5 7 9 II 13 15 17 19 21 23 25 27 29 31
I I I I I I I I I I I 1 I I 1 I I I I I I 1 1 1 1 1 — 1 1 1 — i
59 mm SL
Tirnrmro-
UM^J^W
68 mm SL
VTTtTTTW^-v^
J — l — I — l — I — l — I — I — I I i I I I I i i i i i i i i
3 5 7 9 II 13 15 17 19 21 23 25 27 29
l I I I I
Figure 9.— Schematic representation of vertebral column, dorsal and anal fin, pterygiophore, and hypural develop-
ment in Scomber japonicus, Scombrini, Scombridae. Cartilage, white; ossifying, stippled. Scale represents interneural
and interhaemal space number and vertebra number.
664
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
shaped ossifications similar to those described for
Scombrolabrax (Table 2).
Cartilaginous second dorsal and anal fin pteryg-
iophores developed first simultaneously above inter-
neural spaces and below interhaemal spaces 17-19.
The addition of cartilaginous second dorsal and anal
fin pterygiophores was in an anterior and posterior
direction. Cartilaginous first dorsal fin pterygio-
phores appeared second above interneural spaces
5-8 and were added anteriorly and posteriorly, ter-
minating anteriorly in the third interneural space
and joining with the second dorsal fin pterygio-
phores posteriorly. Second dorsal and anal fin rays
developed in the same sequence as their correspond-
ing pterygiophore, but a little later. The first dor-
sal fin spines developed from anterior in a posterior
direction, but the anteriormost (supernumerary)
spine first developed when seven first dorsal fin
spines were already present (Table 2).
Scomber lacked predorsal bones. The first dorsal
pterygiophore originated from one piece of cartilage
and inserted in the third interneural space support-
ing two fin spines (one supernumerary spine). The
first anal pterygiophore was considerably larger
than all other pterygiophores, but it originated from
only one piece of cartilage supporting two anal
spines (one supernumerary spine). The posterior-
most six dorsal and anal pterygiophores had mid-
dle radials. The last dorsal and anal pterygiophore
supported a double finlet and had a posteriorly bi-
furcated stay (Table 1).
In Scomber, caudal development of the cartilag-
inous parhypural and hypurals 1 and 2 was first
before any other development of cartilaginous
haemal or neural arches and spines along the noto-
chord. The development of the hypural complex
from the first appearance of cartilaginous hypurals
to ossification onset was described by Kohno et al.
(1984) and our findings are in agreement with theirs.
Kramer (1960) described the ossification sequence
in the hypural complex of Scomber. In our speci-
mens, hypurals 1 and 2 were fusing to a ventral
hypural plate before ossification onset. Hypurals 3
and 4 were fusing in some larvae before and in
others after ossification onset. The neural and
haemal elements of preural centra 2 and 3 supported
the procurrent caudal rays. A procurrent spur and
a basally foreshortened ray were absent in Scomber
(Johnson 1975) (Table 1).
Tribe Scomberomorini
Figures 10, 11
Thirty-nine specimens were available: 9 Scomber-
omorus cavalla (4.1-6.2 mm NL), 17 S. maculatus
(6.1 mm NL - 10.2 mm SL, 40.5-67.5 mm SL), 3 S.
regalis (5.3, 6.5 mm NL, 85.0 mm SL), 4 S. tritor
(6.0 mm NL - 8.0 mm SL), 6 Acanthocybium solan-
deri (6.2 mm NL - 10.8 mm SL). None of the above
five species yielded complete developmental series.
However, S. cavalla specimens showed the cartilag-
inous ontogeny of the vertebral column, of the dor-
sal and anal fin pterygiophores and of the hypural
complex. The S. maculatus specimens showed the
latter phases of pterygiophore and hypural complex
development, dorsal and anal fin development, and
the ossification of the vertebral column and the
hypural complex. Specimens of 5. regalis and S.
tritor provided evidence that development for the
Atlantic species of Scomberomorus is very similar.
Specimens of A. solanderi gave incomplete infor-
mation on cartilaginous vertebral column develop-
ment, but adequate information on dorsal and anal
pterygiophore, on dorsal and anal fin, on hypural
complex development, and on the ossification se-
quence of the vertebral column.
Development of the vertebral column in Scomber-
omorus initially started in four places on the noto-
chord: 1) anterodorsad (neural arches and spines on
future centra 1-3), 2) posteroventrad (parhypural,
hypurals 1 and 2), 3) ventrad at the center (four
haemal arches and spines), and 4) dorsad at the
center (six neural arches and spines above initial
haemal spine development). The anterior neural
spines were added posteriad, the neural spines at
the center of the notochord were added anteriorly
and posteriorly, the haemal spines were added most-
ly posteriorly but a few were added in an anterior
direction. All parapophyses were added in an ante-
rior direction. The hypurals were added in a poste-
rior direction, but the two autogenous haemal spines
were added in an anterior direction. The dorsal and
ventral areas of development coalesced and thus car-
tilaginous ontogeny of the vertebral column was
complete. Ossification of the vertebral column ini-
tially started in two places: 1) anteriorly (neural
arches and spines, and centra) and 2) posteriorly
(hypural complex). Ossification of the neural arches
and spines and centra was in a posterior direction.
In the hypural complex ossification started with the
urostyle and proceeded anteriorly to preural cen-
trum 3. Then the ventral hypural plate started to
ossify followed by the dorsal plate, the parhypural,
and the two autogenous haemal spines. Last to start
ossification were the epurals, the uroneural, and the
neural spines. Vertebrae in Scomberomorus had
saddle-shaped ossifications similar to those de-
scribed for Scombrolabrax (Table 2).
665
FISHERY BULLETIN: VOL. 84, NO. 3
2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42
i — i — i — ■ — rn — i — n — i — i — i — i i i i I — n — rn — i — n — I r— n i i i i i n i i i i i i I
ll
Scomberomorus cavalla
11
00 0 0 0
WW \
4.1 mm NL
5 Omm NIL
5.0 mm NL
5.1 mm NL
5.5mm NL
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I 3 5 7 9 II 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51
Figure 10.— Schematic representation of vertebral column, dorsal and anal fin, pterygiophore, and hypural development in
Scomberomorus cavalla and S. maculatus, Scomberomorini, Scombridae. Cartilage, white; ossifying, stippled. Scale represents inter-
neural and interhaemal space number and vertebra number.
666
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
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FISHERY BULLETIN: VOL. 84, NO. 3
Two to five cartilaginous first dorsal fin pteryg-
iophores developed first above interneural spaces
3-5 at the time of ossification onset of the anterior-
most neural arches and spines. The addition of car-
tilaginous first dorsal fin pterygiophores was in a
posterior direction. Five cartilaginous second dor-
sal and anal fin pterygiophores developed second
simultaneously in the anterior portions of the future
second dorsal and anal fins. Some addition of carti-
laginous second dorsal and anal fin pterygiophores
occurred in an anterior direction, but most of the
addition was posteriorly. Dorsal and anal fin rays
and spines developed in the same sequence as their
corresponding pterygiophores, but a little later
(Table 2).
Scomberomorus does not develop predorsal bones.
The first dorsal pterygiophore originated from one
piece of cartilage and inserted in the third inter-
neural space supporting two fin spines (one super-
numerary spine). The first anal pterygiophore
developed from two pieces of cartilage and sup-
ported three spines (two supernumerary spines). The
posteriormost nine dorsal and anal pterygiophores
had middle radials. The last dorsal and anal pteryg-
iophore supported a double finlet and had a non-
bifurcated stay (Table 1).
In Scomberomorus, first caudal development of
the cartilaginous parhypural and hypurals 1 and 2
was concurrent with the anterior development of the
neural spines and the central appearance of haemal
spines. Hypurals 3-5 were added posteriorly, the two
autogenous haemal spines anteriorly. Hypurals 1
and 2 and hypurals 3 and 4 fused before ossifica-
tion onset to a cartilaginous ventral and dorsal
hypural plate. The dorsal and ventral plates fused
after ossification to a single hypural plate with a cen-
tral notch (Collette and Russo 1984). Hypural 5
gradually fused with the paired uroneural forming
an autogenous bone resembling a third epural and
mistaken as such by Leccia (1958). Two epurals
developed anterior to the uroneural-hypural 5. These
epurals remained autogenous. The neural and hae-
mal elements of preural centra 2, 3, 4, and 5 sup-
ported the procurrent caudal rays. A procurrent
spur and basally foreshortened ray were absent in
Scomberomorus (Johnson 1975) (Table 1).
Only six Acanthocybium solanderi were available.
We were therefore unable to ascertain a complete
developmental sequence. Our smallest 6.2 mm NL
specimen had two cartilaginous development centers
along the notochord: some neural spines and arches
anteriorly and the parhypural, hypural 1-3 poste-
riorly. The next larger specimen 9.2 mm SL had all
neural and haemal arches and spines developed, thus
we were unable to tell if in Acanthocybium four ini-
tial centers (as in Scomberomorus) or only three
centers (as in Xiphias and Sarda) of cartilaginous
development along the notochord were present. In
all our Acanthocybium specimens, hypurals 1 and
2 gradually fused before ossification onset to a ven-
tral cartilaginous hypural plate. In the 8.5 mm SL
Acanthocybium, hypurals 3 and 4 were fusing before
ossification onset; in the larger 9.5 and 10.4 mm SL
specimens hypurals 3 and 4 were ossifying while still
separate. The dorsal and ventral hypural plates were
fused in adults to one plate with a notch (Conrad
1938; Collette and Russo 1984) (Table 1). Ossifica-
tion of the vertebral column initially started in four
places and was similar to the ossification in Scomber.
The development of the dorsal and anal fins and
their supporting pterygiophores in Acanthocybium
was similar to that described in Scomberomorus.
Tribe Sardini
Figure 12
Ninety-nine Sarda sarda (2.4-9.0 mm NL or SL,
59-102 mm SL) were available. Of the larval speci-
mens (2.4-9.0 mm NL or SL) only 32 were larger
than 5 mm NL, and of these 10 were between 6.0
and 6.9 mm NL or SL, 6 were between 7.0 and 7.9
mm NL or SL, and 3 were larger than 8 mm SL.
Thus, since development of the vertebral column in
Sarda begins around 5 mm NL, only 32 specimens
were useful to our study and they were too few to
yield a complete developmental series. Our conclu-
sions on Sardini development are not as well sup-
ported as for most other scombroids.
Development of the vertebral column in Sarda ini-
tially started in three places on the notochord: 1)
anterodorsad (neural arch and spine of future cen-
trum 1), 2) posteroventrad (parhypural, hypurals 1
and 2), and 3) ventrad at center (haemal arches and
spines, parapophyses). The anterior neural spines
were added in a posterior direction and the haemal
spines probably first appeared when the correspond-
ing neural spines developed above them at the
center of the notochord. Our evidence, however, is
only indirect, because one 7.5 mm NL specimen had
21 neural spines and no haemal spines, but our 8.1
mm SL specimen had all neural and haemal spines
developed. The cartilaginous hypurals were added
posteriorly, but we could not observe the anterior
addition of the autogenous haemal spines, although
we assume that it happens in Sarda as in other
scombroids with tails. Ossification of the vertebral
column in Sarda initially started in two places: ante-
riorly (neural arches and spines) and posteriorly
668
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50
i I 1 I I I I I I I I I I i I I I — I i I I I I i i I i I I I I ii I I I I I 1
5.3 mm NL
TJS
UnUHHUlHM
6.1 mm NL
I I I l i I l I l I I I l l i I l
W^ 9.0 mm SL
I I I I I I l I l I I i i i I i I i i l l i l I I l
8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48
50
Figure 12.— Schematic representation of vertebral column, dorsal and anal fin, pterygiophore, and hypural development in
Sarda sarda, Sardini, Scombridae. Cartilage, white; ossifying, stippled. Scale represents interneural and interhaemal space
number and vertebra number.
(hypural complex). Our largest 9.0 mm SL specimen
showed ossification to the 11th neural spine. We do
not know if ossification in Sarda proceeds entirely
posteriad or if in Sarda, as in Scomber and Acantho-
cybium, there is some central ossification of neural
and haemal spines before the anterior ossification
has reached the center of the column. The hypural
complex started to ossify early at the time ossifica-
tion on the neural spines began anteriorly. Verte-
brae in Sarda had saddle-shaped ossifications similar
to those described for Scombrolabrax (Table 2).
Cartilaginous first dorsal fin pterygiophores devel-
oped first anteriorly above interneural spaces 2-10
in the 8.1 mm SL specimen. Addition of cartilag-
inous first dorsal fin pterygiophores was in a poste-
rior direction. The 8.4 mm specimen had all first dor-
sal fin pterygiophores and some second dorsal and
anal fin pterygiophores and they were continuous
with each other. Therefore, we are unable to deter-
mine if second dorsal and anal fin pterygiophores
in Sarda developed before first dorsal fin pteryg-
iophores were joined with the second dorsal fin
pterygiophores. Three first dorsal fin spines were
present in the 8.1 mm SL specimen, serially asso-
ciated with the first three pterygiophores. Addition
of first dorsal fin spines was in a posterior direc-
tion, except for the anteriormost first spine (super-
numerary), which developed later in the 9.0 mm SL
Sarda. Second dorsal and anal fin rays were not
developed in our 9.0 mm SL specimen. Our 59 mm
SL specimen had the full adult compliment of fin
rays (Table 2).
669
FISHERY BULLETIN: VOL. 84, NO. 3
Sarda did not develop predorsal bones. The first
dorsal pterygiophore originated from one piece of
cartilage and inserted in the second interneural
space supporting two spines (one supernumerary
spine). We do not know if the first anal pterygio-
phore originated from one or two pieces of cartilage,
but it is most likely that it originated from two pieces
because it supported three fin elements (two super-
numerary spines). The posteriormost seven to nine
dorsal and anal pterygiophores had middle radials.
The last dorsal and anal pterygiophore supported
a double finlet and had a posteriorly bifurcated stay
(Table 1).
In Sarda first caudal development of the carti-
laginous parhypural and hypurals 1 and 2 was con-
current with the beginning development of the ante-
riormost neural arches and spines. Hypurals 1 and
2 fused in the cartilaginous state to form the ven-
tral hypural plate. In three specimens, hypurals 3
and 4 were separate after ossification onset. These
hypurals were fused to the dorsal hypural plate in
juveniles. Hypural 5, the uroneural and two epurals
were separate in our juveniles. Collette and Chao
(1975) found that in adults the dorsal and ventral
plates fused to one hypural plate without a notch
and that the uroneural fused with hypural 5, but the
two epurals remained autogenous. The neural and
haemal elements of preural centra 2, 3, 4, and 5 sup-
ported the procurrent caudal rays. A procurrent
spur and a basally foreshortened ray were absent
in Sarda (Johnson 1975) (Table 1).
Tribe Thunnini
Figure 13
More than 86 specimens were available: 86 Thun-
nus (mostly T. atlanticus and a few Thunnus spp.,
3.7-9.7 mm NL or SL), and a small number of Auxis,
Euthynnus, and Katsuwonus. We were unable to
observe early cartilaginous development in all
genera except Thunnus.
Development of the vertebral column in Thunnus
initially started in four places on the notochord: 1)
anterodorsad (neural arches and spines of future
vertebrae 1-3), 2) posteroventrad (hypurals 1 and
2), 3) ventrad at the center (anteriormost five
haemal arches and spines and posteriormost two
parapophyses), and 4) dorsad at the center (five
neural arches and spines above initial haemal arch
and spine development). The anterior neural arches
and spines were added in a posterior direction, the
central neural arches and spines were added ante-
riorly (coalescing around the future 14th centrum)
and posteriorly toward the epurals. The parapophy-
ses were added in an anterior direction, whereas the
haemal arches and spines were developing in a pos-
terior direction. In the hypural complex hypurals
were added posteriorly, but the parhypural and the
two autogenous haemal spines were added in an
anterior direction, coalescing with the central
haemal arches and spines. Ossification of the verte-
bral column in Thunnini initially started in two
places similar to the ossification described for Scom-
beromorus. Saddle-shaped vertebral ossification
development was observed in all Thunnini examined,
similar to the development described for Scombro-
labra-x (Table 2).
In Thunnini, cartilaginous first dorsal fin pteryg-
iophores developed anteriorly in interneural spaces
3-6 when only few cartilaginous neural spines were
present. Additional pterygiophores were added in
a posterior direction. Later, small cartilaginous sec-
ond dorsal fin pterygiophores appeared in the mid-
dle of the vertebral column above interneural spaces
15-22. As the first dorsal fin pterygiophores devel-
oped in a posterior direction, the second dorsal fin
pterygiophores developed in an anterior and poste-
rior direction until all the dorsal pterygiophores
were continuous. Anal pterygiophores appeared
below interhaemal spaces 20-25 and developed in an
anterior and posterior direction. Addition of the first
dorsal fin spines was in a posterior direction, except
for the anteriormost spine (supernumerary), which
developed when the second and third spine were
already present. The second dorsal and anal fin rays
developed in the same sequence as their correspond-
ing pterygiophores but a little later (Table 2).
All Thunnini species examined lacked predorsal
bones. The first dorsal pterygiophore originated
from one piece of cartilage and inserted in the third
interneural space supporting two fin spines (one
supernumerary spine). The first anal pterygiophore
developed from two pieces of cartilage and sup-
ported three fin spines (two supernumerary spines)
(Potthoff 1975). Middle radials were present on the
posterior eight or nine finlet supporting dorsal and
anal pterygiophores. A one-part posteriorly bifur-
cated stay developed with the posteriormost dorsal
and anal fin pterygiophores (Table 1).
In Thunnus, the caudal complex began to develop
very early concurrently with the first anteriormost
neural spines. Hypurals 1 and 2 and hypurals 3 and
4 developed separate cartilages and fused to a car-
tilaginous dorsal and ventral hypural plate. Potthoff
(1975) stated that hypurals 1 and 2 developed as one
piece of cartilage from the start, but he examined
only specimens larger than 5.0 mm NL not stained
for cartilage. The dorsal and ventral hypural plates
670
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
I 3 5 7 9 II 13 15 17 19 21 23 25 27 29 31 33 35 37 39
i i I i i i i l i i l l i i i i i i l i i l l l — l — l — l — i — i — i — i — i — i — i — i — i — i — i 1
3 7 mm NL
T^
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44mm NL
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I 3 5 7 9 II 13 15 17 19 21 23 25 27 29 31 33 35 37
Figure 13.— Schematic representation of vertebral column, dorsal and anal fin, pterygiophore,
and hypural development in Thunnus atlanticus, Thunnini, Scombridae. Cartilage, white; ossify-
ing, stippled. Scale represents interneural and interhaemal space number and vertebra number.
671
FISHERY BULLETIN: VOL. 84, NO. 3
fused after ossification, but the small hypural 5 re-
mained separate. Preural centra 2 and 3 each had
an autogenous haemal spine. Two epurals and one
uroneural developed dorsad. The anterior epural
fused with the neural arch of Pu2 and the uroneural
fused to the urostyle (Potthoff 1975). The neural and
haemal elements of preural centra 2,3, and 4 sup-
ported the procurrent caudal rays. A procurrent
spur and basally foreshortened ray were absent in
the Thunnini (Johnson 1975) (Table 1).
FAMILY ISTIOPHORIDAE
Figure 14
One hundred and sixteen istiophorids (3.0-227 mm
NL or SL) were available. Most specimens were
caught in the Gulf Stream off Miami, FL. In 67 of
the specimens we were able to count vertebrae; all
had a count of 12 + 12. This identified them as Istio-
phorus platypterus or Tetrapturus spp. (Merrett
1971; Richards 1974). The 67 specimens with the
12 + 12 vertebral count, and the remainder, which
were too small for vertebral counts, probably were
I. platypterus because most adult istiophorids cap-
tured in the Gulf Stream off Miami are that species.
In addition, 12 Makaira nigricans (3.3-5.9 mm NL,
13.3 and 220 mm SL) identified by W. J. Richards4
were examined. The 13.3 and 220 mm SL specimens
had a count of 11 + 13 vertebrae.
Development of the vertebral column initially
started in three places on the notochord: 1) antero-
dorsad (neural arches and spines on future centra
1 and 2), 2) posteroventrad (hypurals), and 3) ven-
trad at the center (anterior haemal arches and pos-
terior parapophyses). The neural arches and spines
were added in a posterior direction. The haemal
arches and spines also were added in a posterior
direction at the time when neural arches and spines
appeared above on the notochord. Parapophyses
were added anteriorly. Hypural bones were added
in a posterior direction, but the parhypural and the
two autogenous haemal spines were added anterior-
ly. Ossification of the vertebral column in istiophor-
ids initially started in two places: ossification of the
anteriormost neural spines and arches proceeded in
a posterior direction. The hypural complex started
ossification before all neural and haemal spines were
ossifying. Saddle-shaped ossifications of the verte-
brae as observed in the Scombrolabracidae, Gem-
pylidae, and Scombridae were not observed in the
4W. J. Richards, Senior Scientist, Southeast Fisheries Center
Miami Laboratory, National Marine Fisheries Service, NOAA, 75
Virginia Beach Drive, Miami, FL 33149, pers. commun. 1983.
Istiophoridae during ontogeny. First ossification of
vertebrae in Istiophoridae was evidenced by the for-
mation of rings of bone around the notochord (Table
2).
Cartilaginous dorsal pterygiophores appeared first
above interneural spaces 3-5. Dorsal pterygiophore
addition was mostly in a posterior direction, except
that those pterygiophores over interneural spaces
2 and 1 were added in an anterior direction. When
dorsal pterygiophore development extended to
above the anterior portion of the anal fin fold, car-
tilaginous anterior anal pterygiophores were seen
below interhaemal spaces 13 and 14, and their addi-
tion was posteriorly abreast of the dorsal pterygio-
phores. At larger sizes dorsal and anal finrays
developed in the same sequence as their supporting
pterygiophores (Table 2).
Istiophorids did not have predorsal bones, instead
the first three interneural spaces were filled with
fin spine supporting pterygiophores. The first dor-
sal pterygiophore originated from one piece of car-
tilage and inserted in the first interneural space sup-
porting three spines (two supernumerary spines).
The anteriormost spine was either small, reduced,
or vestigial. The first anal pterygiophore developed
from two pieces of cartilage supporting two fin
spines (one supernumerary spine). Istiophorids had
one middle radial and one posteriorly bifur-
cated (sometimes nonbifurcated) stay with the
posteriormost dorsal and anal pterygiophore. The
posteriormost dorsal and anal ray were double
(Table 1).
In istiophorids, the caudal complex started to
develop after the precaudal neural spines had devel-
oped. The parhypural and hypurals 1-4 developed
as separate cartilages. In most istiophorid specimens
the cartilages of hypurals 1 and 2 and hypurals 3
and 4 fused to a lower and upper hypural plate
before ossification; in some specimens fusion did not
take place until after ossification onset for the up-
per and lower hypurals. Also, there were specimens
in which none of the cartilaginous hypurals fused.
The 5th hypural did not develop in istiophorids. Dor-
sad 3 epurals and 1 uroneural developed. Preural
centra 2 and 3 each had one autogenous haemal
spine. In adult istiophorids, the fusion of the bones
in the caudal complex was extensive (Gregory and
Conrad 1937); we examined adult specimens of
Istiophorus, Tetrapturus, and Makaira and found
identical hypural fusions in the three genera. The
three epurals remained autogenous, but the uro-
neural, hypurals 1-4, and the parhypural were fused
with each other and with the urostyle to form a
notched hypural plate. The neural and haemal
672
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
2 4 6 8 10 12
14
16
20
22
24
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2 4 6 8 10 12 14 16 18 20 22 24
Figure 14.— Schematic representation of vertebral column, dorsal and anal fin, pterygiophore, and hypural development in
Istiophorus platypterus, Istiophoridae. Cartilage, white; ossifying, stippled. Scale represents interneural and interhaemal space
number and vertebra number.
673
FISHERY BULLETIN: VOL. 84, NO. 3
elements of preural centra 2 and 3 supported pro-
current caudal rays. A procurrent spur and basally
foreshortened ray were absent in the Istiophoridae
(Johnson 1975) (Table 1).
FAMILY XIPHIIDAE
Figure 15
Ninety-five Xiphias gladius specimens (3.7-19.5
ENL or ESL) of this monotypic genus and species
studied by Potthoff and Kelley (1982) were reex-
amined by us.
Development of the vertebral column initially
started in three places on the notochord: 1) antero-
dorsad (neural arches and spines on future centra
1-3), 2) posteroventrad on the notochord (hypurals),
and 3) ventrad at the center (anterior haemal arches
and posterior parapophyses). The neural arches and
spines were added in a posterior direction. When
the developing neural spines had passed the pre-
caudal area, some of the anterior haemal spines
started to develop (except the anteriormost two of
the future caudal vertebrae). Addition of cartilag-
inous neural and haemal spines was in a posterior
direction, except the first two haemal spines which
developed anteriorly. Hypural complex bones were
added in an anterior and posterior direction. Ossi-
fication of the vertebral column in Xiphias initially
started in one place with the anteriormost neural
arches and spines. Ossification then proceeded in a
posterior direction with the hypural complex ossify-
ing last. Saddle-shaped ossifications of the vertebrae
as observed in the Scombrolabracidae, Gempylidae,
and Scombridae was not observed in Xiphias dur-
ing ontogeny. Instead, vertebral ossification was
first noted in Xiphias by the appearance of dorso-
ventral fractures on the notochord followed by the
appearance of ossified vertebrae between the frac-
tures (Table 2).
Cartilaginous dorsal and anal pterygiophores
developed simultaneously before the neural and
haemal spines had reached the area. The dorsal
pterygiophores first developed in a group below the
future middle of the dorsal fin above the future inter-
4
T
10
i r
12
1~
14
"I r
16
20
22
24
26
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4 8mm ENL
0000000
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"VT^ WO
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19 5mm ESL
Figure 15.— Schematic representation of vertebral column, dorsal and anal fin, pterygiophore, and hypural
development in Xiphias gladius, Xiphiidae. Cartilage, white; ossifying, stippled. Scale represents interneural
and interhaemal space number and vertebra number.
674
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
neural spaces 13-16. The anal pterygiophores first
developed in a group above the future anterior part
of the anal fin below interhaemal spaces 16-18. Fur-
ther addition of cartilaginous dorsal and anal pte-
rygiophores was in an anterior and posterior direc-
tion. The posterior pterygiophore additions dorsad
and ventrad were completed before the anterior
additions ceased. The full complement of anal pte-
rygiophores was reached before the full dorsal com-
plement. Dorsal and anal fin rays first originated
in the same areas as the pterygiophores, but at
larger sizes with addition of rays in the same direc-
tions (Table 2).
Xiphias did not have predorsal bones. The first
dorsal pterygiophore originated from one or two
pieces of cartilage and inserted in the second inter-
neural space, supporting from one to three fin
spines. The first anal pterygiophore developed from
one or two pieces of cartilage, supporting from one
to three fin spines. Xiphias had no middle radials
in the dorsal or anal pterygiophores, but a double
ray and a nonbifurcated stay were associated with
the posteriormost dorsal and anal pterygiophores
(Potthoff and Kelley 1982) (Table 1).
In Xiphias, cartilaginous hypurals were first seen
before precaudal neural spine development was com-
plete, but after dorsal and anal pterygiophore devel-
opment had started. The hypural complex develop-
ment was described by Potthoff and Kelley (1982).
Hypurals 1-5 and the parhypural developed from
separate cartilages, and there was no cartilage fu-
sion. There were three epurals and one uroneural.
Only one autogenous haemal spine was present on
preural centrum 2. In adults the three epurals, the
uroneural, hypural 5, and the parhypural remained
autogenous, but hypurals 1-4 fused with each other
and the urostyle forming a notched hypural plate
(Gregory and Conrad 1937). The neural and haemal
elements of only preural centrum 2 supported the
procurrent caudal rays. A procurrent spur and basal-
ly foreshortened ray were absent in Xiphias (John-
son 1975) (Table 1).
DISCUSSION AND CONCLUSION
Developmental features observed in our study are
illustrated in Figures 4-5 and 9-15. These features
along with meristic and osteological characters are
compared among the six scombroid families and the
primitive percoid Morone in Tables 1 and 2. Al-
though our conclusions are still preliminary because
of lack of adequate developmental series for many
genera, some comparisons, based largely on devel-
opment, are worth noticing.
There are three major kinds of early development
and addition of the cartilaginous neural and haemal
arches and spines along the notochord. Each kind
may differ slightly between taxa. Scombrolabrax,
Scomber (Scombrini), Scomberomorus (Scombero-
morini), and Thunnini have one kind in which there
are four initial developments on the notochord, but
not necessarily in the given order, e.g., anteriorly
dorsad, centrally dorsad, centrally ventrad, and pos-
teriorly ventrad with a subsequent merger of the
initial areas. Gempylidae, Sarda (Sardini), Istio-
phoridae, and Xiphiidae have a second kind in which
there are three initial developments, e.g., anterior-
ly dorsad, centrally ventrad, and posteriorly ven-
trad; then the addition is from anterior in a poste-
rior direction with a merger in the posterior, near
the hypural complex. Trichiurus, which lacks hypu-
rals, has the third kind in which there are two ini-
tial developments, e.g., anteriorly dorsad and cen-
trally ventrad with addition in a posterior direction.
We could not fully determine the cartilaginous
development for Acanthocybium, because of an in-
complete series, and for trichiurids with tails,
because a series was lacking.
In the Scombrolabracidae, Gempylidae, and Scom-
bridae, the vertebrae first develop by coalescence
of saddle-shaped ossifications positioned dorsad and
ventrad. We were not able to observe saddle-shaped
ossification in Acanthocybium because we lacked
specimens. The other scombroid families, Trichiu-
ridae (Trichiurus), Istiophoridae, and Xiphiidae, and
the primitive percoid Morone did not have these
saddle-shaped ossifications. Saddle-shaped ossifica-
tions have been observed during ontogeny in other
perciform fish such as Enchelyurus brunneolus
(Blenniidae) by Watson5 and Lutjanus campechanus
(Lutjanidae) by Potthoff and Kelley6. We are unable
to comment at this time on the significance of these
saddle-shaped ossifications until the ontogeny of
many more taxa is studied.
In the Scombrinae two species belonging to two
different tribes share a peculiar ossification se-
quence not observed by us in any other scombroids.
Both in Scomber (Scombrini) and Acanthocybium
(Sardini), initial ossification of the neural and haemal
arches and spines and the hypural complex started
at four locations on the vertebral column (Kramer
6Watson, W. Larval development of Enchelyurus brunneolus
from Hawaiian waters (Pisces: Blennidae: Omobranchini). Un-
publ. manuscr. Marine Ecological Consultants of Southern
California, 533 Stevens Avenue, Soloma Beach, CA 92075.
6Research on the development of Lutjanus campechanus is in
progress at the Southeast Fisheries Center Miami Laboratory, Na-
tional Marine Fisheries Service, NOAA, 75 Virginia Beach Drive,
Miami, FL 33149.
675
FISHERY BULLETIN: VOL. 84, NO. 3
1960). In other scombroids initial ossification was
only anterior and posterior (S comber omorus, Sarda
?, Thunnus, Istiophoridae) or only anterior (Scom-
brolabrax, Gempylidae, Trichiurus, Xiphias).
We believe that the relationship of Acanthocybi-
um to the Sardini should be re-examined in the
future.
The Scombrini and Scombrolabrax (Figs. 1, 9)
share a primitive development in which the second
dorsal fin, anal fin, and pterygiophores develop first
from a center anteriorly and posteriorly, and the
first dorsal fin and pterygiophores develop second,
from a center anteriorly and posteriorly in Scom-
brolabrax, but posteriorly only in Scomber except
for the first dorsal fin spine, which was added later.
The Gempylidae, Thunnini, and Scomberomorus
(Figs. 2, 3, 4, 10, 13) share an advanced develop-
ment in which the first dorsal fin and pterygiophores
develop first from the anteriormost element in a
posterior direction, and the second dorsal fin, anal
fin, and pterygiophores develop second from a
center anteriorly and posteriorly, the first dorsal fin
being separate from the second dorsal fin during
part of the ontogeny. In Acanthocybium, Sarda, and
Thunnini, the development is similar to the advanced
development of the Gempylidae and Scomberomorus
except in Acanthocybium, Sarda, and Thunnini, the
second dorsal fin spine developed first, the first dor-
sal fin spine was added later. The first dorsal fin was
separate for part of the ontogeny from the second
dorsal in Acanthocybium, but we were unable to
observe this in Sarda because of the lack of an ade-
quate size series. In Trichiurus (Fig. 5), the dorsal
fin and pterygiophores develop from the anterior-
most element posteriorly. When dorsal fin develop-
ment reaches above the anal fin, the anal fin
develops from its anteriormost element in a poste-
rior direction. Dorsal and anal fin development then
proceed posteriorly at about the same pace. Tri-
chiurus has a peculiar developmental feature, which
was not observed in any other scombroid. It was that
the anteriormost dorsal fin spines and anal spine and
rays develop before their corresponding pterygio-
phores. Pterygiophore development soon overtook
fin ray development and during further development
more pterygiophores are present than fin rays. In
the Istiophoridae and Xiphiidae, dorsal and anal fin
development differ from the previously described
groups. In the Istiophoridae (Fig. 14) the first dor-
sal fin and pterygiophores develop first from a
center anteriorly and posteriorly. When the poste-
rior portion of the first dorsal fin development
reaches above the anterior portion of the anal fin,
anal rays and pterygiophores are added mostly pos-
teriorly, although a few elements develop in an
anterior direction. The second dorsal fin develops
only in a posterior direction consecutive to the first
dorsal fin. In Xiphias (Fig. 15), the second dorsal
and anal fins and pterygiophores develop first from
a center anteriorly and posteriorly. Development of
the first dorsal fin and pterygiophores then is con-
tinuous with the second dorsal fin in an anterior
direction only.
The hypurals in all scombroids develop as separate
cartilages. Only in Scombrolabrax is there no fusion
of the hypurals in the adults. In the Gempylidae the
extent of the hypural fusion varies for different
genera and we did not observe fusion in the carti-
laginous state. For the trichiurids with tails, not
enough specimens were available to make observa-
tions on hypural fusion. In the remaining scombroids
(Scombridae, Istiophoridae, Xiphiidae) hypurals 1-4
are fused to one hypural plate in adults. Fusion to
one hypural plate came about during ontogeny by
fusion of hypurals 1 and 2 to a ventral and hypurals
3 and 4 to a dorsal hypural plate, with subsequent
fusion of these into one plate. For the ventral plate,
cartilaginous fusion occurs in all tribes of the Scom-
bridae, but in the Istiophoridae fusion is either from
cartilaginous or ossifying hypurals 1 and 2 and in
Xiphias it is always from ossifying hypurals (Table
1). In Scomber, Acanthocybium, and Istiophoridae,
the fusion of hypurals 3 and 4 to the dorsal hypural
plate is variable and occurs either during the carti-
laginous or ossifying state. In Sarda three speci-
mens have fusion of hypurals 3 and 4 in the ossify-
ing state. In Scomberomorus and Thunnus the fusion
to the dorsal hypural plate occurs always in the car-
tilaginous state, whereas in Xiphias it is always in
the ossifying state (Table 1).
The number of centra supporting the caudal rays
varies in the scombroids. In Scombrolabrax, Gem-
pylidae, Trichiuridae with tails, Scomber, and Istio-
phoridae, three vertebrae (including the urostyle)
support the caudal rays. In Xiphias only two verte-
brae support the rays. In the Scombridae more
vertebrae are involved with the support of the
caudal rays, except in Scomber. In the Scombero-
morus species examined by us, five centra support
the rays, but in some species of Scomberomorus only
four centra are involved (Collette and Russo 1984).
In Acanthocybium (Collette and Russo 1984) and
Sarda, five centra are involved with the support of
the rays, whereas in Thunnus only four centra sup-
port the caudal rays (Table 1).
Johnson (fn. 3; in press) is of the opinion that
Scombrolabrax does not belong in the Scombroidei
because it lacks most defining specializations of this
676
POTTHOFF ET AL.: DEVELOPMENT OF SCOMBROID FISHES
group. Bond and Uyeno (1981) removed Scombrola-
brax from the Scombroidei on the basis of one spe-
cialized character. We are of the opinion that Scom-
brolabrax should be retained in the Scombroidei
until we fully understand the significance of devel-
opmental characters. Scombrolabrax shares many
characters with other scombroids, in particular the
absence of predorsal bones coupled with the ante-
rior pterygiophore interneural insertion sequence,
the saddle-shaped ossifications of the vertebrae, the
sequence of neural and haemal arch and spine devel-
opment and the striking resemblance of Scombro-
labrax to Thunnini larvae.
Gempylid and trichiurid relationships await fur-
ther study when complete series of larvae of more
species become available. We believe that Gempy-
lus and Diplospinus are similar and very closely
related. We also believe that the gempylids and tri-
chiurids are very closely related, the trichiurids
representing an advanced gempylid group.
Johnson (in press) has discovered a specialization
(a stay on the 4th pharyngobranchial) unique to the
Scombridae, Istiophoridae, and Xiphiidae but absent
in other Perciformes. From our study we believe
that the billfish (Xiphias and Istiophoridae) do not
belong in the Scombroidei because they differ in
many developmental and meristic characters from
other scombroid members (Tables 1, 2). However,
until more developmental studies are done to deter-
mine the meaning and significance of developmen-
tal characters, it would be premature to suggest
rearranging the Scombroidei.
The full value of early developmental studies for
systematic purposes will be realized when similar
studies have been completed on a greater variety
of fishes. Only then will we be able to interpret the
meaning and significance of some developmental
characters presented here.
ACKNOWLEDGMENTS
We thank G. L. Beardsley, B. B. Collette, A. C.
Jones, G. D. Johnson, and W. J. Richards for critical-
ly reading the manuscript and P. Fisher for typing
many drafts of the manuscript. We thank B. B. Col-
lette, R. H. Gibbs, M. F. Gomon, G. D. Johnson, W.
J. Richards, and J. L. Russo for providing gempy-
lid and trichiurid fishes for clearing and staining.
The Scomberomorus and Acanthocybium material
was loaned to us by M. Leiby and J. Gartner from
the SEAMAP collections. M. P. Fahay, G. H. Moser,
and B. Sumida MacCall generously provided
Scomber and Sarda specimens.
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1981. Remarkable changes in the vertebrae of perciform fish
Scombrolabrax with notes on its anatomy and systematics.
Jpn. J. Ichthyol. 28:259-269.
Collette, B. B., and L. N. Chao.
1975. Systematics and morphology of the bonitos (Sarda) and
their relatives (Scombridae, Sardini). Fish. Bull., U.S. 73:
516-625.
Collette, B. B., and J. L. Russo.
1984. Morphology, systematics and biology of the Spanish
mackerels (Scomberomorus, Scombridae). Fish. Bull., U.S.
82:545-692.
Collette, B. B., T. Potthoff, W. J. Richards, S. Ueyanagi,
J. L. RUSSO, AND Y. NlSHIKAWA.
1984. Scombroidei: development and relationships. In H. G.
Moser, W. J. Richards, D. M. Cohen, M. P. Fahay, A. W.
Kendall, Jr., and S. L. Richardson (editors), Ontogeny and
systematics of fishes, p. 591-620. Am. Soc. Ichthyol.
Herpetol., Spec. Publ. 1.
Conrad, G. M.
1938. The osteology and relationships of the wahoo (Acan-
thocybium solandri), a scombroid fish. Am. Mus. Nov. 1000,
p. 1-32.
Fritzsche, R. A., and G. D. Johnson.
1980. Early osteological development of white perch and
striped bass with emphasis on identification of their larvae.
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Gosline, W. A.
1968. The suborders of perciform fishes. Proc. U.S. Natl.
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Greenwood, P. H., D. E. Rosen, S. H. Weitzman, and G. S.
Myers.
1966. Phyletic studies of teleostean fishes, with a provisional
classification of living forms. Bull. Am. Mus. Nat. Hist.
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Gregory, W. K., and G. M. Conrad.
1937. The comparative osteology of the swordfish (Xiphias)
and the sailfish (Istiophorus). Am. Mus. Novit. 952, p. 1-
25.
Johnson, G. D.
1975. The procurrent spur: an undescribed perciform caudal
character and its phylogenetic implications. Occas. Pap.
Calif. Acad. Sci. 121, p. 1-23.
In press. Scombroid phylogeny: an alternative hypothesis.
Bull. Mar. Sci. 39.
Kohno, H., M. Shimizu, and Y. Nose.
1984. Morphological aspects of the development of swimming
and feeding functions in larval Scomber japonicus. Bull.
Jpn. Soc. Sci. Fish. 50:1125-1137.
Kramer, D.
1960. Development of eggs and larvae of Pacific mackerel
and distribution and abundance of larvae 1952-56. U.S.
Fish Wildl. Serv., Fish. Bull. 60:393-438.
Leccia, F. M.
1958. The comparative osteology of the scombroid fishes of
the genus Scomberomorus from Florida. Bull. Mar. Sci.
Gulf. Caribb. 8:299-341.
Leis, J. M., and W. J. Richards.
1984. Acanthuroidei: development and relationships. In H.
G. Moser, W. J. Richards, D. M. Cohen, M. P. Fahay, A. W.
Kendall, Jr., and S. L. Richardson (editors), Ontogeny and
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Matsubara, K., and T. Iwai.
1958. Anatomy and relationships of the Japanese fishes of
the family Gempylidae. Mem. Coll. Agric. Kyoto Univ.,
Fish. Ser. Spec. No., p. 23-54.
Matsumoto, W. M., E. H. Ahlstrom, S. Jones, W. L. Klawe,
W. J. Richards, and S. Ueyanagi.
1972. On the clarification of larval tuna identification, par-
ticularly in the genus Thunnus. Fish. Bull, U.S. 70:1-12.
Merrett, N. R.
1971. Aspects of the biology of billfish (Istiophoridae) from
the equatorial western Indian Ocean. J. Zool. 163:351-395.
Nakamura, I., and E. Fujii.
1983. A new genus and species of Gempylidae (Pisces: Per-
ciformes) from the Tonga Ridge. Publ. Seto Mar. Biol. Lab.
27(4/6, Art. 10):173-191.
Okiyama, M., and S. Ueyanagi.
1978. Interrelationships of scombroid fishes: an aspect from
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Potthoff, T.
1975. Development and structure of the caudal complex, the
vertebral column, and the pterygiophores in the blackfin tuna
(Thunnus atlanticus, Pisces Scombridae). Bull. Mar. Sci.
25:205-231.
1984. Clearing and staining techniques. In H. G. Moser, W.
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Potthoff, T., and S. Kelley.
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other scombrids taken by terns in the Dry Tortugas, Florida.
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Richards, W. J., and W. L. Klawe.
1972. Indexed bibliography of the eggs and young of tunas
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1974. Analysis of the taxonomic characters of young scom-
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Sato, S.
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678
AGE AND GROWTH OF THE MARINE CATFISH,
NETUMA BARBA (SILURIFORMES, ARIIDAE), IN THE ESTUARY OF
THE PATOS LAGOON (BRASIL)1
Enir Girondi Reis2
ABSTRACT
Otolith cross sections from Netuma barba were used for age and growth determinations. There is close
agreement between average back-calculated lengths and average observed lengths determined from
otoliths at capture for each year class. One opaque and one hyaline zone is formed annually. The hyaline
zone appears to be formed during the breeding season when the estuarine mature population is scarcely
feeding. Von Bertalanffy growth parameters were estimated through Beverton's method which showed
the smallest residual variance between observed and calculated lengths for year class. The growth equa-
tion (mm) is Lt = 638 [1 - exp (-0.1287(f + 0.195))]. The largest specimen observed was a 980 mm
female, 36 years old. The life span of N. barba was estimated to be 23.1 years and the natural mortality
rate 0.13.
The sea catfish, Netuma barba (Lacepede 1803),
ranges in the western Atlantic from Bahia (lat.
17°00'S) in Brasil (Gunther 1864) to San Bias (lat.
40°32'S) Argentina (Lopez and Bellisio 1965). It is
the second most important estuarine fishery re-
source in the Patos Lagoon and is caught with gill
nets (Reis 1982a). The species accounts for about
29% of the total fish landings in the estuary from
October to December, a period when it migrates
from the sea to spawn. During the remaining
months the species is dispersed in low abundance
in the ocean (Reis in press). Observations on Netuma
barba in Brasil have been restricted to taxonomy
(Higuchi et al. 1982) and to feeding and reproduc-
tion (Ihering 1888, 1896; Nomura and Menezes 1964;
Reis in press).
Age determinations in catfishes are usually based
on reading vertebrae and pectoral or dorsal spines
(Pantulu 1962; Tweddle 1975). Pectoral spines of
Netuma barba were not used in the present study
because they showed inconsistencies in age deter-
mination. However, a preliminary investigation
revealed the presence of clear and readable zones
in otoliths. This paper deals with the interpretation
of these zones, the possible causes of zone forma-
tion, and the determination of growth of Netuma
barba in the estuary of the Patos Lagoon.
'Based on a thesis in partial fulfillment of the requirements for
the MS degree, Fundacao Universidade do Rio Grande - Rio Grande
(Brasil).
2Departamento de Oceanografia, Fundacao Universidade do Rio
Grande, Caixa Postal 474, 96200 - Rio Grande - RS, Brasil.
MATERIALS AND METHODS
Study Area
The Patos Lagoon, the largest lagoon system in
southern Brasil (10,360 km2), is connected to the
Atlantic Ocean by a narrow access canal (Fig. 1).
The estuary of the lagoon serves as a breeding,
nursery, and feeding ground for most of the coastal
fish which migrate through the canal and represent
a significant percentage of the national fishery
resource.
Collections of adult Netuma barba were made
from fish-processing plants located in the estuarine
zone of the lagoon, off the coast of Rio Grande to
Sao Lourenco do Sul, a town located 94 km inland
(Fig. 1). Juveniles were collected by special research
surveys carried out in the estuary. Data were col-
lected from September 1977 to December 1980 on
4,120 specimens. No samples were available from
January to March because of a closed fishing season
of Ariidae in the area, and few samples were col-
lected from April to July due to the absence of the
species in the estuary.
Sampling Procedure
Specimens were measured (total length, mm),
weighed (g), and sexed. Lapillus otoliths were re-
moved, sectioned transversally next to the nucleus,
polished, and were examined under a 10 x binocu-
lar microscope. The dorsal, polished half of the
otoliths was observed with transmitted light. The
Manuscript accepted January 1986.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986
679
FISHERY BULLETIN: VOL. 84, NO. 3
ESTUARY OF THE PATOS LAGOON
32?-
S. LourtnfO
do Su
PATOS
LAGOON
RIO GRANDE
do SUL
»*
>v
53<
52°
5I(
Figure 1.— Coastal lagoon system of southern Brasil (A) and the study area (B).
type of deposit (opaque or hyaline) on the otolith
margin and the number of hyaline zones were re-
corded for each otolith. Back-calculation was done
over the surface, the total length of the otolith (Co)
and the length between the nucleus and each hya-
line zone (ci) (Fig. 2) were measured with an ocular
micrometer. The term nucleus used here refers to
the central area of the otolith limited by the first
zone (Jearld 1983).
Growth curves for males and females were cal-
culated using the mean lengths for year class. The
parameters of the von Bertalanffy growth equation
were determined:
Lt = Lm [1 - e-^'-W]
(1)
where Lt is the total length at time t, LM is the
maximum attainable size, K is the growth coeffi-
680
REIS: AGE AND GROWTH OF MARINE CATFISH
VS.
a.e.
s.e.
d.s.
Figure 2.— A lapillus otolith oiNetuma barba showing opaque ( + )
and hyaline (b) zones, the nucleus (N), the axes where back-
calculation was made (Co = distance between the nucleus and the
otolith's edge; ci = distance from the nucleus to "i" hyaline zone)
and the position of otolith on fish head (a.e. = antisulcal end; s.e.
= sulcal end; d.s. = dorsal surface; v.s. = ventral surface; and
hyaline zones = I-IX).
cient, and t0 a correction on the time axis. The
parameters of Equation (1) were estimated by deter-
mining the predictive regression of ln(Loo - Lt)
against t (Beverton 1954):
lnCZ^ - Lt) = \nL„ + K(t0 - t)
(2)
where K is the slope of the regression line and the
^/-intercept of Equation (2) can be equated to In Lm
+ Kt0 providing the value of t0 (Ricker 1975). Trial
plots, including values of Lm first derived by the
methods of Walford (1946) and Gulland (1964),
yielded the L^ which gives the straightest line. The
agreement between observed and calculated lengths
for year class was determined by residual variance
(S2y) expressed by
„,„ Z. (observed Lt - calculated Lt)2
o y = (o)
N - 1
where N is the number of age classes.
Length-weight relationship was determined for
males and females
Wt = t*Ltv
(4)
where Wt is the weight at time t, and \x and v the
coefficients of the functional regression between Wt
and Lt (Ricker 1973). The condition factor was
calculated for each sex as follows:
K =
Wt
Ltv
(5)
Wt = W*, [1 - e-K«-y]"
(6)
expressed growth in weight, where W„ is the max-
imum attainable weight obtained by solving for L^
in Equation (4).
The life span was estimated:
^•0.95 - ^0
ln(l - P)
K
(Taylor 1960) (7)
where A0 95 is the time required to attain 95% of
Loo, P = 0.95 and t0 and K are derived from the
growth equation. The natural mortality coefficient
(M) was estimated according to Taylor (1960)
M =
ln(l - P)
A0.
(8)
95
and
Statistical analyses were done when necessary
(Snedecor and Cochran 1970; Sokal and Rohlf 1981).
RESULTS AND DISCUSSION
Age Determination
The lapillus otolith used for the determination of
age oiNetuma barba is the most developed ear bone
in the Ariidae (Stinton 1975), its length attaining
3% of fish fork length (Reis 1982b). Growth zones
can be observed on a sectioned otolith from the
sulcal to the antisulcal end and from the nucleus on
the dorsal face to the ventral one (Fig. 2). The hya-
line and opaque zones are clearly evident even in
otoliths of old specimens. Under transmitted light
the opaque zones, or fast-growth zones, are white
(broad) and hyaline zones, or slow-growth zones, are
dark (narrow) (Fig. 2). Warburton (1978) counted
growth checks on whole otoliths of Galeichthys
caerulescens (Giinther), and Dmitrenko (1975)
studied Arius thalassinus (Riippel) by viewing the
otoliths the same way as in the present paper. The
number of hyaline zones on sectioned otoliths and
of growth checks observed on whole otoliths (War-
burton 1978) were compared. A smaller number of
growth checks was encountered in all cases when
using whole otoliths.
In the present study only 2.4% of the otoliths were
considered illegible. About 60% agreement was ob-
tained when otoliths were read on two different oc-
casions separated by a month. Disagreement was
due to the inability to distinguish the first hyaline
zone and those near the otolith's edge. When the
same otoliths were analyzed for the third time, the
681
FISHERY BULLETIN: VOL. 84, NO. 3
agreement between observations increased to
79.9%.
Time of Zone Formation
The percentage of hyaline and opaque edged oto-
liths was plotted for each month (Fig. 3). Otoliths
showing hyaline edge are more abundant in Decem-
ber when they comprise 63.7% of the total; opaque
edged otoliths are fewer in this month (33.9%). Stu-
dent's £-test (Snedecor and Cochran 1970) showed
that proportions between hyaline and opaque edged
otoliths differ significantly (P < 0.05) for most
months (Fig. 3). Also, the mean width of the opaque
zone on the otolith edge decreased towards the end
of the year (Fig. 4), indicating a recent hyaline zone
formation. The period of zone formation is not the
same for all individuals, the result of individual
growth differences. It is evident, however, that only
one hyaline and one opaque zone is formed each
year. Formation of slow-growth zones during warm
months in Netuma barba coincides with the spawn-
ing period and the cessation of feeding activity (Reis
in press). Both events suggest a decrease or a pause
in growth when hyaline zones are formed. Menon
(1953) observed that decreased feeding and gonad
maturation may cause a periodic formation of the
growth marks in skeletal parts of fish. During the
too
90
80-
j 70
Ul
0 60
ui
ec
"■ 50
ui
«* 40
§ 30
e
Ul
01 20
10
/ \
/ \
/ \
— HYALINE EDGE
-x OPAQUE EOGE
155 2W 179
OCT. NOV. DEC.
1977
48 74 22 12 75 42 73 44
APP..MAY.JUN. JUL. AUG. SEPT. OCT. NOV.DEC.
1978
35 23 76 82 67
AUG.SEPTQCT. NOV DEC.
1979
65 175 251 200 n
SEPT.OCT.NOV. DEC. MONTH
1980
Figure 3.— Percentage of hyaline and opaque edge on otoliths of Netuma barba related to the months of four years (* P < 0.05; n =
number of specimens).
z
o
N
4-
o
o
ui
X
X
\-
o
MALES
t
SEPT.
55
— i —
OCT.
101
ft
80
ft
FEMALES
fl
26
71
NOV.
DEC.
T
SEPT.
OCT.
141
— I —
NOV.
94 n
— i
DEC. MONTH
Figure 4.— Mean width and confidence limits at P < 0.05 level of the last opaque zone
on otolith's edge for males and females of Netuma barba (n = number of specimens).
682
REIS: AGE AND GROWTH OF MARINE CATFISH
remaining months, when Netuma barba is at sea
actively feeding and the gonads are resting (Reis in
press), the opaque zones appear to be laid down due
to fast somatic growth. According to Pannella
(1974), fishes of temperate environments tend to
form opaque zones or fast-growth zones during
warm months but the synonymity of the terms sum-
mer and opaque, winter and hyaline has to be
demonstrated in each instance rather than accepted
as a general fact. For Netuma barba slow-growth
zones are formed during warm months and may be
related to the maturation of the gonads and a pause
in feeding activity. Gonad maturation may be one
of the causative factors of hyaline formation in
adults; however, a plausible cause still needs to be
established for immature specimens.
GROWTH
Growth in Length
Sectioned otolith lengths (measured as shown in
Figure 2), and fish lengths were best fitted to the
power curve:
Lt = 1.89 Co1047
r = 0.960;
n = 689,
and the equation for back-calculation was
, 1.047
Lt i = Lt
~Co
where Lt % is the length of fish when zone "i" was
formed. Observed and back-calculated mean lengths
for year class for each sex increase as one opaque
and one hyaline zones are formed in the otolith each
year (Table 1). Up to age 11, the mean lengths are
similar; older females had mean lengths greater than
males. The same was true for mean weight although
a small number of specimens were analyzed from
age 11 onward. Observed lengths are usually higher
than back-calculated lengths except in ages that few
specimens were analyzed.
Lengths corresponding to ages 8 to 12 are most
frequent in the samples since they are most affected
by the mesh size of the fishing gear used in the
estuary. Mean observed lengths at these ages agree
closely with mean back-calculated lengths (Fig. 5)
for both sexes. Gill nets are highly size selective and
retain fish at lengths of 370-520 mm (Reis 1982a).
The analysis of variance (Sokal and Rohlf 1981)
showed that observed lengths at ages 5, 6, and 7
are significantly higher than back-calculated lengths
(P < 0.05) which could be due to the capture of the
largest specimens of these ages since the minimum
size of fish held by gill nets depends on the maxi-
mum body girth (opercle). Mean back-calculated
lengths showed no definitive tendencies for any
age class (Fig. 6) indicating no growth changes. Fur-
Table 1 .—Mean observed and back-calculated lengths of males
and females of Netuma barba for each age class (sample size in
parentheses).
Estimated
age
Mean observed
length
Male
Female
Mean back-calculated
length
Male
Female
1
84
96
65
63
( 10) |
4)
(310)
(370)
2
145
152
140
137
( 31) |
21)
(303)
(371)
3
203
197
193
192
( 40)
50)
(295)
(362)
4
228
261
244
245
( 7)
2)
(291)
(359)
5
348
146
300
299
( 16)
1)
(286)
(357)
6
378
365
347
347
( 28)
11)
(281)
(349)
7
403
394
386
385
( 59)
56)
(263)
(336)
8
415
416
413
412
(144)
111)
(241)
(313)
9
433
431
430
433
(291)
281)
(140)
(193)
10
452
463
444
446
( 94)
120)
( 79)
(129)
11
476
493
455
462
( 73)
138)
( 31)
( 54)
12
490
526
460
507
( 57)
51)
( 8)
( 8)
13
464
602
508
612
( 15)
23)
( 4)
( 3)
14
551
667
480
637
( 10)
21)
( 3)
( 2)
15
522
622
520
578
( 13)
5)
( 2)
( 1)
16
533
620
528
608
( 10)
3)
( 1)
( 1)
17
494
647
546
637
( 2)
2)
( 1)
( 1)
18
620
714
564
657
( 1)
; 1)
( 1)
( 1)
19
588
554
—
666
( 4)
3)
—
( 1)
20
550
860
—
696
( 1)
1)
—
( 1)
21
520
520
—
706
( 2)
2)
—
( 1)
22
490
649
—
—
( 1)
1)
—
—
23
—
736
■n
—
—
24
680
( 1\
'/
—
—
36
930
980
—
—
( 1)
1)
—
—
683
FISHERY BULLETIN: VOL. 84, NO. 3
Figure 5.— Mean observed and back-calculated
lengths for year class of Netuma barba (* P <
0.05).
| 500
h 400
o
y 300
< 200
O
•- 100
.-^1*-*
-*-~
.-3P*
S*
S
-+■ BACK-CALCULATION
-OBSERVED DATA
I 'I I I T I"
I 2 3 4 5 6 7 8 9 10 II 12
ESTIMATED AGE
40
20
40
20
40
20
40
20
1st HYALINE ZONE 2nd HYALINE ZONE ESTIMATED AGE
'\.
/
/
\
f I * f I "^^^T"
/
n- II
n-19
T ■ T » ■
V
r-£
n»20
40-
v
o
2
UJ
2 20
cc
b.
UJ
° 40
Z^y\
v
n=34
■i r- ■ i"1
/
/•
S
r
\
./
. — ■-
n-206
2
UJ
cc
20
40
20
40
20
/
/'
/
\
n*l36
:/v
r
/
\
V
n-126
VL
\.
\
n«94
40'
20
vx
I * I
n«!8
10
12
30 70 90 110 130 90 110 130 150 170 190 210
TOTAL LENGTH (mm)
Figure 6.— Back-calculated lengths frequencies at first and second hyaline zones
for year class of Netuma barba (n = number of specimens).
thermore, as the modes for each year class are
similar, age determination can be considered
consistent.
Validation of Age
Validation of the otolith method for aging Netuma
684
REIS: AGE AND GROWTH OF MARINE CATFISH
barba is supported by the following: 1) one opaque
and one hyaline zone is formed annually (Figs. 3,
4); 2) a gradual decrease of length increments with
age (Table 1); 3) observed lengths generally agree
with back-calculated lengths (Fig. 5); and 4) distri-
bution of back-calculated lengths for previous ages
shows similar modes for each year class (Fig. 6).
Length-weight Relationship and
Condition Factor
A total of 685 specimens captured during 1980
was used to compute the length-weight relationship
for each sex:
Male Wt = 4.70 x 10"6 Lt3u
Female Wt = 2.19 x 10"6 Lt326
Total Wt = 4.41 x 10"6 Lt315
r = 0.992 n = 332
r = 0.952 n = 363
r = 0.987 n = 685
The analysis of covariance (Snedecor and Cochran
1970) at P < 0.05 level showed significant difference
only for the \i value, and for that reason condition
factor (K) was determined for each sex. There is a
decrease of mean K values towards the end of the
year (Fig. 7). The condition factor for males is
always higher probably due to a more intense feed-
ing prior to reproduction. Low K values reveal the
stress the fish suffers when it is scarcely feeding and
fat reserves are being diverted to gonad maturation
(Reis in press), thereby causing a cessation of
growth. I proposed that K values for males will
sharply decrease after spawning due to an oral in-
cubation period that lasts 1 to 2 mo and prevents
males from feeding (Reis in press).
Calculation of Growth
Parameters
cr
o
t-
z
o
Q
Z
o
o
cc
o
b.
O
o
fl 8
fl
ft
MALES
&
m
hlO o
m
z
H
O
I
I>
10
34 35
54 66
56
44
FEMALES
m
3J
O
o
i
>
10?
26
H
SEPT.
36 48
I TC
OCT.
72 85
X JL
NOV.
32
X
68 n
DEC. MONTH
Figure 7.—K condition factor and percent change for males and
females of Netuma barba related to time (n = number of specimens;
I = first half of the month; II = second half of the month)
Von Bertalanffy growth parameters were esti-
mated by Beverton's (1954) method which presented
the smallest residual variance between observed and
calculated lengths for year class on the ages that
are most affected by gear selectivity (8-12 yr old).
For fish populations captured from a certain age on-
ward, the smallest residual variance should be
sought for all year classes from age at first capture.
For Netuma barba the smallest residual variance
could not be ascertained by this method because the
true length distribution is unknown due to the use
of gillnets as fishing gear. Growth equation for age
1 to 12 for both sexes in represented by
Lt = 638 [1 - e-o.i287(t+o.i95)]_
Figure 8 shows both calculated and observed lengths
for each year class.
Growth in weight for each sex resulted in
Male
Female
Wt = 2981.89 [1 - e-°-1287<e+0-195)fu
Wt = 3035.70 [1 - e-0.128W + 0.195)]3.26
-500
E
^400
o
-I
300
_>200
2100-
S
.^"
Loo=638nrn * * Colculoted Ltngtht
K =0,1287 . _ Observed Length*
I 2 3 4 5 6 7 8 9 10 II 12
ESTIMATED AGE
Figure 8.— Growth curve of Netuma barba.
685
FISHERY BULLETIN: VOL. 84, NO. 3
Maximum Size and Age,
Life Span, and Mortality Rate
Netuma barba is a long lived, slow growing species
with a low mortality rate. Specimens as long as the
theoretical mean length (638 mm) are frequently
captured. The largest catfish observed was a 980
mm female 36 yr old. Netuma barba life span was
estimated to be 23.1 yr and its mortality rate was
0.13. I assumed that the estimate of M (natural
mortality) is accurate, since Netuma barba reveals
a long life span, a capacity to avoid predation
through the defense represented by its hard dorsal
and pectoral spines and a parent-juvenile care
behavior (Reis in press). Pauly (1980) suggested that
species with low mortality rates are related to high
Loo values and to low growth coefficients. These
characteristics combined with the fact that Netuma
barba has a low fecundity (Reis in press) define the
species as /f- strategists (Gunderson 1980).
ACKNOWLEDGMENTS
I am greatly indebted to J. P. Castello for his
assistance and valuable suggestions and to the staff
of Fisheries Biology Laboratory, Department of
Oceanography, Fundacao Universidade do Rio
Grande.
LITERATURE CITED
Beverton, R. J. H.
1954. Notes on the use of theoretical models in the study of
the dynamics of exploited fish populations. U.S. FisKLab.,
Beaufort, N.C., Misc. Contrib. 2, 159 p.
Dmitrenko, E. M.
1975. Size-age composition of the giant catfish, Arius
thalassinus in the vicinity of Kathiawar Peninsula (India).
Vopr. Ikhtiol. 15:695-702.
GULLAND, J. A.
1964. Manual of methods for fish population analysis. FAO
Fish. Tech. Pap. 40, 61 p.
Gunderson, D. R.
1980. Using r-K selection theory to predict natural mortality.
Can. J. Fish. Aquat. Sci. 37:2266-2271.
GUNTHER, A.
1864. Catalogue of the fishes in the British Museum. 5.
Catalogue of the Physostomi; Ariina. Br. Mus., p. 138-
182.
Higuchi, H., E. G. Reis, and F. G. Araujo.
1982. A new species of marine catfish from the coast of Rio
Grande do Sul, with comments on the nominal genus Netuma
Bleeker, 1858 of the Southwest Atlantic (Siluriformes,
Ariidae). Atlantica 5(1):1-15.
Ihering, H., Von.
1888. Ueber brutpluge und Entwicklung des bagre (Arius
commersoni). Biol. Cent. 8:268-271.
1896. Os peixes da costa do mar do Estado do Rio Grande
do Sul. Rev. Mus. Paul. 2:25-63.
Jearld, A., Jr.
1983. Age determination. In L. A. Nielsen and D. L. John-
son (editors), Fisheries techniques, p. 301-324. Am. Fish.
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LOpez, R. B., and N. B. Bellisio.
1965. Contribucion al conocimiento del Tachysurus barbus
(Lacepede), bagre del mar argentino (Pisces, Ariidae). In
Anais II Congreso Latino-Americano Zoologia, p. 145-153.
Menon, M. D.
1953. The determination of age and growth of fishes of
tropical and subtropical waters. J. Bombay Elist. Sec. 51:
623-635.
Nomura, H., and N. A. Menezes.
1964. Peixes marinhos. In P. E. Vanzolini (editor), Hist6ria
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Pannella, G.
1974'. Otolith growth patterns: An aid in age determination
in temperate and tropical fishes. In T. B. Bagenal (editor),
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Univ. Reading, Engl.; Unwin Brothers, Ltd., Engl.
Pantulu, V. R.
1962. On the use of pectoral spines for the determination of
age and growth of Pangasius pangasius (Hamilton Buch).
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Pauly, D.
1980. On the interrelationship between natural mortality,
growth parameters, and mean environmental temperature
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Reis, E. G.
1982a. Idade, crescimento e reproducao de Netuma barba
(Siluriformes, Ariidae) no estuario da Lagoa dos Patos (RS).
M.S. Thesis, Fundacao Universidade do Rio Grande, Brasil,
114 p.
1982b. Anatomy of the inner ear of Netuma barba (Lacepede,
1803), Siluriformes, Ariidae. Atlantica 5(1): 16-22.
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686
MONITORING THE SEA SURFACE CHLOROPHYLL CONCENTRATION
IN THE TROPICAL PACIFIC:
CONSEQUENCES OF THE 1982-83 EL NINO
Yves Dandonneau1
ABSTRACT
The sea surface chlorophyll concentration (SSCC) is routinely measured in the tropical Pacific using filtra-
tions made aboard merchant ships that sail from New Caledonia to Japan, North America, Panama, New
Zealand, and Australia. About 4,000 measurements are collected every year, allowing a tentative monitor-
ing of SSCC in the Pacific. Heavy smoothing made it possible to map quarterly charts of SSCC which
cover the 1982-83 El Nino episode. The usually enriched belt which corresponds to the equatorial upwell-
ing vanished after September 1982, except for a reduced zone east of long. 120° W, where a moderate
enrichment persisted throughout the warm event. It recovered after July 1983, spreading westwards
to long. 170°E. During the mature phase of El Nino (October 1982-June 1983), an enriched zone ap-
peared in the western Pacific, centered at about lat. 7°N, consistent with a rise of the thermocline in
this region. An examination of oceanographic data collected in this region since 1970 shows that nutrients
from below the thermocline are consumed by the phytoplankton during each El Nino. This western Pacific
enrichment was weakened with time, and the period from April to June 1983 was characterized by low
SSCC values over most of the tropical Pacific. Unusually high SSCC values are reported in subtropical
zones, during the austral winters of 1982 and 1983 in the southwestern Pacific and during the 1982 autumn
in the northeastern Pacific, which may be due to advection of rich water from higher latitudes and to
intensified vertical mixing by strong westerly winds, respectively.
El Nino was first observed and experienced in Peru,
where it was given its name and became a familiar
part of Peruvian life. Although the southern oscilla-
tion was identified more than 60 yr ago (Walker
1924), the relation between the El Nino phenomenon
and ocean-scale features was only established after
the 1957-58 event by Bjerknes (1966). It is now well
established that El Nino is simply the most obvious
consequence of important oceanographic and
meteorological changes in the Pacific Ocean
(Donguy and Henin 1976; Quinn et al. 1978; Cane
1983). One would expect biological changes at the
same scale. These, however, have only been studied
in the eastern Pacific (Walsh 1981; Chelton et al.
1982; Barber and Chavez 1983) where a pronounced
decrease in phytoplankton biomass and primary pro-
duction is observed. Farther west in the equatorial
zone, the decrease in primary productivity has been
shown only by indirect observations on marine birds
(Schreiber and Schreiber 1984) and on abnormal
distributions of some fishing grounds in relation to
changes of water mass (Donguy et al. 1978; Yama-
naka 1984). The difficult problem of monitoring the
intensity of primary production on a large scale is
troupe SURTROPAC, Centre ORSTOM, B.P. A5, Noumea,
New Caledonia.
4S7 -US'
Manuscript accepted January 1986.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
usually reserved for satellite-borne sensors. A
modest attempt, however, is in progress, as a part
of the SURTROPAC program (ORSTOM, Noumea)
based upon chlorophyll samples taken by voluntary
observers on ships of opportunity. Each year about
4,000 sea surface chlorophyll concentrations (SSCC)
are collected in this way, distributed along maritime
lanes from the Tasman Sea to Panama, North
America, or Japan. These data cover the tropical
Pacific from lat. 30 °S to 30 °N, and from long.
140°E to 80°W. There are large gaps both in space,
between the main lanes, and in time, between con-
secutive crossings. But, on a quarterly basis, the
SSCC data are numerous enough to allow a crude
view of the whole tropical Pacific Ocean, with the
advantage of using a single methodology. The con-
sequences of the 1982-83 El Nino can thus be ex-
amined, and most of the attention will be directed
towards the central and western Pacific, where pres-
ent knowledge is very incomplete.
METHODS
Chlorophyll Measurements
SSCC measurements are made according to a non-
extractive method (Dandonneau 1982). Twenty milli-
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FISHERY BULLETIN: VOL. 84, NO. 3
liters of seawater are filtered on 13 mm HAWP
Millipore filters, using a syringe and Swinnex type
filtering cartridges. The filters are then stored in
a dark place at ambient temperature. When the
observing ship reaches Noumea, the filters are taken
to the laboratory for fluorescence measurements.
A 3-wk minimum time lag is needed between filtra-
tion and measurement, after which degradation pro-
cesses lead to stable fluorescent chlorophyll by-
products on the filters. The fluorescence (Ff) of the
filters is then measured without extraction, using
a specially adapted sample holder.
The measurement error e is proportional to the
chlorophyll concentration C and can be expressed
as e = |SSCC-C|/C where SSCC is measured by the
non-extractive method while C is obtained by a more
conventional technique (Holm-Hansen et al. 1965).
Ninety-five percent of e values are <0.6 (Dandon-
neau 1982, and confirmed by later tests). This value
is probably an overestimate of e since it results both
from the error on SSCC and from the unknown error
on C. Different phytoplankton populations can also
result in different fluorescence to chlorophyll ratios
for the dry filters. This ratio has shown no signifi-
cant change between winter and summer conditions
around New Caledonia where a mixed regime alter-
nates with a stratified one (Dandonneau and Gohin
1984). The risk of a variation of the ratio in other
environments has not been examined, and must be
kept in mind. The few SSCC data points at latitudes
higher than 30° were not taken into account for this
reason.
Calibrations
SSCC is estimated using SSCC = k Ff where k
is a calibration coefficient that must be corrected
from time to time. Twenty milliliters from a sea-
water sample are filtered giving a fluorescence Ff0
after 21 d of storage. A larger volume V from the
same sample is filtered on a glass fiber filter,
ground, and extracted by a volume v of 90% acetone.
The fluorescence of the extract is Fe0. Knowing the
fluorescence to chlorophyll ratio of the fluorometer,
R0, determined from a known solution of pure
chlorophyll a, we can estimate the following chloro-
phyll concentration of the seawater sample:
C0 = (Fe0 x v)l(R0 x V);
we obtain then k0 = Ff0IC0.
k0 is sensitive to detrital material in turbid
coastal waters, so these main calibrations are made
during offshore oceanographic cruises. As such op-
portunities are infrequent, secondary calibrations
are made more frequently with known solutions of
pure chlorophyll a, giving Rt instead of R0. We then
assume that kt = k0 x RJRq. This procedure does
not consider correction for chlorophylls b and c, nor
does it consider correction for phaeopigments, which
has recently proven to be uncertain when the fluor-
ometer is fitted with a commonly supplied blue ex-
citation lamp (Baker et al. 1983). Although the SSCC
data presented in this work are expressed in milli-
grams of chlorophyll a, they should be considered
only as indices of phytoplankton abundance.
Data Rejection
The crew members who take the seawater
samples and make the filtrations are voluntary
observers. Errors may occur which are difficult to
detect because, unlike temperature or salinity, 1)
any SSCC value in the interval 0-1 mg-m-3, which
covers almost the whole data set, is a possible one
anywhere in the tropical Pacific, and 2) the auto-
correlation of SSCC decreases very quickly with
time or space, so that surrounding data cannot help
in error detection. Therefore, all the data are ac-
cepted, unless the filter exhibits an obvious fault
(i.e., breaking, stain, extraneous material). Occa-
sionally, all the data from a ship's voyage were
evidently too high, by a factor 3 or 5. Contamina-
tion by a polluted sampling bucket was the cause,
and the data from the entire voyage were rejected.
Other possible errors are more insidious, such as
insufficient care in keeping the filters out of light,
or using an oxidized sampling bucket. These errors
result in slightly lowered values, but there is no way
to correct them and, in most cases, no way to even
detect these biases. Such data are entered in the
data bank. As a resulting constraint, any estimate
from this SSCC data set must be developed from
many data, in order to minimize the effect of a few
possibly biased values.
Mapping Techniques
In a previous work (Dandonneau and Gohin 1984)
the principles of objective analysis were applied to
compute best estimates of SSCC at a given place
and time in the southwestern tropical Pacific. The
studied area in the current study is much larger and
more complex, and the density of data is not high
enough to allow good estimates of the statistics of
the field. Hence, the use of an objective analysis of
the SSCC data has been excluded. The SSCC
mapped here on Figure 1 have been estimated using
688
DANDONNEAU: MONITORING SEA SURFACE CHLOROPHYLL CONCENTRATION
20*N
M'S
20*N
20*S .
20*N
M'S
20* N
20*S
UO'E
100" W
20* N
20*S
100'W
Figure 1. -Quarterly charts of SSCC (sea surface chlorophyll concentrations) in the tropical Pacific from January 1, 1982 to December
31, 1983. Areas where SSCC is >0.10 mg nT3 are shaded with large dots. Smaller dots represent the data points.
1=1 1=1
where i3 is the SSCC estimate at longitude Xj and
latitude y^, and ptj is the weight given to observa-
tion t{ for the estimation tj. p^ is given by
Vij = [R2 + (Xi - xf + a2 (yt - t//]"1
where a accounts for anisotropy of the SSCC varia-
tions in space. We used a = 2, so that observations
at a distance Ay in latitude are given the same
weight as observations at a distance kx = 2hy in
longitude, p^ was set to zero when (xt - Xjf + a2
(Vi ~ Vj)2 was >160, so that the observations were
considered as "non useful" when outside an ellipse
centered at (Xj, y^) with a principal axis equal to
about 25° longitude, and a small axis equal to about
13° latitude. In order to avoid hazardous estimates
at the margin of the contoured area, tj has not been
estimated when rij (the number of useful observa-
tions) was <12.
689
FISHERY BULLETIN: VOL. 84, NO. 3
R = 0 would give an infinite weight to an obser-
vation k available at xk = Xj and yk = jjj. We would
then obtain tj = tk regardless of the other observa-
tions. This is acceptable only if the instrumental and
sampling errors on tk were null, which is not the
case. Thus, R accounts for the errors on the obser-
vations. We choose R2 = 25, which, together with
a = 2 and ptj > (25 + 160)" \ performed an effi-
cient smoothing and preserved the large-scale infor-
mation.
RESULTS
The sequence of quarterly mean SSCC for 1982
and 1983 is presented in Figure 1, together with the
positions of the data. The western part, north of lat.
20°N, is poorly sampled. The data range between
0.05 and 0.20 mg-m-3. The highest values are
found during the northern spring of 1982, and the
northern winter of 1983. The 1982 winter, and the
spring and fall of 1983 exhibit a few values >0.10
mg-m"3. The 1982 winter and fall show low SSCC,
like the summer of both years, below 0.10 mg-m-3.
The eastern part, north of lat. 10°N, has gener-
ally low SSCC values, often below 0.05 mg-m-3.
Exceptions are the spring of 1982 at the extreme
north, and, mainly, the fall of 1982 during which the
mean values exceeded 0.20 mg-m-3 off California.
Low SSCC values are observed in the western
part between the Equator and lat. 20°N until the
summer of 1982. They are abruptly replaced at the
end of 1982 by high values which persist until March
1983. Later, low values, generally below 0.05
mg-m"3, dominate again between lat. 5°N and
20°N, while SSCC >0.10 mg-m"3 shift back south-
ward to the Equator.
The equatorial zone shows high SSCC in January-
March 1982, between America and long. 160° E.
Values higher than 0.10 mg-m-3 spread from lat.
10°N and 10°S in the central Pacific, and to 15°S
at 120°W. From April to June 1982, the enriched
zone shifts eastwards and southwards. The east-
wards shift continues between July and September
and is accompanied by a decrease of SSCC in the
eastern Pacific, with mean values <0.15 mg- nr3.
From October 1982 to June 1983, a narrow band
with SSCC between 0.10 and 0.15 mg-m"3 in the
eastern Pacific is the only remnant of the equator-
ial enrichment. A normal situation returned after
the El Nino, in July-September 1983, with SSCC
values >0.15 mg-m-3 spreading westwards to
long. 170°E. In October-December 1983, SSCC
>0.10 mg-m-3 are seen all along the Equator.
South of lat. 20° S, an SSCC increase is observed
during the austral winter. The increase started in
April-June in 1982, the maximum was reached in
July-September, with SSCC >0.20 mg-m-3 spread-
ing northward to 22 °S, and low values were seen
again in October-December. The increase during the
austral winter of 1983 was of a lesser extent, being
well developed only during July-September, with
SSCC >0.20 mg-m-3 limited to the south of 28°S.
The intermediate zone, from lat. 10°S to 20°S,
between the equatorial upwelling and higher lati-
tudes where a winter increase is observed, gener-
ally has low chlorophyll concentrations, below 0.10
mg-m-3. The lowest concentrations are seen in
austral summer, from October 1982 to June 1983,
and in October-December 1983. The highest concen-
trations are associated with a strengthening of the
equatorial upwelling (around long. 140 °W in April-
June 1982; westwards spreading of richer waters
from the eastern Pacific in July-September 1982 and
1983).
When looking at the whole series of maps, the
most striking feature is the reduction of the equa-
torial upwelling enriched area after the onset of El
Nino. The most pronounced stage was in April-June
1983, with poor waters over most of the tropical
Pacific. On the contrary, a zone centered at lat.
10°N, west of the dateline, which is usually occupied
by chlorophyll-poor waters, had higher SSCC dur-
ing the 1982-83 El Nino.
DISCUSSION
Equatorial Upwelling
The collapse of the equatorial upwelling after the
onset of El Nino, when westerlies have replaced the
trade winds at the Equator, consistently results in
a decrease in SSCC. This decrease has already been
documented for the eastern Pacific in the Galapagos
Islands region by Feldman et al. (1984) using sea
color satellite images. It corresponds to a decrease
in primary production of the whole photic layer
(Barber and Chavez 1983). The data presented here
show that the equatorial zone was impoverished
westwards to nearly 180°. This is in agreement with
the reproductive failure and disappearance of sea-
bird communities at Christmas Atoll (lat. 2°N, long.
157°W) in November 1982; Schreiber and Schrei-
ber (1984) attributed these events to the establish-
ment of an oligotrophic oceanic ecosystem instead
of a productive one. Successful reproduction started
again for some birds species in June 1983, and hatch-
ing occurred in July-September 1983, when SSCC
690
DANDONNEAU: MONITORING SEA SURFACE CHLOROPHYLL CONCENTRATION
higher than 0.15 mg-m~3 reappeared at the
Equator (Fig.l).
Western Pacific Around Lat. 7°N.
Under normal conditions (see Figure 1: January
to March 1982, July to December 1983) the equa-
torial upwelling also drives a chlorophyll-rich zone
west of 180°. This does not appear on the map of
Koblentz-Mishke et al. (1970) on the primary pro-
duction in the world ocean, but is described as an
episodic feature by Oudot and Wauthy (1976). The
area with SSCC >0.15 mg-m~3 which appears
north of the Equator, centered at about 7°N from
October 1982 to March 1983 (Fig. 1) has nothing to
do with the equatorial upwelling. Based on approx-
imately 100 SSCC data points obtained by three dif-
ferent merchant ships, this chlorophyll-rich area can
hardly be thought to result from measurement
errors. It rather may be related to the eastward
draining of warm water from the western tropical
Pacific and consequent thinning of the surface mixed
layer and drop of the sea level (Wyrtki 1985). A
simultaneous cooling of the sea surface by 1°C oc-
curred in this region during El Nino, which can be
explained by advection of cooler water, and also by
other potentially important processes which are
more difficult to quantify (Meyers and Donguy
1984). The observed SSCC increase supports the
hypothesis that vertical mixing of cooler nutrient-
rich deep water might be one of these processes.
Even if vertical mixing is unlikely, the 50 m rise of
the thermocline which has been observed at lat. 7°N
between January 1982 and January 1983 (Meyers
and Donguy 1984) allows more light to penetrate
to the deep chlorophyll maximum. This hypothesis
is supported by the shift which occurred between
January 1982 and January 1983 in the nitrate-tem-
perature relationship (Fig. 2; data collected by the
Japan Meteorological Agency along long. 137°E
aboard RV Ryofu Maru; Anonymous 1972-84). The
nitrate concentration at a given temperature (which
we assume to represent a given water mass)
dropped by about 2 ^moles-L-1. Shifts in the
nitrate-temperature relationship provide informa-
tion on the consumption of nitrate by the phyto-
25
20-
TCC)
N03 (yumole.1"1 )
(♦) January 1982
(♦) January 1972
January 1973
•ITCC)
Figure 2.— Nutrient-temperature relationships between lat. 6°N and 9°N. Crosses: observations before an El Nino; open circles:
observations after an El Nino. (Data from the RV Ryofu Maru cruises at long. 137°E, Anonymous 1972 to 1984).
691
FISHERY BULLETIN: VOL. 84, NO. 3
plankton (Voituriez and Herbland 1984). We can
then suggest that new nitrates have been assim-
ilated during El Nino in the western Pacific at lat.
6-9°N. The 2 /imoles-L-1 drop in nitrate concentra-
tion is observed in the interval 17°-22°C, corre-
sponding to a 35 m thick water layer (Anonymous
1972-84), so that the amount of new nitrates used
by photosynthesis is 70 fimoles-m"2, or 980
mg-m-2. If CIN = 9.01 and C/Chl = 114 in surface
waters of the oligotrophic central North Pacific
(Sharp et al. 1980), this amount of nitrogen corre-
sponds to 77 mg Chi a-m-2. It represents an im-
portant supply in an ecosystem where the chloro-
phyll concentration is usually low.
Figure 3 shows the variations of integrated
chlorophyll (0-200 m) between lat. 6°N and 9°N at
long. 137°E, obtained from the Ryofu Maru data
(Anonymous 1972-84). Values during the 1982-83 El
Nino are similar to those since July 1981, i.e., below
50 mg-m-2. SSCC from the same data set also
shows low values during the 1982-83 El Nino, con-
flicting with the results mapped on Figure 1. Re-
cent El Nino events in 1972 and 1976 resulted in
a drop of the sea level in the western Pacific (Meyers
1982). Low sea level was also recorded during an
El Nino like event in the western Pacific in 1979-80
(Donguy and Dessier 1983). These low sea level
episodes during which the thermocline is shallow
(Wyrtki 1978), yet do not correspond to high SSCC
or high integrated chlorophyll values in the Ryofu
Maru results (Fig. 3). It seems however that the
nutricline depth is shallower during these four epi-
sodes (Fig. 3). All of them are moreover charac-
terized by a shift in the nutrient-temperature rela-
tionship (Fig. 2) indicating a consumption of new
nutrients. We are dealing with an SSCC enrichment
in the northwestern tropical Pacific which persists
for several months (October 1982-March 1983) and
is consistent with an input of new nutrients from
below, but which does not appear in the chlorophyll
concentrations measured every 6 mo on the Ryofu
Maru. Both data sources have weaknesses. The
SSCC monitoring does not measure what occurs
below the surface. A significant correlation exists
between SSCC and integrated chlorophyll on broad
data sets (Lorenzen 1970; Piatt and Herman 1983),
but oligotrophic ecosystems often show no relation-
ship or, sometimes, inverse relationships (Hayward
and Venrick 1982). The Ryofu Maru data at 137 °E
between 6°N and 9°N allow a look at this problem
(Fig. 4): the correlation between SSCC and in-
tegrated chlorophyll is significant at the 1% level.
The value r = 0.52 obtained with individual stations
increases to r = 0.70 when enlarging the spatial
scale (i.e., taking mean values between 6°N and 9°N
instead of individual stations); a further improve-
ment would probably be obtained by enlarging the
time scale, but appropriate time series do not exist
SSCC(mg m-3)
A-
.2-
0
— i »— ^ 1 1^ r- — -t ^
Integrated Chlor. (0-200m , mg.m-2)
100-.
50-
0-
—I r-^ 1 1 1 — ■
Depth of nutricline ( m )
100-
50-
0-
70
75
80
Figure 3.— Long-term evolution of lat. 6°N-9°N averaged parameters related
to the primary production (data from the RV Ryofu Maru cruises at long.
137°E, Anonymous 1972 to 1984). Upper and middle panels: the chlorophyll
concentrations primarily expressed in active chlorophyll a and pheophytin have
been converted into chlorophyll a equivalents (Dandonneau 1979). Lower panel:
the continuous line joins the depth of P04 = 0.35 /^moleL"1; open circles
represent the depths of N03 = 1 ^mole-L"1. Thickened marks on the horizon-
tal axis indicate the low sea level episodes in the western tropical Pacific.
692
DANDONNEAU: MONITORING SEA SURFACE CHLOROPHYLL CONCENTRATION
Integrated Chlorophyll (0- 200m)
: (mg.m~z)
^S •
♦
100-
• ♦*•* ~.i*r
n = 128
r = .52
50-
.•V n=26
r =.70
0-
1 1 1
— i 1
.10
.20 .30 .40
.50
5SCC(mg.m-3)
Figure 4.— Integrated chlorophyll (0-200 m)/SSCC relationship between
lat. 6°N and 9°N (data from the RV Ryofu Maru cruises at long. 137°E,
Anonymous 1972 to 1984). Points and continuous line: individual stations.
Crosses and dashed line: averaged values for each cruise.
in this region. We can thus conclude that SSCC is
a reasonable index of the chlorophyll content in the
photic layer. The weakness of the Ryofu Maru data
series is that only 4-6 stations within 3 d are avail-
able for each El Nino episode. This sampling pat-
tern can describe the vertical structure of the ocean,
but it is not helpful in large-scale studies based on
chlorophyll, in which the signal to noise ratio is very
low (Dandonneau and Gohin 1984).
Subtropical Zones
At the start of the 1982-83 El Nino (and a possi-
ble cause of it?) strong southerly winds were re-
corded east of Australia in June and July 1982
(Harrison and Cane 1984). In the Coral and Tasman
Seas, a chlorophyll enrichment occurs in austral
winter between 22 °S and higher latitudes (Dandon-
neau and Gohin 1984). This chlorophyll enrichment
can be seen in austral autumn and winter of 1982
(Fig. 1), while it only appears in winter in 1983.
Moreover, SSCC higher than 0.15 mg-m-3 spread
northward to lat. 20 °S in July-September 1982
around long. 160°E, but only to 24°S in July-Sep-
tember 1983 at the same longitude. The long and
intense SSCC winter increase in this area in 1982
may be the result of advection of richer water from
the south after the strong wind anomaly. In the
Northern Hemisphere, a zone with high SSCC
values is observed off North America during the fall
of 1982 (Fig. 1); this feature is especially noteworthy
since most regions of the Pacific (even those from
the same merchant ship voyage) show low SSCC
values. Like other El Ninos, the 1982-83 one re-
sulted in temperatures and sea levels higher than
normal along the California coast, and strong
westerly winds at about 30°N. One would not ex-
pect increased chlorophyll concentrations with
higher temperatures, and according to Chelton et
al. (1982), El Nino episodes are likely to diminish
advection of water from the north which generates
a higher biomass. However, our data points cor-
responding to the enriched zone were far offshore
(Fig. 1) and the thermal anomaly there did not great-
ly differ from zero. The high SSCC values off North
America during the fall of 1982 might then be
related to the severe wind conditions which pre-
vailed during this time, and probably induced ver-
tical mixing of deep nutrients.
A few more features which appear on Figure 1
would be worthy of discussion, but conclusion is
hindered by the lack of accordance with a poorly
known field of oceanic properties and by the risk
of sampling or instrumental errors in SSCC
measurements. For instance the shape of the area
with SSCC >0.15 rng-m-3 centered slightly south
of the Equator at 165°W in July- September 1982
(Fig. 1), while the upwelling was collapsing, is sur-
693
FISHERY BULLETIN: VOL. 84, NO. 3
prisingly similar to the shape of the maximum of
cloudiness in September 1982, derived from satellite
measurements of outgoing long wave radiation (Gill
and Rasmusson 1983). Similarity might be causal,
i.e., high SSCC values might result from a response
of the phytoplankton to attenuation of light by the
clouds, or from enhanced phytoplankton growth
caused by precipitation of dust and aerosols by the
rain (Menzel and Spaeth 1962). It may also result,
at least partly, from sampling artifacts.
The major features shown by this SSCC monitor-
ing experiment are in agreement with the large-
scale processes that affect the tropical Pacific dur-
ing El Nino episodes. The collapse of the equatorial
upwelling in October 1982 resulted in a nearly com-
plete disappearance of the chlorophyll-rich area
which is usually located across the Equator. A
moderate enrichment persisted, however, east of
long. 120°W. In the northwestern tropical Pacific,
the eastward drift of the warmwater pool was
followed by conditions which stimulated photosyn-
thesis: a shallower thermocline, and more light
penetrating to the nutrients gave rise to unusually
high chlorophyll concentrations west of 180° from
October 1982 to March 1983. In April-June 1983,
the equatorial upwelling in the eastern Pacific was
still reduced by the El Nino conditions, and the
enrichment in the northwestern tropical Pacific was
less intense; during this period, low chlorophyll con-
centrations prevailed over most of the tropical
Pacific.
ACKNOWLEDGMENTS
I would like to thank Henri Walico for the
thousands of chlorophyll measurements which are
the basis of the present work. I am indebted to the
captains and crews of the merchant ships who call
at Noumea for kindly and carefully sampling and
filtering at sea.
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695
ANATOMICAL TRAUMA TO SPONGE-CORAL REEF FISHES
CAPTURED BY TRAWLING AND ANGLING
S. Gordon Rogers,1 Hiram T. Langston,2 and
Timothy E. Targett3
ABSTRACT
External signs of trauma were examined in 15 sponge-coral reef fish species captured while trawling
and angling at 37 m depth. Internal evidence of trauma was noted for all species and quantified for a
sample of angling-caught black sea bass, Centropristis striata. Distinct differences were noted in the
types and frequencies of trauma experienced among species, and between gear types within species.
Black sea bass; red snappers, Lutjanus campechanus; short bigeyes, Pristigenys alta; and Mycteroperea
groupers exhibited high frequencies of oral protrusions. Planehead filefish, Monacanthus hispidus; orange
filefish, Aleuterus schoepfi; and blue angelfish, Holacanthus bermudensis, were particularly prone to cloacal
protrusions. External signs of trauma were few in vermilion snappers, Rhomboplites aurorubens; porgies
(Stemotomus chrysops, Calamus leucosteus, and Pagrus pagrus); tomtates, Haemulon aurolineatum; and
two trawl-caught serranids (Centropristis ocyurus and Diplectrum formosum). Angling produced oral
protrusions in black sea bass more frequently than trawling. Trawl-caught red snappers had a higher
stomach eversion frequency when brought to the surface more quickly. Angling-caught black sea bass
experienced high frequencies of tissue emphysema and swim-bladder rupture. These results should be
considered in studies of feeding biology, released-fish survivorship, and fishery management.
Anatomical trauma experienced by fishes during
capture is interesting from several standpoints. Mor-
tality of individuals caused by stress, tissue damage,
organ displacement, and resulting aberrant behavior
has been recognized primarily for its effects on the
survival of released fish in mark-and-recapture
studies (Ricker 1949; Parker et al. 1959, 1963; Got-
shall 1964; Beamish 1966; Moe 1966; Laird and Stott
1978; Pawson and Lockwood 1980; Fable 1980;
Grimes et al. 1983). Mortality of fishes released by
fishermen is an important consideration for stock
assessment and management (Black 1958; Pawson
and Lockwood 1980; Matheson and Huntsman
1984). Recent management plans for the U.S. Gulf
and South Atlantic snapper-grouper fisheries
(GOMFMC 1981; SAFMC 1983a, b) recommended
implementation of minimum sizes for several
species. The sizes in the South Atlantic were deter-
mined from yield-per-recruit (YPR) models incor-
porating assumed survival rates for undersized,
^kidaway Institute of Oceanography, University System of
Georgia, POB 13687, Savannah, GA 31416; present address:
Coastal Resources Division, Georgia Department of Natural
Resources, 1200 Glynn Avenue, Brunswick, GA 31523.
2Skidaway Institute of Oceanography, University System of
Georgia, POB 13687, Savannah, GA 31416.
3Skidaway Institute of Oceanography, University System of
Georgia, POB 13687, Savannah, GA 31416; present address:
University of Delaware, College of Marine Studies, Lewes, DE
19958.
released fishes (SAFMC 1983a). Size regulations
were predicted on survivorship of ^60%. Gulf YPR
models did not incorporate survival rates, effectively
assuming 100% survival.
Other workers have indicated difficulty in obtain-
ing specimens of snapper-grouper species for quan-
titative analyses of feeding biology from depths
which caused stomach eversion and loss of gut con-
tents (Stearns 1884; Adams and Kendall 1891;
Camber 1955; Mosely 1966; Moe 1969; Bradley and
Bryan 1975; Link 1980; Ross 1982). This is of par-
ticular concern for studies comparing food habits
across depth zones (Moseley 1966). Differences be-
tween fish species captured by identical gear at
similar depths and differences within species be-
tween gear types introduce additional variation.
This study addresses the types and frequencies of
anatomical trauma experienced by sponge-coral reef
fishes captured by angling and trawling at a single
depth. These data are discussed in relation to trophic
studies, future studies of trauma during capture,
survival following release, and management of
snapper-grouper fisheries.
METHODS
Fishes were caught by angling and trawling at a
low-relief (<1 m) sponge-coral reef 37 m deep on the
continental shelf 84 km east of Sapelo Island, GA
Manuscript accepted January 1986.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
697
FISHERY BULLETIN: VOL. 84, NO. 3
(lat. 31°26'N, long. 80°20'W; central South Atlan-
tic Bight). Angling gear was standard hand-operated
boat rods rigged with double-hooked terminal
tackle and baited with squid. Hook sizes were 3/0
to 5/0. Fishes were brought to the surface as quick-
ly as possible (about 1 m/s; somewhat slower for
large snappers and groupers). Trawling was con-
ducted from two vessels, each rigged for stern
trawling but with some differences in gear and
handling.
The trawl gear on the RV Georgia Bulldog was
a 25 m, 4-seam high-rise roller trawl with tongue.
Meshes were (stretched) 20 cm in the wings and
tongue, 10 cm in the belly and bag (2 cm liner), and
7.5 cm in an extension. Cables connecting the trawl
and doors produced a sweep of 31.1 m; the rise on
the tongue was 6.1 m (J. B. Rivers4). The rig had
a vertical haulback rate of 0.12-0.15 m/s.
The trawl gear on the RV Blue Fin was a modified
No. 36 Yankee flat roller trawl. Meshes were
(stretched) 5 cm in the wings and belly and 3.5 cm
in the bag (2 cm liner). The total sweep was 22.1
m and the rise at the center of the headrope was
3.7 m (Rivers fn. 4). The rig had a vertical haulback
rate of 0.1 m/s. Gear handling was otherwise
identical.
Tows were 20 min long. The fish catch was sorted
to species and the alimentary tracts samples re-
moved; or samples were placed in 20 L buckets with
ice-seawater mixture, frozen on board, and pro-
cessed in the laboratory. Data on anatomical trauma
were recorded during dissections. An angling catch
of 34 black sea bass, Centropristis striata, was put
on ice and dissected 2 days later for examination
of internal trauma. No samples were subjected to
the bin-type icing procedures common on commer-
cial snapper-grouper vessels. Fishes were collected
from July through December in 1983 and in Sep-
tember 1984.
External evidence of trauma consisted of several
types of protrusion of the gastrointestinal tract.
These were classified as
1) Oral eversion - stomach everted into the
pharynx and often present in the mouth, pull-
ing the pyloric area and the intestine with it.
2) Cloacal protrusion - intestine protruded from
the cloacal area. Initially such protrusions were
not classified further; however, detailed dissec-
tions showed that they were either
4J. B. Rivers, Marine Fisheries Specialist, University of Georgia
Fisheries Extension Station, POB Z, Brunswick, GA 31523, pers.
commun. October 1984.
a) Herniations - disruptions of the body wall
in the pericloacal area through which the
gut protruded or
b) Intussusceptions - actual eversion of the
terminal portion of the intestine through its
own lumen.
3) Branchial protrusions - portions of the gut pro-
truded through the branchial opening.
Results are expressed as occurrences and percent-
age frequencies. Frequencies of herniations and in-
tussusceptions were calculated by dividing the
observed number in a class by the total number of
classified cloacal protrusions, then multiplying the
result by the total proportion of cloacal protrusions.
Example (from Table 1): planehead filefish herni-
ations, (99/(99 + 22)) (160/440) = 0.30.
Internal evidence of trauma included 1) the pres-
ence of gas in the tissues (tissue emphysema) and
2) rupture of the swim bladder. Although notes on
both phenomena were kept for all fish species, their
frequencies were enumerated only for the 34 care-
fully examined, angling-caught black sea bass.
Among-species and between-gear comparisons of
trauma were performed by using Pearson's test for
goodness of fit (yielding a x2 value). The null
hypotheses were specified as homogenous (equal)
proportions of specimens exhibiting a particular
symptom, based on the overall proportion of fish
with the symptom across species or gears (signifi-
cant departures were P < 0.05).
RESULTS
Dissection records of 1928 trawl-caught and 235
angling-caught fishes of 15 species were collated for
external evidence of trauma (Table 1). Seven species
were not caught with angling gear. Scamp, Myctero-
perca phenax, and gag, M. microlepis, were com-
bined to form a Mycteroperca grouper category due
to low numbers collected.
Trawl-caught red snappers, Lutjanus campecha-
nus; Mycteroperca groupers; short bigeyes, Pristi-
genys alta; planehead filefish, Monacathus hispidus;
orange filefish, Aleuterus schoepfi; and blue angel-
fish, Holacanthus bermudensis, experienced fre-
quent gut displacements (Table 1). These were oral
eversions in red snappers, short bigeyes, and Myc-
teroperca groupers; cloacal protrusions in orange
filefish and blue angelfish; and all three categories
(including branchial protrusion) in planehead filefish.
Alimentary tract displacements were minimal in
trawl-caught black sea bass; bank sea bass, Centro-
pristis ocyurus; sand perch, Diplectrumformosum;
698
ROGERS ET AL.: ANATOMICAL TRAUMA TO SPONGE-CORAL REEF FISHES
Table 1 .—Numbers and percentage frequencies (in parentheses; a = 1 %) of alimentary tract displacements in sponge-coral reef fishes
collected by trawling (T) and angling (A) in 37 m depth. Dashes (— ) indicate no data. Within cloacal protrusions, H = herniations, I =
intussusceptions, U = unclassified, and TC = total cloacal. N = number of specimens examined.
Oral
eversions
Cloacal protrusions
Branchial
Total
Species
H
I
u
TC
L^ 1 Ul Iwl IIUI
protrusions
displacements
N
black sea bass
T
4(2)
0
0
0
0
0
4(2)
200
Centropristis striata
A
45(27)
0
0
0
0
0
45(27)
169
red snapper
T
26(55)
0
0
0
0
0
26(55)
47
Lutjanus campechanus
A
1(50)
0
0
0
0
0
1(50)
2
bank sea bass
T
0
0
0
0
0
0
0
39
Centropristis ocyurus
A
1(33)
0
0
0
0
0
1(33)
3
short bigeye
T
8(22)
0
0
0
0
0
8(22)
37
Pristigenys alta
A
—
—
—
—
—
—
—
0
sand perch
T
0
0
0
0
0
0
0
19
Diplectrum formosum
A
2(18)
0
0
0
0
0
0
11
Mycteroperca groupers
T
5(29)
0
0
0
0
0
5(29)
17
A
0
0
0
0
0
0
0
1
planehead filefish
T
3(1)
99(30)
22(7)
39
160(36)
14(3)
177(40)
440
Monacanthus hispidus
A
—
—
—
—
—
—
—
0
orange filefish
T
0
1(4)
4(17)
7
12(21)
0
12(21)
58
Aleuterus schoepfi
A
—
—
—
—
—
—
—
0
blue angelfish
T
0
4(30)
1(8)
4
9(38)
0
9(38)
24
Holacanthus bermudensis
A
—
—
—
—
—
—
—
0
vermilion snapper
T
0
0
0
0
0
0
0
339
Rhomoboplites aurorubens
A
0
0
0
1
1(4)
0
1(4)
28
whitebone porgy
T
0
1(3)
1(3)
0
2(6)
0
2(6)
33
Calamus leucosteus
A
—
—
—
—
—
—
—
0
scup
T
0
1(1)
0
2
3(1)
0
3(1)
286
Stenotomus chrysops
A
—
—
—
—
—
—
—
0
tomtate
T
0
0
0
2
2(a)
0
2(a)
372
Haemulon aurolineatum
A
—
—
—
—
—
—
—
0
red porgy
T
0
0
1(6)
0
1(6)
1(6)
2(12)
17
Pagrus pagrus
A
0
0
0
0
0
0
0
21
tomtate, Haemulon aurolineatum; scup5, Stenoto-
mus chrysops; whitebone porgies, Calamus leucos-
teur; red porgies, Pagrus pagrus; and vermilion
snappers, Rhomboplites aurorubens.
Angling-caught black sea bass had high frequen-
cies of oral eversion. Angling-caught red porgies and
vermilion snappers exhibited few or no protrusions.
Angling data for all other species are too sparse to
estimate protrusion frequencies.
There was a significant lack of homogeneity in the
frequencies of oral eversions between species within
trawl (x2 = 695, df = 13, P « 0.01) and angling-
caught (x2 = 14.2, df = 6, P < 0.05) samples. The
trawling value resulted from high frequencies for
red snapper, Mycteroperca groupers, and short
bigeye; these three categories accounted for 95%
5The taxonomic status of this species is unclear (B. Roumillat,
South Carolina Marine Resources Research Institute, POB 12559,
Charleston, SC, 29412 pers. commun.) and is properly listed as scup
(Stenotomus chrysops (Robins et al. 1980; SAFMC 1983a, b))
although several authors have recently used the nomen southern
porgy (S. aculeatus (Miller and Richards 1980; Wenner 1983;
Sedberry and Van Dolah 1984)). Still others have classified South
Atlantic-caught Stenotomus as longspine porgy (S. caprinus
(Chester et al. 1984)).
of the x2 statistic. Among angling-caught fishes, a
high value for black sea bass and low values for red
porgy and vermilion snapper accounted for 91% of
the x2 statistic.
The high frequencies of cloacal protrusions in
trawl-caught planehead filefish, orange filefish, and
blue angelfish (21-38%) and low values in all other
species (<7%) produced a highly significant depar-
ture from homogeneity (x2 = 470, df = 13, P «
0.001). Seven of the 15 fish species did not display
the symptom (Table 1). Only one of the angling-
caught specimens (a vermilion snapper) experienced
cloacal protrusion. Of those cloacal protrusions
classified for blue angelfish and the two filefish
species, all herniations (Table 1) had fecal material
in the protruded gut portion.
Only planehead filefish experienced branchial pro-
trusions. Tomtate, vermilion snapper, scup, red
porgy, and whitebone porgy were notably free of
all forms of alimentary tract displacement.
Swim-bladder rupture was noted for all fish
species. Tissue emphysema was detected only in
black sea bass. Of the 34 black sea bass exam-
ined in detail for internal trauma, 33 (97%)
699
FISHERY BULLETIN: VOL. 84, NO. 3
exhibited swim-bladder rupture (1 specimen had 2
points of rupture), and 27 (79%) had tissue emphy-
sema.
Significantly more angling-caught black sea bass
had oral protrusions than those caught by trawling
(X2 = 138, df = 1, P « 0.001). For trawl-caught
red snappers, significantly more fish caught aboard
the Georgia Bulldog (26 of 39) had oral eversions
than those caught aboard the Blue Fin (0 of 8) (x2
= 5.34, df = 1, P < 0.025). No other comparisons
for combinations of symptoms, species, and gear
types yielded significant results. However, all oral
eversions noted for Mycteroperca groupers were
produced by Georgia Bulldog trawling gear, and
those noted for sand perch were produced by
angling gear.
DISCUSSION
Differences Due to Species and Gear
Differences between fish species (captured by
identical gear) in the type and frequency of gut
displacement are likely due to differences in bone
structure and relative swim-bladder volume. Except
for planehead filefish, which exhibited all forms of
external evidence, those species which experienced
frequent oral eversions did not present cloacal ever-
sions and vice versa (Table 1; refer also to the anal-
yses of categorized data). In this study the leather-
jackets (Balistidae) and angelfishes (Holacanthidae)
experienced high frequencies of gut displacements
toward the cloacal area. These taxa have a relatively
restricted pharyngeal area and the leatherjackets
have a bony sternum which further defines a "path
of least resistance" toward the cloaca. Other fishes
which may be similarly susceptible to cloacal pro-
trusions include other balistids, acanthurids, chae-
todontids, and scarids.
Larger mouthed species such as lutjanids (Stearns
1884; Adams and Kendall 1891; Camber 1955;
Moseley 1966; Bradley and Bryan 1975; this study),
serranids (Moe 1969; Link 1980; Matheson and
Huntsman 1984; this study), priacanthids (this
study), and scorpaenids (Gotshall 1964) experience
oral eversion more frequently than cloacal protru-
sion. Fishes with medium-sized mouths and "non-
directing" body morphologies (e.g., vermilion snap-
per, tomtate, and sparids in this study) exhibit
neither type of gut protrusion, instead having a
general swelling of the body cavity.
The relative volume of the swim bladder varies
from 0 to 6% of total body volume in marine fishes
(Jones 1957). Although measurements were not
made, the patterns of protrusion in this and other
studies (above) suggest that species-specific differ-
ences in swim-bladder volume result in varying
degrees of internal pressure on ascent. This may
contribute to differences in gut protrusion and the
extent of body cavity swelling.
It is not clear why varying rates of ascent would
induce varying frequencies of gut protrusion within
a fish species. Differences between fish species in
the rates at which gases can be resorbed from the
swim bladder likely had little effect on patterns of
protrusion. Achievement of equilibrium through
resorption requires time on the order of hours
(Brown 1939; Jones 1951). This is a longer time-scale
than the normal vertical movements of most fishes
(Steen 1970) and vertical displacements while trawl-
ing and angling. Also, the absolute magnitude of
swim-bladder expansion is independent of the rate
of ascent and should not be considered a factor. Yet,
a pattern is apparent in the higher values for angling
versus trawl-caught black sea bass and also for red
snappers caught with Georgia Bulldog versus Blue
Fin trawling gear. Mosely (1966) reported higher
oral eversion frequencies for red snappers taken by
angling versus those taken while trawling at inter-
mediate shelf depths (42-60 m). Bradley and Bryan
(1975) also noted for red snappers that angling pro-
duced more stomach eversions than trawling, but
stated that their data were confounded by differ-
ences in the average depths of fishing efforts. Addi-
tionally, stomach eversion frequencies for our trawl-
caught red snappers (83% taken with "rapid ascent"
Georgia Bulldog gear) were 7.5-9.5 times higher
than those reported in the literature from similar
depths (Fig. 1A; Moseley 1966; Bradley and Bryan
1975). It is tempting to attribute these results to dif-
ferences in vertical haulback rates. The rate of swim-
bladder expansion, linked directly to changes in
hydrostasis (Steen 1970) and therefore qualitative-
ly more or less "violent", may govern the nature
and extent of injuries.
An additional factor contributing potentially to the
types and frequencies of gut protrusion is the con-
sistency, amount, and position of prey material in
the alimentary tract. Firm material may function
as a bonelike directing structure or be what an ex-
panding swim bladder acts upon. It is interesting
that all of the herniated intestines in planehead file-
fish, blue angel fish, and orange filefish contain fecal
material. If hydrostatic forces within a fish's body
cavity are influenced by gut contents, unequal and
variable allocation of sampling effort and catch over
a diel feeding cycle could alter estimates of protru-
sion frequency for a given fish species. The major-
700
ROGERS ET AL.: ANATOMICAL TRAUMA TO SPONGE-CORAL REEF FISHES
A
60
50
a. 40
c 30-
oj
O 20^
10
0
Trawl Caught
i i i i i i 1 1 1 1
0 10 20 30 40 50 60 70 80 90 100
e.
Ul
S
100
90
80
70
60
C 50
£ 40
30
20
10-
o-
Angling Caught
i i i i i i i 1 1 1
0 10 20 30 40 50 60 70 80 90 100
Bottom Depth (m)
Figure 1.— Plots of the proportions of red snappers with everted
stomachs (PE) captured by (A) trawling and (B) angling as a func-
tion of bottom depth (data from Camber 1955; Moseley 1966;
Bradley and Bryan 1975; except this study). Ordinates were arc-
sine transformed (Snedecor and Cochran 1980). Abscissas are
plotted as actual depths or midpoints of ranges. The dashed line
(plot ^4) is the least-squares line including data from this study.
The only significant relationship was for trawl-caught fishes from
the literature (r = 0.90, df = 5, P < 0.01).
ity of orange filefish were collected during periods
of the day when there was very little material in the
alimentary tract, which is likely responsible for her-
niation/intussesception rates at variance with plane-
head filefish and blue angelfish values. Sampling of
other species was more equitably distributed over
the 24-h period.
Considerations for Feeding Studies
Negligible biases in stomach and intestinal con-
tents are expected among trawl-caught black sea
bass, bank sea bass, tomtate, the three porgy
species, sand perch, and vermilion snapper at depths
of 37 m. Angling-caught red porgies and vermilion
snappers should be equally free of bias-producing
gut displacements at these depths. However, cau-
tion is necessary in analyses of stomach contents for
trawl-caught red snappers, Mycteroperca groupers,
short bigeyes, and angling-caught black sea bass
from 37 m. Stomach content data for angling-caught
red snappers, groupers, bank sea bass, and sand
perch should also be interpreted with attention to
the likelihood of bias. These considerations have
been previously acknowledged for angling-caught
black sea bass and bank sea bass (Link 1980), trawl
and angling-caught red snappers (Stearns 1884;
Adams and Kendall 1891; Camber 1955; Moseley
1966; Bradley and Bryan 1975), angling-caught red
groupers, Epinephelus morio (Moe 1969), and
angling and longline-caught blueline tilefish, Caulo-
latilus microps (Ross 1982), from southeastern U.S.
shelf and slope waters. Moseley (1966) and Link
(1980) both stated that partial or full stomach ever-
sion renders quantification of consumed prey
suspect, particularly with respect to across-depth
comparisons (e.g., Godfriaux 1974). Studies of food
habits of fishes in the South Atlantic and Gulf of
Mexico shelf snapper-grouper complex have either
not discussed depth as a diet-determining variable
(Camber 1955; Moseley 1966; Moe 1969; Bradley
and Bryan 1975; Dixon 1975; Henwood et al. 1978;
Ross 1982; Steimle and Ogren 1982) or if depth was
considered, dealt with fishes not prone to stomach-
eversion bias (Manooch 1977; Grimes 1979; Sed-
berry 1985).
Species and gear-specific considerations should
also be made for analyses of daily feeding chron-
ologies and rations based on stomach content
weights. Fishes with partially or completely everted
stomachs should be eliminated from the data set.
It is clear that trawl-caught specimens of most
species are more suited to such analyses than those
caught with angling gear. However, some species
cannot be efficiently collected with trawling gear at
certain times of day, over certain types of bottom,
or indeed at all. Extra angling effort (offsetting
eversion rates) and well-designed multigear ap-
proaches (including traps and longlines) can be used
to complete data sets for such fishes.
Displacements of the posterior portion of the
alimentary tract can also have significant effects on
studies of feeding biology. Trawl-caught planehead
filefish, blue angelfish, and orange filefish are sub-
ject to such bias. Prey position data used to examine
the rate of movement and evacuation of material
through the gut (e.g., Klumpp and Nichols 1983) will
be affected by both herniations and intussusceptions.
During herniation, fecal material is either shifted
into the protruded portion of the intestine or the
701
FISHERY BULLETIN: VOL. 84, NO. 3
material already present in that segment is isolated
from what might otherwise be a continuous column
of material. Both potentially produce gaps or
"clumping" of intestinal contents. Collection of data
affected by intestinal displacements should also in-
corporate increased sampling so that specimens with
herniations or intussusceptions can be eliminated
from the data set without a significant loss of
information.
Survivorship: Experimental Design
and Fishery Management
Our data show that experimental studies of sur-
vivorship and the physiological responses of sponge-
coral reef fishes following capture and release should
stratify their designs by gear. Traps and longlines
should be considered in future studies because of the
gear-specific vertical haulback rates and other stress
factors. Additional considerations are capture depth
(Gotshall 1964; Moe 1966, 1969; Moseley 1966;
Bradley and Bryan 1975; Grimes et al. 1983), preda-
tion on injured and disoriented fishes (Parker et al.
1959, 1963; Randall 1960; Topp 1963; Gotshall 1964;
Fable 1980), crowding and abrasion in the gear
(Pawson and Lockwood 1980), degree of gut full-
ness (related to stress from diverted blood supply;
Beamish 1966), physiological state related to long-
term feeding/activity cycles (Parker et al. 1959),
water column temperature structure, currents, and
turbidity. Many of the factors covary with depth and
fluctuate seasonally.
The anatomical derangements investigated in the
present study are severe trauma. Oral and cloacal
protrusions would very likely cause high rates of
mortality in subsequently released fishes. Obstruc-
tion of the gastrointestinal tract would normally be
serious and interference with the blood supply to the
gastric and intestinal walls would lead to severe cir-
culatory impairment. Gotshall (1964) has shown that
returns from tagged blue rockfish, Sebastes mys-
tinus requiring stomach replacement and swim-
bladder deflation were less than half those from fish
requiring only swim-bladder deflation. These fish en-
dured everted stomachs for only a few minutes.
Topp (1963) has noted that the everted stomachs of
Lutjanus snappers are frequently perforated by the
fish's teeth. The effects of such injuries on survival
require further study.
Expansion of the swim bladder in specimens which
do not experience gut protrusions likely induces in-
ternal damage undetected by external examination.
Aquarists commonly use swim-bladder deflation
techniques to increase survivorship of specimens suf-
fering from decompression symptoms (D. Miller6).
Gotshall (1964) increased tag returns of blue rock-
fish by deflating expanded swim bladders of speci-
mens collected as deep as 90 m. The technique also
reduces the effects of exopthalmia (protruding eyes
produced by expansion of gas into the cranial region)
on blue rockfish (Gotshall 1964), vermilion snapper,
big eye (Priacanthus arenatus), and short bigeye (D.
Miller fn. 6).
Although tissue emphysema per se may not be
lethal, swim-bladder rupture probably is for some
species. Jones (1949) reported 90% mortality of 600
perches, Percafluviatilis, with swim bladders rup-
tured while being raised rapidly from 13.7 m. Topp
(1963) speculated that survivorship of sponge-coral
reef fishes with ruptured swim bladders is very low.
However, R. O. Parker7 has observed healing of rup-
tured swim bladders in black sea bass. Further ex-
perimentation is needed to determine the effects of
swim-bladder rupture on a species-specific basis.
It is likely that survivorship following release
varies with depth due to hydrostatic factors alone.
Regression of trawl-caught red snapper stomach
eversion proportions on capture depth (values from
the literature) explains 80% of the variance in the
observed data (Fig. L4; r = 0.90, df = 5, P < 0.01).
Inclusion of our trawl-caught red snapper data
rendered the relationship nonsignificant (Fig. L4;
r = 0.70, df = 6, P < 0.05). A similar plot of angling-
caught red snapper data from the literature was not
significant (Fig. IB; r = 0.58; df = 5; 0.10 < P <
0.05), possibly because of the differences in the sizes
of red snappers hooked with respect to depth (see
Figure 1 citations) and resultant differences in the
rates of ascent, or ontogenetic differences in relative
swim-bladder volume. Note that increased depth
eventually outweighs any real effect of the size of
the fish and tenacity of its struggle against the
angling gear, or anatomical variation, rendering the
overall relationship positive albeit nonlinear. The
above data (Fig. LA, B) also indicate that red snap-
pers caught with any gear over bottoms <30 m deep
do not suffer significant trauma. Similarly, depths
< 20 m introduced no difficulties to a food habits
study of this species (Moseley 1966).
Clearly, regulations which diminish removal of
fishes (e.g., gear/method restrictions, area/time
closures) will be more effective over a larger depth
6D. M. Miller, Curator, University of Georgia Marine Education
Center, POB 13687, Savannah, GA 31416, pers. commun.
November 1984.
7R. O. Parker, National Marine Fisheries Service, Southeast
Fisheries Center, Beaufort Laboratory, POB 500, Beaufort, NC
28516, pers. commun. October 1984.
702
ROGERS ET AL.: ANATOMICAL TRAUMA TO SPONGE-CORAL REEF FISHES
range than release measures. Current management
of the southeastern U.S. snapper-grouper fisheries
guarantees subjection of protected size classes to
stress and trauma. However, it is conceivable that
swim-bladder deflation techniques could improve the
effectiveness of current regulations.
The data we have presented show that the effects
of capture on sponge-coral reef fishes vary between
species and gears. These are important considera-
tions for studies of feeding biology. Additional data
on fish species survivorship following releases,
stratified by gear and depth, will allow fine-tuning
of present snapper-grouper management policies.
ACKNOWLEDGMENTS
Special thanks go to the captains and crews of the
RV Blue Fin, RV Georgia Bulldog, and FV Sanc-
tuary. Trawl doors for the RV Blue Fin were loaned
by S. Drummond, Southeast Fisheries Center Pas-
cagoula Laboratory, National Marine Fisheries Ser-
vice. D. Wyanski, B. Wells, C. Haney, T. Chestnut,
D. Miller, P. Schlein, B. Goggins, J. Rivers, M. Har-
ris, J. Hightower, and a host of volunteers assisted
in the field. D. Wyanski, B. Wells, A. Acevedo, and
L. Creasman assisted in the laboratory. The figure
was drafted by A. Boyette. The manuscript was im-
proved with comments from G. Helfman, S. Larson,
and two anonymous reviewers; it was typed by L.
Wainright and W. Roberts. The research benefited
from discussions with R. Parker, C. Haney, D.
Miller, P. Van Veld, and L. Wall. This work was sup-
ported by NOAA Sea Grants to T. E. Targett and
M. V. Rawson (NA80AA-D-00091 collectively) and
by operating funds at Skidaway Institute of Ocean-
ography.
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1974. South Atlantic Bight reef fish communities as repre-
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1975. Evidence for mesopelagic feeding by the vermilion
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Fable, W. A. Jr.
1980. Tagging studies of the red snapper (Lutjanus cam-
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GOTSHALL, D. W.
1964. Increasing tagged rockfish (genus Sebastodes) survival
by deflating the swim bladder. Calif. Fish Game 50:253-
260.
Grimes, C. B.
1979. Diet and feeding ecology of the vermilion snapper,
Rhomboplites aurorubens (Cuvier) from North Carolina and
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Grimes, C. B., S. C. Turner, and K. W. Able.
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1978. Feeding habits and food of the longspined porgy, Steno-
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1949. The teleostean swimbladder and vertical migration.
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1951. The swimbladder and the vertical movements of teleo-
stean fishes. I. Physical factors. J. Exp. Biol. 28:553-566.
1957. The swimbladder. In M. E. Brown (editor), The
physiology of fishes. II. Behavior, p. 305-322. Acad. Press,
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Klumpp, D. W., and P. D. Nichols.
1983. Nutrition of the southern sea garfish Hyporhamphus
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Laird, L. M., and B. Stott.
1978. Marking and tagging. In T. Bagenal (editor), Methods
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Blackwell Sci. Publ., Oxf.
Link, G. W., Jr.
1980. Age, growth, reproduction, feeding, and ecological
observations on the three species of Centropristis (Pisces:
Serranidae) in North Carolina waters. Ph.D. Thesis, Univ.
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1977. Foods of the red porgy, Pagrus pagrus, Linnaeus
(Pisces: Sparidae), from North Carolina and South Carolina.
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FISHERY BULLETIN: VOL. 84, NO. 3
speckled hind and snowy grouper from the United States
South Atlantic Bight. Trans. Am. Fish. Soc. 113:607-616.
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determining distributions in the South Atlantic Bight. Proc.
Ann. Gulf Caribb. Fish. Inst. 32:114-130.
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1966. Tagging fishes in Florida offshore waters. Fla. Board
Conserv., Div. Southwest Fish. Tech. Ser. 49, 40 p.
1969. Biology of the red grouper Epinephelus morio (Valen-
ciennes) from the eastern Gulf of Mexico. Fla. State Board
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1966. Biology of the red snapper, Lutjanus aya Bloch, of the
northwestern Gulf of Mexico. Publ. Inst. Mar. Sci., Univ.
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Parker, R. R., E. C. Black, and P. A. Larkin.
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(Oncorhynchus). J. Fish. Res. Board Can. 16:429-448.
1963. Some aspects of fish-marking mortality. In Northwest
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probable cause. Rapp. P. -v. Reun. Cons. int. Explor. Mer
177:439-443.
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1960. The case of the free-loading barracuda. Sea Front.
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1949. Effects of removal of fins upon the growth and sur-
vival of spiny-rayed fishes. J. Wild]. Manage. 13:29-40.
Robins, C. R., R. M. Bailey, C. E. Bond, J. R. Brooker, E. A.
Lachner, R. N. Lea, and W. B. Scott.
1980. A list of common and scientific names of fishes from
the United States and Canada. Am. Fish. Soc. Spec. Pub.
12, 174 p.
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1982. Feeding habits of the gray tilefish, Caulolatilus
microps (Goode and Bean, 1878), from North Carolina and
South Carolina waters. Bull. Mar. Sci. 32:448-454.
SAFMC (South Atlantic Fishery Management Council).
1983a. Source document for the snapper-grouper fishery of
the South Atlantic region. SAFMC, Charleston, SC.
1983b. Fishery management plan, regulatory impact review,
and final environmental impact statement for the snapper-
grouper fishery of the South Atlantic region. SAFMC,
Charleston, SC.
Sedberry, G. R.
1985. Food and feeding of the tomtate, Haemulon aur'o-
lineatum (Pisces, Haemulidae), in the South Atlantic Bight.
Fish. Bull., U.S. 73:461-466.
Sedberry, G. R., and R. F. Van Dolah.
1984. Demersal fish assemblages associated with hard bot-
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Stearns, S.
1884. On the position and character of the fishing grounds
of the Gulf of Mexico. Bull. U.S. Fish. Comm. 4:289-290.
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1970. The swim bladder as a hydrostatic organ. In W. S.
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The nervous system, circulation, and respiration, p. 413-443.
Acad. Press, N.Y.
Steimle, F. W., Jr., and L. Ogren.
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44(6-7):49-52.
Topp, R.
1963. The tagging of fishes in Florida 1962 program. Fla.
Board Conserv., Mar. Lab. Prof. Pap. Ser. 5, 76 p.
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704
ANNUAL PRODUCTION OF EVISCERATED BODY WEIGHT, FAT, AND
GONADS BY PACIFIC HERRING, CLUPEA HARENGUS PALLASI,
NEAR AUKE BAY, SOUTHEASTERN ALASKA
Jay C. Quast1
ABSTRACT
Pacific herring, Clupea harengus pallasi, grow according to the constant-proportion growth model, which
requires that yearly growth in body length be a constant proportion of growth during the previous year.
Herring have one or two growth stanzas (periods of constant-proportional growth) in the eastern Pacific
Ocean and eastern Bering Sea, and grow faster in the eastern Bering Sea than in the northeastern Pacific
Ocean.
With growth, total and eviscerated body weights of fresh Auke Bay herring bear an exponential
relationship to body length (BL) that is slightly greater than cubic, and evisceration does not lower variabili-
ty in length-weight relationships. With growth, an increasing part of the annual product (growth plus
gonads) is partitioned into gonads so that in the largest fish most of the annual product is gonads. The
annual product is constantly proportional to BL through ages 2-6 and also through ages 9-12, but the
proportion is considerably smaller in the 9- to 12-yr-old fish. The two differing proportions may indicate
that young and old Auke Bay herring occupy slightly different feeding niches and that the trophic en-
vironment in the Auke Bay vicinity may not support the older fish as well as the younger.
Pacific herring spawn in April or May in the Auke Bay vicinity, as zooplankton density rapidly in-
creases to its peak in June. The time of spawning seems optimal for rapid building of fat reserves and
feeding of newly hatched larvae.
Pacific herring, Clupea harengus pallasi, range off
western North America, from the Chukchi Sea to
San Diego, CA, and have been commercially ex-
ploited over the entire range (Rounsefell 1930;
McLean and Delaney 1978; Spratt 1981). Pacific
herring usually occupy extensive reaches of coast,
from tens to hundreds of miles, and populations are
particularly dense around the Alexander Archi-
pelago of southeastern Alaska and the archipelago
off British Columbia (from charts or fisheries maps
in Rounsefell 1930, McLean and Delaney 1978, and
Spratt 1981). Yet, even where dense, populations
can be locally distinctive in vertebral number and
spawning time (Rounsefell and Dahlgren 1935;
Hourston 1980).
Pacific herring have been commercially harvested
in Alaska since the late 1800's (Rounsefell 1930),
principally for reduction to meal and oil. Herring
were also pickled, starting in 1900, but the industry
never became large and declined in the 1920's. A
fishery for Pacific halibut, Hippoglossus stenolepis,
bait had a similar rise and decline. The reduction
Northwest and Alaska Fisheries Center Auke Bay Laboratory,
National Marine Fisheries Service, NOAA, P.O. Box 210155, Auke
Bay, AK 99821; present address: 1565 Jamestown Street S.E.,
Salem, OR 97302.
Manuscript accepted December 1985.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
fishery ended in the 1960's, and the principal fishery
for Pacific herring in Alaska now is sac roe, which
is exported to Japan.
The biology of Pacific herring in Alaska has not
been thoroughly described. The study by Rounse-
fell (1930) is the most comprehensive work, and
Rounsefell and Dahlgren (1935) separated stocks in
southeastern Alaska on the basis of vertebral counts.
Skud (1963) analyzed tag returns, and Carlson
(1980) described the ecology of Auke Bay herring.
Reid (1971) summarized some biological character-
istics of herring taken for the reduction fishery from
1929 to 1966.
Because Pacific herring are economically and
ecologically important in southeastern Alaska and
there is little information on the growth, produc-
tivity, and life history of this species in this region,
I undertook a 1-yr study of a population in the Auke
Bay vicinity (Auke Bay is about 16 km northwest
of Juneau). Goals of the study were to compare
growth of Pacific herring in the Auke Bay vicinity
with growth of Pacific herring from other locales
in the eastern Pacific Ocean and relate annual pro-
duction of fat, gonads, and eviscerated weight in the
Auke Bay herring to the annual cycle of food supply.
Pacific herring of the Auke Bay vicinity are one
of the innermost and northernmost populations in
705
FISHERY BULLETIN: VOL. 84, NO. 3
the Alexander Archipelago (Auke Bay is about 80
nmi [148 km] by water from the open coast).
Although this population may contain more than one
spawning stock, it will be identified with Auke Bay
in the present study (local populations spawn with-
in weeks of each other and within a few nautical
miles).
METHODS
Auke Bay herring were sampled several times
monthly from April 1973 to March 1974; however,
no fish were taken in February 1974. The fish were
captured principally by jigging with bright hooks or
hooks wrapped with colored yarn. Samples were also
taken during spring 1973 from nearby locales in
southeastern Alaska, including Hood Bay (off
Chatham Strait, southwest of Juneau), Carroll In-
let (near Ketchikan), and Katlian Bay (near Sitka),
and also from the eastern Bering Sea west of
Nunivak Island.
Auke Bay herring were usually examined fresh
but sometimes were frozen and examined within 1
wk. Lengths were originally measured as standard
lengths (SL, tip of upper jaw to end of hypural
bones) but were later converted to body length (BL,
tip of lower jaw to end of hypural bones) by multi-
plying SL by 1.0132, the average ratio in 126
specimens from Auke Bay.
Body lengths were back-calculated from scales
taken from above the pectoral fins and posterior to
the opercular flap. The calculations followed the pro-
portional method of Whitney and Carlander (1956),
which should reduce the variation in BL-scale size
relationships because the method adjusts for possi-
ble differences in scale length in the same-sized fish.
This method requires that the regression between
BL and scale length be linear, which was satisfied
(Fig. 1). The intercept of the regression (55 mm) was
somewhat higher than the median BL (36.5 mm) for
first squamation of 16 preserved specimens;
however, the differences between estimates for BL
at first squamation are probably important only for
fish younger than 1 yr. The regression fit the data
well for herring >1 yr old (Fig. 1). I also attempted
to reduce variability in the back-calculations for the
Auke Bay fish by averaging focus-to-annulus
distances from left and right sides of the scales (an-
nuli were as well defined at the sides as in the
centerline of the scale), but only a centerline
measurement was used in samples from other
geographic regions.
After the growth data were analyzed by Walford
graphs (Walford 1946), linear regressions (Walford
regressions) were fit by least squares to adult sec-
tions of constant parameters (stanzas) that were
indicated on the graphs. Both the Walford regres-
sion and von Bertalanffy formulation are variants
of the constant-proportion growth model, which
requires that growth in one year be a constant pro-
portion of growth the preceding year (Ricker 1975).
(The slope of a Walford regression equals the von
Bertalanffy e~K, and the intercept equals L (1 -
e~K).)
Annual changes in development of fat and gonads
were evaluated by indices that were derived from
total body weights, eviscerated body weights, and
gonad weights. I estimated unbound water in the
eviscerated body tissues and gonads as the percent-
age weight lost by drying 1 cm wide transverse body
sections and entire gonads in a drying oven for more
than 4 d at 27° C, a period that yielded weight stabil-
ity. Visual estimates of visceral fat used a four-point
scale (from none to heavy), and visual estimates of
maturity used a seven-point scale, as follows (Roman
numerals in brackets refer to a similar scale
developed by Hay and Outram (1981) for Pacific
herring): 1) Newly regenerating [VIII], 2) regen-
erating [III], 3) nearly mature [IV], 4) ripe [V], 5)
ripe and running [VI], 6) partially spawned [VII],
and 7) spawned out [VII]. Fresh body, eviscerated,
and gonad weights were regressed on body lengths
by least squares after logarithmic transformation
of variates. Statistical tests were significant when
P < 0.05.
Scales of Pacific herring from southeastern Alaska
and the eastern Bering Sea probably have two an-
nuli in the first growth year. When the annulus
nearest to the scale focus of Auke Bay herring was
used for back-calculations, the BL's were much
smaller (average of 65 mm) for the first winter than
the BL's of juvenile herring (at least 80 mm) cap-
tured at the end of their first year in Auke Bay by
Jones (1978). Pacific herring in British Columbia at-
tain a length of at least 80 mm by their first Sep-
tember (Hourston 1958). Furthermore, when the
first annulus was used as the first year mark, Wal-
ford graphs of the growth data were erratic and
differed markedly from graphs of the same type of
data in the literature. When the second annulus was
used as the first year mark, the graphs were sim-
ple and corresponded to graphs of similar data from
the literature.
There was no indication of Lee's phenomenon
(slower growth in longer lived individuals) in the
back-calculated BL's, but there was evidence of a
changing relation between growth back-calculated
for ages 1 and 2 and the span of years that was used
706
QUAST: BODY WEIGHT, FAT, AND GONADS OF PACIFIC HERRING
250
200 —
x
r-
O
z
UJ
_l
>
a
o
150
100 —
BL
N
54.855 + 0.6309 S
= 234, R = 0.84
OL^J I I I I I I I I I I I I I I I I I I I I L
100
200 300 400
PROJECTED SCALE SIZE (S) IN MM
500
Figure 1.— Relationship between body length (BL) and projected scale size (S) of Pacific herring from Auke
Bay, AK.
in the back-calculations. When the estimates of
growth to ages 1 and 2 were compared for all
specimens, those from herring aged 2-4 at time of
capture (back-calculated over a span of 0-2 yr) had
slower-than-average growth, and those herring aged
4-7 (back-calculated over a span of 3-5 yr) had faster-
than-average growth (Fig. 2). Estimates for the
oldest herring (back-calculated over a span of >6 yr),
however, gave mixed results. The trends in fish of
5 yr and younger may have been caused by en-
vironmental influences because the trends occur in
sets of years (fish aged 2-4, when captured, spent
their first or second growth years in 1970-72, and
those aged 4-7 spent their first or second growth
years principally in 1966-69).
GROWTH
The average size-at-age data in my samples of
Pacific herring from the eastern Pacific and east-
ern Bering Sea and data from the literature for
those regions usually formed two stanzas on Wal-
ford graphs and inflected at ages 2 or 3 (see Figure
3 for examples). The data for Norwegian and Mur-
man stocks of Atlantic herring, Clupea harengus
harengus, (Svetovidov 1952) also formed two stan-
zas and intersected at age 2. Although the stanzas
for all of my back-calculated data from the eastern
Pacific Ocean intersected at age 2, stanzas for two
populations from California (data from Spratt 1981)
intersected at age 3, and a plot of Naumenko's
707
FISHERY BULLETIN: VOL. 84, NO. 3
10
<
a:
<
LU
>
OS
O
LL
z
<
LU
o
OH
Z
o
<
>
G
LU
(J
<
H
Z
LU
u
LU
a:
c
(+)5-
0 -
(-)5-
10 -
-
•
t * .
A
A A
A
A
• A
• •
•
•
A
~
A
A BACK CALCULATED TO 1ST YR.
MARK
•
• BACK CALCULATED TO 2ND YR.
MARK
i
i
1 1 1 1 1 1 1
i
_L
2 3 4 5 6 7
NO. ANNULI BACK-CALCULATED
10
Figure 2.— Relationship between extent of back-calculation from scales and the body length estimated
at 1 and 2 yr in Pacific herring from Auke Bay, AK. Points indicate the deviation of size estimates for
age-1 and age-2 Pacific herring from the average for all annuli (the second annulus was taken as the first
year's mark).
(1979) data from the eastern Bering Sea had only
one stanza. Regardless of the data source, linear
regressions (Walford regressions) closely fit the data
in the growth stanzas (Tables 1, 2).
The method of aging Pacific herring can influence
estimates of growth. In the data that I examined
for this study, adult stanzas based on back-calculated
lengths usually had lower slopes than adult stanzas
based on terminal-lengths-at age (Table 1). Further-
more, the plots of back-calculated data inflected
either at 2 yr or not at all, in contrast to plots of
lengths-at-terminal-age, which inflected at 3 yr in
three of six examples (Table 1). Important factors,
however, remain uncontrolled in this comparison.
For instance, the lengths-at-terminal-age from the
literature were based on summer sampling; hence,
they include additional growth after annulus
formation. The lengths-at-terminal-age were from
populations near or on the open coast, which may
grow faster than populations from protected and
possibly less productive waters within the Alex-
ander Archipelago. Furthermore, it is not clear
that the Alaskan data for lengths-at-terminal-age
used the second scale annulus as the first year's
mark.
Walford graphs for Pacific herring from Tomales
Bay, CA (data from Spratt 1981), and the eastern
Bering Sea (this study) indicated that juvenile
growth success and age at inflection (intersection
of juvenile and adult stanzas) are more important
determinants of adult size at age than either length
at year 1 or the slope of the adult stanza, the adult
growth proportion (Table 1; Fig. 3). The data in-
dicate that herring from the Bering Sea quickly
outgrow those from Tomales Bay although the BL's
of the two groups were almost identical at ages 1
708
QUAST: BODY WEIGHT, FAT, AND GONADS OF PACIFIC HERRING
Table 1 .—Growth characteristics and growth parameters of Pacific herring from the northeastern Pacific Ocean
and eastern Bering Sea, based on data from the present study and from the literature. Growth is portrayed by
the Walford version of the constant-proportion growth model (see text). Because Reid's (1971) data were gathered
from a summer fishery, body lengths are longer than they were at the time of annulus formation and may not
be comparable to back-calculated data or to lengths-at-terminal-age collected on or near the time of annulus
formation. The inflections column refers to the junction of juvenile stanzas with stanzas for adults. Juvenile stanzas
on the Walford graphs were fit by eye to sizes at ages 1 and 2, or ages 1-3; adult stanzas were fit by least squares.
Size at
age 1
Inflec-
tion
Adult stanza
Aging
Capture location
(mm)
at year
Intercept
Slope
R2
method
Source
Back-calculated lengths:
Auke Bay vicinity
93.3
2
64.89
0.709
0.998
scales
this study
Hood Bay, Chatham Strait
90.8
2
66.31
0.664
0.995
scales
this study
Katlian Bay
101.5
2
81.50
0.659
0.991
scales
this study
Carroll Inlet
102.7
2
83.61
0.632
0.999
scales
this study
Eastern Bering Sea
112.8
2
79.26
0.727
0.993
scales
this study
Eastern Bering Sea
90.3
?1
88.79
0.722
0.999
scales
Naumenko 1979
Lengths-at-terminal-age:
Auke Bay vicinity
—
2
64.94
0.716
0.983
scales
Blankenbeckler 19792
Prince William Sound, AK
131.4
3
40.60
0.859
0.985
scales
Reid 1971
Kodiak vicinity, AK
132.1
2 +
55.99
0.792
0.990
scales
Reid 1971
Southeastern Alaska
145.1
2 +
52.14
0.788
0.967
scales
Reid 1971
San Francisco, CA
113
3
44.87
0.816
0.989
otoliths
Spratt 1981
Tomales Bay, CA
113
3
36.95
0.871
0.996
otoliths
Spratt 1981
No inflection apparent.
2Blankenbeckler, D. 1978. Age, growth, maturation, and parasite occurrence of Pacific herring (Clupea pallasi) from
southeastern Alaska, 1974 through 1976. Alaska Dep. Fish Game, Tech. Data Rep. 39, 88 p.
and 2, and the adult stanza was steeper for herring
from Tomales Bay. The Bering Sea herring, how-
ever, inflected to a steeper slope at age 2 rather than
age 3. Environment may not determine the time
of inflection in Pacific herring because juveniles
both from the Bering Sea and Tomales Bay had
similar BL's during the first 2 yr (Fig. 3) although
the environments of the locales probably differ
greatly.
Weight-Length Relationships
Total weight (W, grams) relates to BL (milli-
meters) in fresh Pacific herring from the Auke Bay
vicinity as W = (4.4467 x 10"6)BL3-2232 (N = 491;
R2 = 0.97). The lower confidence limit for the ex-
ponent exceeds 3.0, and the exponent exceeds 3.0
in reports for herring in most locales; e.g., Pacific
herring from Tomales Bay, 2.93 (Spratt 1981); San
Francisco Bay, 3.23 (Spratt 1981); the east coast of
Vancouver Island, 3.26 (Hart et al. 1940), and
Barkley Sound, British Columbia, 3.46 (Hart et al.
1940); and in Atlantic herring, 3.15 and 3.5 (Hart
et al. 1940). Many differences between exponents,
as cited, may not be biologically significant because
weight-length relationships vary seasonally and be-
tween sexes, even in eviscerated fish. The exponent
for the relationship between BL and total weight
probably exceeds 3.0 in healthy herring populations
because, as noted in later paragraphs, both eviscer-
ated and gonad fresh weights also have exponents
>3.0 when related to BL.
Eviscerated weight of Auke Bay herring also had
an exponential relationship to BL that significantly
exceeded 3.0 [(W = 5.0894 x 10"6)BL3 16640; Fig.
4]. In theory, evisceration avoids large potential
weight variations caused by seasonal changes in
gonads and fat deposits about the viscera, and vari-
able food content; yet, eviscerated weight (Sy ■ x =
0.1030) was at least as variable a function of BL as
total weight (Sy -x = 0.0953) in the same specimens,
and both total weight and eviscerated weight had
the same coefficient of determination (0.97). The
lack of decreased variability in the weight of evis-
cerated herring, as a function of BL, compared with
whole fish is evidence that building of visceral fat
and gonads does not simply add weight, but rather
that some compensatory mechanism may act be-
tween these apparent weight sources and the evis-
cerated body.
In contrast to the results of Hart et al. (1940),
Hickling (1940) found markedly low exponents, 2.13
and 2.37, for the relationship between eviscerated
weight and BL for Atlantic herring from the North
Sea, values that are strikingly lower than those ex-
pected for fishes in general. For example, Quast
(1968) gave exponents of 2.7-4.5 for 32 species of
marine fishes in southeastern California, including
3.9 for the northern anchovy, Engraulis mordax.
Hickling' s exponents may be too low because the
709
FISHERY BULLETIN: VOL. 84, NO. 3
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710
QUAST: BODY WEIGHT, FAT, AND GONADS OF PACIFIC HERRING
• AUKE BAY, BACK-CALCULATED (THIS STUDY)
*" * TOM ALES BAY, CALIF., TERMINAL LENGTHS (SPRATT 1981)
0 ° BERING SEA, BACK-CALCULATED (THIS STUDY)
A * BERING SEA, BACK-CALCULATED (NAUMENKO 1979)
50
100
BL.
150
(MM)
200
250
Figure 3.— Examples of Walford trends in body length of Pacific herring from widely separated locales in the eastern Pacific Ocean
and Bering Sea. Heavy solid line through origin is the line of zero growth, and numbered points indicate ages in years. Adult stanzas
were fit by least squares, and the juvenile stanzas were fit by eye. Data from Naumenko (1979) represent 25 yr of collections.
effective range of BL's was limited (near 50 mm)
in his data sets and his data were grouped in 10 mm
size classes. (In contrast, BL's extended over about
130 mm in the Auke Bay herring, and lengths were
taken to 1 mm.)
In Pacific herring, the relationship between evis-
cerated weight and BL varies with season and sex
(Fig. 5), and the relationship for Atlantic herring
should vary similarly. Although Hickling (1940) con-
cluded that regressions of eviscerated weight on BL
differed by sex in Atlantic herring (W = 0.0661
BL2
312
in
males, and W = 1.1471 BL1-456
in
females), his samples probably were too restricted
seasonally to estimate reliably the relationship be-
tween eviscerated weight and BL for all seasons.
Because of seasonal variation in fat content of the
musculature (discussed in the next section), data for
a single season cannot represent an average over
all seasons in Pacific or Atlantic herring of either
sex.
711
FISHERY BULLETIN: VOL. 84, NO. 3
5. 175
— 4.425
r-
X
u
Q
LU
H 3.675
<
LU
U
in
>
LU
5 2.925
2.175
Y = -12. 18836 + 3. 16640 X
N = 491
_L
l
J L
J L
4.600
4.800
5.000 5.200
LN BODY LENGTH (X)
5.400
Figure 4.— Relationship between body length and eviscerated body weight in fresh Pacific herring in the vicinity of
Auke Bay, AK, sexes combined. Variates transformed to their natural logarithms (LN). Points represent 1-9 specimens.
Seasonal Cycles in Fat and Gonads
Adult Pacific herring feed chiefly on zooplankton
and small fishes (Hart 1973). In the Auke Bay vicin-
ity, zooplankton peak in abundance in June or July
and are virtually absent from November to March
(Fig. 6; fig. 3 in Carlson 1980). In an unpublished
study of Auke Bay herring, stomachs were mostly
empty during late fall and winter (R. E. Haight,
cited in Carlson 1980).
Pacific herring spawn in Auke Bay in late April
or May but may spawn as late as 4 June (Wing2).
Eggs hatch 14-20 d after spawning, based on incu-
bation temperatures for herring in British Colum-
bia (Outram 19653) and temperatures for mid-
April and May in Auke Bay, which are similar to
2B. L. Wing, Northwest and Alaska Fisheries Center Auke Bay
Laboratory, National Marine Fisheries Service, NOAA, P.O. Box
210155, Auke Bay, AK 99821, pers. commun. November 1981.
3Outram, D. N. 1965. Canada's Pacific herring. Dep. Fish.
Can., Ottawa, Fish. Res. Board Can., Biol. Stn., Nanaimo, B.C.,
23 p.
those for British Columbia (Wing4). The time of
spawning seems optimal to allow spawned fish and
their newly hatched larvae to feed during the
heaviest zooplankton concentrations of the year
(Fig. 6).
Because the peak in zooplankton abundance is
relatively brief, the period immediately after spawn-
ing is critical for fattening of adults and for growth
and survival of newly hatched larvae. Feeding and
fattening of all life stages of Auke Bay herring may
also be aided by the submarine illumination afforded
by the longest days and highest levels of light, early
in the summer.
Fat accumulated about the viscera during the
period of maximum zooplankton abundance and
reached highest indices shortly afterward, about
mid-July (Fig. 6). It then declined rapidly but slightly
differently in each sex. There is evidence, also, based
4B. L. Wing, Northwest and Alaska Fisheries Center Auke Bay
Laboratory, National Marine Fisheries Service, NOAA, P.O. Box
210155, Auke Bay, AK 99821, pers. commun. July 1983.
712
QUAST: BODY WEIGHT, FAT, AND GONADS OF PACIFIC HERRING
JAN I FEB I MAR ■ APR H MAY I JUN ' JUL ' AUG ' SEP ' OCT1 NOV ' DEC
Figure 5.— Seasonal variation in eviscerated weight as shown by monthly samples of fresh Pacific herring near Auke
Bay, AK, given as percentage departure from the weight predicted by the general eviscerated weight/BL regression
for these fish (see Figure 4). The percentage departure is given relative to its yearly average to highlight seasonal
changes. Data fit by eye.
on the water content of the musculature, that intra-
muscular fat varied seasonally and paralleled the
development of visceral fat— water content of evis-
cerated body sections for the sexes behaved in an
opposite fashion to visceral fat, being highest in
April-May and at low levels between June and Octo-
ber (Table 3). In contrast to the water content of
the musculature, eviscerated weight increased
relative to BL after May (Fig. 5). If the increase in
eviscerated weight were caused by increased
somatic hydration, variation in hydration would
have paralleled variation in eviscerated weight, but
instead, the values for hydration decreased after
May. Some other factor must be responsible for the
increased eviscerated weights after May, and a like-
ly candidate is fat, because eviscerated weight in-
creased over the same period that visceral fat was
building. Hart et al. (1940) also described an ap-
parent reciprocal relationship between water and
oil content in Pacific herring from British Colum-
bia, and Love (1970) discussed the same relation-
Table 3.— Average hydration of musculature as
a percentage of wet weight, by month in Pacific
herring from Auke Bay, AK.
Males
Females
Month
N
Percent
N
Percent
January
15
69.2
6
68.4
March
17
71.1
19
71.0
April
26
75.3
25
76.0
May
29
77.0
29
76.0
June
8
61.7
12
66.5
July
8
60.8
12
61.5
August
10
60.7
10
61.1
September
23
61.7
30
62.7
October
12
61.9
18
61.5
November
1
62.6
6
60.6
December
3
65.0
25
63.1
ship in Atlantic herring and other fish species with
fatty tissues.
The timing of gonad development, as indicated by
seasonal development of gonads, differed in the
sexes in Pacific herring from Auke Bay. Males were
713
FISHERY BULLETIN: VOL. 84. NO. 3
' JAN ' FEB ' MAR ' APR ' MAY ' JUN ' JUL ' AUG1 SEP ' OCT ' NOV1 DEC
Figure 6.— Three annual cycles that relate to the condition of Pacific herring in the vicinity of
Auke Bay, AK: A visual index of visceral fat (see text); gonad indices based on (wet) gonad weights
as a percentage of the eviscerated (wet) body weights that would be expected at various BL's (see
Figure 4); and an annual cycle of zooplankton density, from displacement volumes for 1962-64 given
in Wing and Reid (1972). Points based on less than five specimens are enclosed in parentheses.
Curves fit by eye.
714
QUAST: BODY WEIGHT, FAT, AND GONADS OF PACIFIC HERRING
nearly ready to spawn in November but females
delayed readiness until perhaps 4 mo later (Fig. 6),
a delay that was confirmed by visual judgments of
maturity, see table below (sample size in paren-
theses):
Percentage of herring judged ripe
Sept. Oct. Nov.- Jan. Mar.
Males
Females
4(23)
0(31)
92(12)
11(18)
95(19)
79(38)
94(18)
90(20)
These data differ in some important respects from
those of Hay and Outram (1981) for Pacific herring
in British Columbia. Their gonadosomatic index has
sharper peaks in maturity of gonads and different
timing of the peaks than the Pacific herring from
Auke Bay. For example, in their data, testes were
only developing (a low gonadosomatic index) in Oc-
tober (the fish spawned in late February and early
March), but testes were near maximum fullness
(high index values) in October in herring from Auke
Bay (Fig. 6). However, Hay and Outram used total
weight in their index. If total weight is used for the
index, the divisor will include a considerable weight
of fat about the viscera in the fall and negligible
weight in the spring, with the result that even if
gonad weights remain the same from November to
February, the decline in the amount of fat would
cause the index to increase. In my study of the
Pacific herring in Auke Bay, I divided gonad
weight by eviscerated body weight, which should
avoid an appreciable error in the gonadosomatic
index that would be caused by variation in visceral
fat.
Within each sex, seasonal profiles for gonad in-
dices are nearly opposite the profiles for indices of
visceral fat (Fig. 6). The annual cycles in fat and
gonad indices (Fig. 6) in Pacific herring from Auke
Bay resemble those noted by Blaxter and Holliday
(1963) for spring spawning in Atlantic herring: "In
winter-spring herring the good feeding conditions
in late spring and early summer (after spawning)
build up the fat reserves. With development of the
gonads in late autumn feeding stops and spawning
in December-March means that the fish overwinter
and spawn with fat reserves considerably lower than
the autumn spawners." Visceral fat in male Auke
Bay herring is lowest in winter (perhaps as early
as November), but in females does not reach lowest
values until April. Correspondingly, the testes build
rapidly in late summer and fall and appear to be
heaviest by October or shortly after, but the ovaries
are not at their heaviest until shortly before spawn-
ing, in April or May. Hydration is not responsible
for sexual differences in development of gonad
weight from January to March because, as the
following table indicates, hydration remains virtual-
ly constant from November to March in both sexes
(Table 4).
Table 4. — Average hydration of gonads, as a
percentage of wet weight, by month in Pacific
herring from Auke Bay. AK.
Males
Females
Month
N
Percent
N
Percent
January
14
76.2
5
73.6
March
16
76.1
17
71.3
April
39
82.6
33
84.5
May
24
83.7
24
77.2
June
6
75.5
9
77.7
July
18
73.6
19
76.2
August
25
77.9
21
80.7
September
19
77.6
25
78.6
October
12
76.9
18
74.5
November
1
76.1
6
72.7
December
3
74.2
25
71.2
This seasonal, mirror imagery between develop-
ment of fat and gonads, with the images differing
for sexes, is evidence for a strong physiological
coupling between fat depots and gonads. Fat depots
enable Pacific herring to accommodate two critical
cycles in their life history that are badly out of phase:
The zooplankton cycle, with its brief, summer peak
that builds fat depots rapidly and is followed by low
levels of food abundance from October to March; and
the gonad cycle that slowly removes fat from the
depots with the slow building of testes from July
through October and the slower building of ovaries
from July through March.
Are the seasonal cycles of gonad maturity in
Pacific herring from Auke Bay determined by gene-
tics or are the gonads responding principally to
cyclical changes in the immediate environment? lies
(1984) felt that Atlantic herring are remarkably in-
dependent of their environment. Genetic control of
gonad maturity seems likely except for spawning,
which appears to respond to local temperatures
(Outram 1965, see footnote 3). Gonads must build
well in advance of spawning, and spawning dates
vary from November in the southern limits of the
eastern Pacific range (Spratt 1981) to June in Auke
Bay. Female Auke Bay herring mature sexually and
use fat deposits later in the fall than do males and
thus anticipate a later spawning date. Male herring
in the eastern Pacific Ocean, in contrast, appear to
build testes early enough to spawn at any date be-
715
FISHERY BULLETIN: VOL. 84, NO. 3
tween November and June. Only the ovarian cycle
seems to correspond closely to the local environmen-
tal conditions that seem optimal for larval growth
and survival. Possibly, the genes that are respon-
sible for local adaptation of spawning stocks are sex
linked for females and are selected through larval
survival.
Annual Production of Eviscerated
Weight and Reproductive Tissues
Although Pacific herring usually have only one
major spawning per site in the Auke Bay vicinity,
there may be a succession of lesser spawnings each
spring. Unspawned fish are rarely seen as late as
July (author's observations and comments by salmon
fishermen who jig herring for bait). Although Wing
(see footnote 2) recorded spawnings in Auke Bay
between 24 and 29 April 1973, herring must spawn
for at least 2 mo in Auke Bay because some fish
sampled in 1973 were partially spawned or ripe and
running in May and June (Fig. 7). Presumably, local
conditions influence the number of eggs deposited
on any date.
The relationship between fecundity, as indicated
by mature ovarian weight, and BL was greater than
cubic, in agreement with data on other clupeiod
species (Blaxter and Hunter 1982). Samples of Auke
Bay herring had an exponent of 3.94 (Fig. 8), within
the range (3.07-4.50) for Atlantic herring as given
by Paulson and Smith (1977), from the literature.
These authors gave an exponent of 3.32 for Pacific
herring they sampled in Prince William Sound.
Perhaps, the exponent for fecundity would have
been higher for the herring Paulson and Smith
sampled in Prince William Sound had their collec-
tions included smaller fish (their smallest were near
180 mm long, but fish as small as 130 mm were
available in samples from Auke Bay). The exponent
for testicular weight was considerably higher than
that for ovarian weight in Auke Bay herring (Fig.
8); however, the difference may not be real because
the confidence limits for the two exponents over-
lapped considerably.
The scatter in the plots of gonad and testes
weights on BL for Auke Bay herring (Fig. 8) and
for Pacific herring from Prince William Sound (fig.
1 in Paulson and Smith 1977) indicate that some of
the herring may have been partially spawned when
they were collected (fully spawned fish were not
used in my data). If samples for fecundity are taken
in the spawning season, there is the risk that some
PERCENTAGE IN STAGE:
1-10
11-50
51-100
0
0
0
1
10
8
1
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0
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7
39
: 1 7:
.Ian
Fph
Mar
Anr
Ma v
ini
Can
Or-t
Mnu
r\ar-
MATURITY STAGE:
1. IMMATURE
2. SPAWNED OUT AND
REGENERATING
3. REGENERATING
U. MATURING
5. RIPE
6. PARTIALLY SPAWNED
OR RIPE AND RUNNING
7. SPAWNED OUT
N = 21 0 38 80 59 20 55 80 54 30 7 29
Figure 7.— Maturity of Pacific herring near Auke Bay, AK, by month (sexes combined). Numbers in boxes are percent-
ages of herring that were visually classified into maturity stages on examination. Total fish by month are given
in the bottom line. Data for February were extrapolated from January and March.
716
QUAST: BODY WEIGHT, FAT, AND GONADS OF PACIFIC HERRING
fish will have spawned partially and that fecundity
estimates will be too low.
When the relationships between BL, weight, and
fecundity in Pacific herring from Auke Bay were
used in a model of annual changes in gonad weight
and eviscerated weight, production of eviscerated
weight decreased rapidly with age or size (Table 5,
col. 3). Gonad production (Table 5, col. 4), in con-
trast, increased yearly but appeared to approach an
asymptote at about 31-34 g in the oldest fish. With
age, more of the annual product (annual increment
in eviscerated weight plus gonad weight) was par-
3.525
2.775
2.025
1.275
h-
x
2 0.525
LU
a
< 4.125
z
o
u
3.375
LN CONW =~ 20.44468+ 4.41971 (LN BL)
MALES
N = 63
i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — r
2.625
1.875
1 .125
LN CONW =- 17.78385 + 3.93569 (LN BL)
FEMALES
N = 61
' I ' ' ' I
1 ' I
J L
_L
I
J L
4.875 5.025 5.175
LN BL (MM)
5.325
5.475
Figure 8.— Relationships between (wet) gonad weight (GONW) and BL in fresh Pacific her-
ring collected from March to May 1973 near Auke Bay, AK (variates transformed by natural
logarithms (LN). Data (not shown) that formed a separate cluster of points near the abscissa
for each sex probably represented spawned fish and were not used in the regressions. Points
represent 1-2 specimens.
717
FISHERY BULLETIN: VOL. 84, NO. 3
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titioned into gonads, which by age 12 composed
nearly all of the annual production (Table 5, col. 8).
As the herring grew, the annual product was more
closely related to BL than to eviscerated body
weight (Table 5, cols. 6, 7), evidence that individual
herring in the Alike Bay vicinity may use food more
in proportion to their BL than their weight. Further-
more, although the relationship between annual
product and BL was nearly constant within age
groups 3-6 and 8-12 (Table 5, col. 6), productivity
was much lower in the 8-12 group. Young Auke Bay
herring may be more successful for their size in find-
ing food than are older individuals, because impor-
tant foods needed by older herring may be scarce
in the Auke Bay vicinity, which is about 80 nmi (148
km) by water from the open ocean.
There is indirect evidence from the characteristics
of growth and production in Auke Bay herring and
growth characteristics of other Pacific herring in the
northeastern Pacific Ocean and Bering Sea that not
only growth but the annual product relative to her-
ring size and the partitioning of the annual product
may vary with the population. If the relationship
between eviscerated weight and BL in Auke Bay
herring is used with growth data of Pacific herring
from other locales in the eastern Pacific Ocean and
Bering Sea (Table 1), striking differences are visi-
ble in the annual product of eviscerated weight (Fig.
9). For example, if 190 mm herring (3-yr-olds) in the
Bering Sea produce gonads in the same proportion
to eviscerated weight as 190 mm herring in Auke
Bay (5-yr-olds; Table 5, col. 8), gonads and
eviscerated weight would each form about one-half
of the annual product of Bering Sea herring. How-
ever, this proportion would be much too high for
herring in Bering Sea during their first year of
gonad production, according to the model based on
Auke Bay herring, if Bering Sea herring mature as
2- or 3-yr-olds. If production of eviscerated weight
and gonads is scheduled according to age, rather
than proportion of annual product, similar conflicts
result; thus, Pacific herring from different regions
probably differ in characteristics for production of
eviscerated weight and gonads.
CONCLUSIONS
Pacific herring grow in the eastern Pacific Ocean
according to the constant-proportion model; i.e.,
growth in one year is a constant proportion of the
amount grown the previous year. Growth stanzas
(regions of constant growth parameters) for juve-
niles and adults usually inflect near age 2, and the
change in growth is probably related to sexual
718
QUAST: BODY WEIGHT, FAT, AND GONADS OF PACIFIC HERRING
50
40
3 |(a8.0) BERING SEA
(NAUMENKO)
4
30
G
LU
H
<
a:
LU
O
CO
>
1 20
<
10
SAN FRANC
J L_L
TOMALES BAY
100
150
BL (MM)
AT
200
ANNULUS
250
Figure 9.— Hypothetical growth in (fresh) eviscerated body weight by Pacific herring at locales in
the eastern Pacific Ocean and eastern Bering Sea. Data were based on relationships between eviscerated
body weight and BL in samples from the Auke Bay vicinity and data on growth reported in the literature
(see Table 1). Numbered points are ages at the beginning of annual growth increments. The dashed
vertical line is for comparative purposes and intersects the graphs at 190 mm BL. The second annulus
was taken as the first year mark in specimens from Auke Bay, Katlian Bay, and Bering Sea (this study).
maturity. Size of adults is influenced more by
growth rate of juveniles and the size at inflection
of growth stanzas than by the constant of propor-
tional growth after inflection.
In the Auke Bay vicinity, a sharp increase of zoo-
plankton abundance in June is the determinent for
the annual cycles of fattening and spawning in
Pacific herring, and spawning in April or May seems
optimally timed for growth of newly hatched fry.
In summer, fat builds rapidly about the viscera and
in the musculature of adults, as a reserve for gonad
development and metabolism in fall and winter when
food is scarce and herring do not feed. lies (1984)
found that in Atlantic herring fat is assimilated and
deposited almost unchanged during the feeding
cycle and is not utilized for metabolism until the
metabolic pool of protein is exhausted. He also
hypothesizes that annual somatic growth declines
719
FISHERY BULLETIN: VOL. 84, NO. 3
with gonad growth and ceases with depletion of the
protein pool.
Male Pacific herring from Auke Bay build gonads
and use their fat reserves more rapidly than do
females. Testes may be near spawning condition in
November, but ovaries are not full sized until April.
Males may be ready or nearly ready to spawn in
November over the entire eastern Pacific Ocean, but
females delay spawning until local conditions of
temperature and food abundance are optimal for
larval growth.
The exponents for total and eviscerated body
weights, as functions of BL, exceed 3.0 in Pacific
herring from Auke Bay, and probably in Atlantic
herring as well because of their similar morphology.
Weight of mature gonads also have a greater-than-
cubic relationship to BL in Auke Bay herring (the
exponent was 4.4 for testes; the exponent of 3.9 for
ovaries was within the range for ovaries in Atlan-
tic herring).
The annual product (eviscerated body weight and
gonad weight) is constantly proportional to BL
through ages 2-6 and also through ages 8-12 in
Pacific herring from Auke Bay, but the proportion
is considerably lower in the 8-12 group. However,
despite the two levels of production relative to BL,
annual production corresponds more closely to BL
than to eviscerated weight. Annual production may
be lower relative to BL in the older group because
suitable foods for adults may not be abundant in the
Auke Bay vicinity. Most annual production in young
Auke Bay herring goes into growth of eviscerated
body weight. After age 6, production of sex prod-
ucts predominates, and by age 12, sex products com-
pose over 90% of annual production.
Pacific herring probably develop genetic stocks
that are distinguished by locale, spawning time, and
cycles of gonad maturity and fat utilization in the
females. The stocks probably are distinguished also
by growth rate, age, or size at growth inflection and
by partitioning of annual product between eviscer-
ated body weight and gonads.
ACKNOWLEDGMENTS
I especially thank Elizabeth L. Hall, NMFS Auke
Bay Laboratory, for her exacting scale measure-
ments and painstaking preparation of specimens,
and H. Richard Carlson and Richard E. Haight, also
of the Auke Bay Laboratory, who obtained the her-
ring samples from the Auke Bay vicinity, sometimes
under severe weather conditions. My thanks to the
Alaska Department of Fish and Game for samples
from Carroll Inlet, Katlian Bay, and the eastern Ber-
ing Sea, and to Petersburg Fisheries, Inc., for the
opportunity to collect specimens from the herring
fishery at Hood Bay. Helpful reviews of the manu-
script were provided by H. Richard Carlson, Robert
R. Simpson, and Bruce L. Wing of the Auke Bay
Laboratory.
LITERATURE CITED
Blaxter, J. H. S., and F. G. T. Holliday.
1963. The behavior and physiology of herring and other
clupeids. In F. S. Russell (editor), Advances in marine
biology, Vol. 1, p. 261-393. Acad. Press, N.Y.
Blaxter, J. H. S., and J. R. Hunter.
1982. The biology of the clupeoid fishes. In J. H. S. Blax-
ter, F. S. Russell, and M. Young (editors), Advances in
marine biology, Vol. 20, p. 1-223. Acad. Press. N.Y.
Carlson, H. R.
1980. Seasonal distribution and environment of Pacific her-
ring near Auke Bay, Lynn Canal, southeastern Alaska.
Trans. Am. Fish. Soc. 109:71-78.
Hart, J. L.
1973. Pacific fishes of Canada. Fish. Res. Board Can. Bull.
180, 740 p.
Hart, J. L., A. L. Tester, D. Beall, and J. P. Tully.
1940. Proximate analysis of British Columbia herring in rela-
tion to season and condition factor. J. Fish. Res. Board Can.
4:478-490.
Hay, D. E., and D. N. Outram.
1981. Assessing and monitoring maturity and gonad develop-
ment in Pacific herring. Can. Tech. Rep. Fish. Aquat. Sci.
998, 31 p.
Hickling, C. F.
1940. The fecundity of the herring of the southern North Sea.
J. Mar. Biol. Assoc. U.K. 24:619-632.
HOURSTON, A. S.
1958. Population studies on juvenile herring in Barkley
Sound, British Columbia. J. Fish. Res. Board Can. 15:909-
960.
1980. Timing of herring spawnings in British Columbia, 1942-
1979. Can. Ind. Rep. Fish. Aquat. Sci. 118, 101 p.
Iles, T. D.
1984. Allocation of resources to gonad and soma in Atlantic
herring, Clupea harengus L. In G. W. Potts and R. J.
Wootton (editors), Fish Reproduction: Strategies and tac-
tics, p. 331-347. Acad. Press, N.Y.
Jones, J. D.
1978. Growth of larval Pacific herring in Auke Bay, Alaska,
in 1975 and 1976. M.S. Thesis, Univ. Alaska, Juneau, 23 p.
Love, R. M.
1970. The chemical biology of fishes. Acad. Press, NY., 547
P-
McLean, R. F., and K. J. Delaney.
1978. Alaska's fisheries atlas. Alaska, Dep. Fish Game, 2
vol., 81 p.
Naumenko, N. I.
1979. Features of growth of young eastern Bering Sea her-
ring, Clupea harengus pallasi. J. Ichthyol. 19(6):152-156.
Paulson, A. C, and R. L. Smith.
1977. Latitudinal variation of Pacific herring fecundity.
Trans. Am. Fish. Soc. 106:244-247.
Quast, J. C.
1968. Estimates of the populations and the standing crop of
720
QUAST: BODY WEIGHT, FAT, AND GONADS OF PACIFIC HERRING
fishes, pp. 57-79. In W. J. North and C. L. Hubbs (editors),
Utilization of kelp-bed resources in southern California, 264
p. Calif. Dep. Fish Game Fish Bull. 139.
Reid, G. M.
1971. Age composition, weight, length, and sex of herring,
Clupea pallasi, used for reduction in Alaska, 1929-66. U.S.
Dep. Commer., NOAA Tech. Rep. NMFS SSR-F 634, 25 p.
RiCKER, W. E.
1975. Computation and interpretation of biological statistics
of fish populations. Fish. Res. Board Can. Bull. 191, 382 p.
ROUNSEFELL, G. A.
1930. Contribution to the biology of the Pacific herring,
Clupea pallasi, and the condition of the fishery in Alaska.
Bull. U.S. Bur. Fish. 45:227-320.
ROUNSEFELL, G. A., AND E. N. DAHLGREN.
1935. Races of herring, Clupea pallasi, in southeastern
Alaska. Bull. U.S. Bur. Fish. 48:119-141.
Skud, B. E.
1963. Herring tagging experiments in southeastern Alaska.
U.S. Fish and Wild]. Serv. Fish. Bull. 63:19-32.
Spratt, J. E.
1981 . Status of the Pacific herring, Clupea harengus pallasi,
resource in California, 1972 to 1980. Calif. Dep. Fish Game
Bull. 171, 107 p.
Svetovidov, A. N.
1952. Clupeidae. InE. N..Pavlovskii and A. A. Shtakel'berg
(editors), Fauna of U.S.S.R., Fishes, Vol. 11, No. 1. Israel
Program for Scientific Translations (translated from Rus-
sian by Z. Krauthamer and E. Roifer), 428 p.
Walford, L. A.
1946. A new graphic method of describing the growth of
animals. Biol. Bull. 90(2):141-147.
Whitney, R. R., and K. D. Carlander.
1956. Interpretation of body-scale regression for computing
body length of fish. J. Wildl. Manage. 20:21-27.
Wing, B. L., and G. M. Reid.
1972. Surface zooplankton from Auke Bay and vicinity, south-
eastern Alaska, August 1962 to January 1964. U.S. Dep.
Commer., NOAA, NMFS Data Rep. 72, 764 p.
721
CONTRIBUTIONS TO THE
LIFE HISTORY OF BLACK SEA BASS, CENTROPRISTIS STRIATA,
OFF THE SOUTHEASTERN UNITED STATES1
Charles A. Wenner, William A. Roumillat, and C. Wayne Waltz2
ABSTRACT
Ages of black sea bass, Centropristis striata, from the South Atlantic Bight were determined from otoliths.
Analysis of marginal increments showed that annulus formation occurred in April and May. The von
Bertalanffy growth equation derived from back-calculated mean standard lengths at age was It = 341
(1 - e-0-2309(f+o.30io)^ wjjere £ js age jn years an(j \f _ standard length at age. The oldest fish was age
10.
Centropristis striata is a protogynous hermaphrodite that undergoes sex succession at ages 1 through
8. The process of sex succession is described from histological examination of the gonads. The major
spawning period is from March to May, and a minor spawn occurs in September-October. Mature males
and females were encountered at age 1. Fecundity estimates ranged from 17,000 in a 108 mm SL female
to 1,050,000 in a 438 mm SL fish, and were significantly related to length, weight, and age.
The instantaneous rate of total mortality of C. striata from catch curve analysis, ranged from 0.721
in 1978 to 1.320 in 1981 for commercial fish traps and 0.726 in 1979 to 1.430 in 1981 for hook-and-line
gear. Petersen mark-recapture techniques were used to determine the population size of C. striata on
two shallow-water patch reefs. Conversions of these estimates to densities gave 14-125 individuals per
hectare.
The black sea bass, Centropristis striata (Linnaeus),
is an important recreational and commercial ser-
ranid (Huntsman 1976; Musick and Mercer 1977;
Low 1981) that occurs along the east coast of the
United States from Massachusetts to Florida, with
occasional individuals as far south as the Florida
Keys (Fischer 1978). Within this range, C. striata
is thought to form two populations separated at
Cape Hatteras (Mercer 1978). The northern popula-
tion migrates seasonally from shallow waters along
the Middle Atlantic and southern New England
coasts during summer to deeper water in the south-
ern part of the Middle Atlantic Bight during the
winter (Musick and Mercer 1977). Black sea bass in
the Middle Atlantic Bight are harvested commer-
cially with traps in shallow water during summer
and with otter trawl gear when aggregated in
deeper water in winter (Frame and Pearce 1973).
Commercial catches are almost exclusively from
traps in that part of the South Atlantic Bight from
Cape Fear, NC to Cape Canaveral, FL where fish-
ing is largely confined to patch reefs (live bottom
habitat of Struhsaker 1969 or inshore sponge-coral
Contribution No. 205 from the South Carolina Marine Resources
Center, Marine Resources Research Institute.
2Marine Resources Research Institute, South Carolina Wildlife
and Marine Resources Department, P.O. Box 12559, Charleston,
SC 29412.
habitat of Powles and Barans 1980) at depths from
20 to 46 m. South Carolina commercial landings
were as high as 350.7 metric tons (t) in 1970, but
show large annual fluctuations (Fig. 1).
Both the northern and southern populations have
been aged by analyzing otoliths (Mercer 1978), with
nine age groups identified north of Cape Hatteras
and eight along the southeastern U.S. coast. How-
ever, sampling techniques could have biased the
findings on southern C. striata since fishes came
from commercial catches which are frequently culled
at sea (Mercer 1978).
Black sea bass are protogynous hermaphrodites
(Lavenda 1949), wherein most individuals function
first as a female and later as a male. Most females
mature by age 2; older age classes are composed
predominately of male fish although sexually active
males are in all age groups. Sexual succession oc-
curs at ages 1 through 5 (Mercer 1978). The north-
ern population spawns from June to October with
peak reproduction in July and August off Virginia
(Mercer 1978).
There is insufficient published information to
describe the life history of this valuable commercial
and recreational species in the South Atlantic Bight
in detail. This report describes aspects of the life
history of C. striata from the South Atlantic Bight,
including age and growth, sex ratios, size and age
Manuscript accepted October 1985.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
723
FISHERY BULLETIN: VOL. 84, NO. 3
300
c
o|2
c —
9 9
o e
w Z
il
< i
UJ
</5
2
O O
o "■
_l
<
o
200
100
— i — i — r
1950
"i — r
— i r
1955
— I r
1960
~\ 1
1965
1 T
— i r
1970
n 1 r
1975
n 1 — r — r
1980
YEAR
Figure 1.— Annual commercial landings of Centropristis striata in South Carolina.
at maturity and sexual succession, and fecundity.
Additional information includes Petersen mark-
recapture estimates of standing crop on reefs, and
trends in the size and age composition with in-
creased exploitation.
MATERIALS AND METHODS
Age and Growth
Most specimens were taken from the inshore
sponge-coral habitat between lat. 31.5° and 33.5°N
by commercial black sea bass traps (Rivers 1966),
Antillean-S traps (Powles and Barans 1980), hand-
lines, and trawl surveys from June 1978 through
September 1981. Supplemental specimens were
obtained from South Carolina commercial landings
and other research programs to determine season-
al gonadal condition and time of annulus forma-
tion.
Centropristis striata were weighed to the nearest
g and total (TL) and standard (SL) lengths were
recorded to the nearest mm. Sagittae were removed
and stored dry in envelopes for subsequent age
determination. Unless damaged, the left sagitta was
placed concave side up in a dish of water over a dark
field and viewed at 12 x magnification using a binoc-
ular microscope. When viewed with reflected light,
sagittae displayed a central opaque field surrounded
by alternating translucent and opaque bands. The
central field varied in size and shape from a small
opaque nucleus to a large opaque zone consisting of
one or more broken rings (Fig. 2A, B). Since ap-
parent daily growth rings have been observed on
both the sagitta and lapillus of C. striata (Johnson3),
this zone was interpreted by counting rings from
the primordium to the edge of the central field. Oto-
liths were finely ground on both sides until the cen-
tral area of apparent daily rings could be observed
(Fig. 3A, B). They were then viewed with trans-
mitted light on a compound microscope at 500 x
and/or 1,000 x magnification.
The intercept of the otolith radius-SL relationship
was used to derive mean back-calculated size at age
by the Fraser-Lee method (Poole 1961; Carlander
1982). The von Bertalanffy growth equation (Ber-
talanffy 1938) was fitted to mean back-calculated
SL at age using the SAS NLIN procedure (Helwig
and Council 1979) employing Marquardt's algorithm
and the SAS NLIN weight statement; mean back-
calculated lengths were weighted by the reciprocal
of the standard error of the mean squared. Both
standard least squares linear regression (Sokal
and Rohlf 1981) and geometric mean (GM) func-
tional regression analyses were used to describe
the relationship of length to length and length to
weight.
3G. David Johnson, Fish Division, U.S. National Museum,
Washington, D.C. 20560, pers. commun. April 1982.
724
WENNER ET AL.: LIFE HISTORY OF BLACK SEA BASS
\*m
A
w
t
B
Figure 2.— Photomicrograph (16 x ) of the left sagittae from young-of-the-year Centropristis striata. A) Otolith with a small central
nucleus (between arrows). B) Otolith with a large central zone consisting of a few broken rings (between arrows). Bars equal 1 mm.
725
FISHERY BULLETIN: VOL. 84, NO. 3
„
B
Figure 3.— Photomicrograph of sagittae from young-of-the-year Centropristis striata. A) Central primordium of the opaque
nucleus showing growth rings for fish #1, Table 2; 400 x magnification. B) Area of otolith near the edge of the central zone
showing growth rings of fish #8, Table 2; 250 x magnification.
726
WENNER ET AL.: LIFE HISTORY OF BLACK SEA BASS
Reproduction
Reproductive organs from 6,685 C. striata were
resected at sea and fixed in formol-alcohol solution
(Humason 1972) or 10% seawater Formalin4. After
2-6 wk fixation, the tissues were transferred to 50%
isopropanol, processed through an Auto-Technican
2A Tissue Processor, vacuum infiltrated, and
blocked in paraffin. Sections (7 ^m) were cut from
each gonad by a rotary microtome, stained with Har-
ris hematoxylin, and counter-stained with eosin-y.
Histological sections from 300 fishes were read by
two observers to develop agreement on sex and
maturity stages; the remaining sections were then
examined by a single observer. Sex and maturity
stages (Table 1) which provided an accurate and ob-
jective estimate of reproductive status were modi-
fied from Smith (1965), Hilge (1977), and Mercer
(1978) to determine size and age at first maturity,
spawning season, and sex composition. The stage
of gametogenesis and terminology used in gonadal
descriptions follow Smith (1965), Combs (1969),
Hyder (1969), Moe (1969), Mercer (1978), and
Wallace and Selman (1981).
We included as males not only individuals whose
gonads consisted entirely of testicular tissue but also
those with functional testicular tissue (as judged by
active spermatogenesis) as well as traces of inactive
ovarian tissue. Females were defined as either
having entirely ovarian gonads or inactive testicular
4Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Table 1. — Histological criteria used in determining gonadal con-
dition of black sea bass, Centropristis striata.
Gonad class
Testicular state
Ovarian state
Immature
Developing
Ripe
(running)
Spent
Resting
Transitional
Little or no spermatocyte
development.
A few primary and sec-
ondary spermatocytes
through lumina filled
with spermatozoa.
Predominance of sper-
matozoa, little active
spermatogenesis.
No spermatogenic activ-
ity, some residual sperm
present in tubules.
Some mitotic regenera-
tion of spermatogonia
and interstitial tissues.
Small (<100 /jm) baso-
philic oocytes.
Predominance of oo-
cytes with yolk vesicle
formation through late
vitellogenesis.
Late vitellogenesis and
presence of hydrated
oocytes.
Unspawned, mature
oocytes undergoing
atresia.
Predominance of small
basophilic oocytes with
residual traces of
atresia.
Inactive or regressing
ovarian tissue with con-
current testicular prolif-
eration.
tissue in a functional ovary. Transitional gonads in-
cluded only those with obviously proliferating tes-
ticular tissue within a nonactive, regressing ovary.
Simultaneous gonads were those combining equal-
ly developed male and female tissue. Immature
bisexual gonads were designated as simultaneous
juveniles to avoid any implication as to their func-
tion at maturity.
We successfully sexed 80-90% of the fish sampled
by histological examination every month but April.
More than 75% of those sampled in April were sexed
by gross examination of the gonads, and although
our determinations of the functional sexes of these
gonads were probably correct, the relative occur-
rence of transitional and simultaneous gonads in
April samples remains unclear. These data were
thus used only to complete the seasonal frequencies
of functional sexes.
Gonads from 115 maturing females collected dur-
ing April 1979 were removed at sea, split open with
a longitudinal incision, and placed in Gilson's solu-
tion (Bagenal 1967). Separated oocytes were washed
and stored in 70% isopropyl alcohol after digestion
of the ovarian tunic and connective tissue and then
were decanted into a separatory funnel and diluted
to 1 L for enumeration. Three to five 1 mL sub-
samples were removed from the suspension, which
was well mixed by continuous aeration through the
bottom of the funnel. Each subsample was trans-
ferred to a petri dish and counted at a magnifica-
tion of 10 x . Only ova >0.15 mm in diameter were
counted since histological examination of the gonads
of maturing and spent females showed only oocytes
>0.15 mm developed during the spawning season.
Total fecundity was estimated by expanding the
mean of the subsamples to the total sample volume.
Total fecundity was related to length and weight by
standard least squares linear regression (Sokol and
Rohlf 1981) and GM functional regression (Ricker
1973).
Mortality Estimates
Plots of logp frequency on age indicated that
black sea bass are fully recruited to commercial
traps and hook-and-line gear at age 4, so mortality
analysis applies to age 4 and older. The instanta-
neous rate of total mortality (Z) was estimated by
standard least squares regression (Sokol and Rohlf
1981) from the slope of the right descending limb
of the catch curve (Ricker 1975). Values of Z were
also obtained by converting (appendix I in Ricker
1975) rates of survival (S) derived by Heinke, and
Chapman and Robson estimates (Everhart and
727
FISHERY BULLETIN: VOL. 84, NO. 3
Youngs 1981). Not all fish collected were aged, so
fish of known age were grouped into 1 cm length
intervals by gear type for each survey to calculate
percentages of each age in each size interval. These
percentages were applied to the number of C. striata
in each length interval to estimate age composition
for the unaged fish (Ricker 1975).
Population Estimates at
Specific Reef Sites
Petersen mark-recapture experiments were con-
ducted at site 1 (lat. 32°30.3'N, long. 79°41.9'W;
depth = 20 m; area =160 ha) during the summer
of 1981 to estimate the population size of C. striata
on this reef. In the summers of 1982 and 1983, we
studied a second reef also (site 2: lat. 32°28.3'N,
long. 78°14.5'W; depth = 23 m; area = 120 ha).
These reef areas were defined by the presence of
attached algae and invertebrate growth (porifera,
corals, echinoderms, bryozoans, anthozoans, and
ascidians) as observed with a HYDRO products
TC-125-5DA low-light-level underwater television
camera during transects across the sites (for more
details, see Wenner 1983). Study areas were mapped
with an EPSCO C-Plot II LORAN-C plotter inter-
phased with a SITEX 707 LORAN-C receiver.
Black sea bass were captured and recaptured at
each site with commercial traps (Rivers 1966) and
Florida snapper traps (0.9 m wide x 1.2 m long x
0.6 m high) fished for 45-90 min with cut clupeid bait
(Brevoortia tyr annus and Alosa aestivalis). Black
sea bass >20 cm TL, the approximate size of full
retention in the traps, were measured to the nearest
mm TL and tagged with 13 mm diameter plastic disc
tags attached under the first dorsal fin with a nickel
pin trimmed to the proper length and held in place
with a 13 mm diameter plastic backing disc. Expan-
sion of the swim bladder, due to reduced hydrostatic
pressure, caused captured fish to float, so gas was
released from the swim bladder with a 20-gauge
hypodermic needle to enable fish to return to the
bottom. For each experiment, 50-75 tagged fish,
handled in the same fashion as those released, were
held on the bottom in wire cages for about 24 h to
determine tag-related mortality. Tagged fish were
released over the reef, and sampling for recaptures
started 24 h after tagging began. Experiments were
completed in 48 h except at site 2 during the sum-
mer of 1982 when tagging was interrupted for 48
h by weather.
Preliminary estimates of population size are
needed to determine sample sizes required for
precise Petersen estimates (Everhart and Youngs
1981). Powles and Barans (1980) estimated the mean
density of C. striata on reefs was 51 fish/ha from
underwater television transects; expansion to the
areas of our study sites gave preliminary estimates
of 8,160 C. striata on site 1 and 6,120 on site 2. At
site 1 we needed to tag 1,000 fish and examine 550
for tags to have an error no greater than 25% for
19 times out of 20 (1 - a = 0.95 and P = 0.25). At
site 2, we needed to tag 1,000 fish and examine 500.
We used the adjusted Petersen estimate (Ricker
1975, p. 78):
N* =
(M + 1) (C + 1)
(R + 1)
where N*
M
C
R
estimated population size
number of fish tagged
sample taken for census
number of tags returned in the sam-
ple taken for census.
The biomass of C. striata for each year and site
was estimated as
Biomass = 21— x PE x g\
where n1 = number of tagged fish in each 1 cm
TL interval
n = total number of tagged fish
PE = population size from the Petersen
estimate
g = weight in grams for the midpoint of
each 1 cm TL size interval derived
from the total length-weight rela-
tionship
a = number of 1 cm TL intervals of
tagged fish.
In addition, the upper and lower confidence limits
were substituted for PE in the above expression for
estimates of the biomass at those population sizes.
RESULTS
Age and Growth
We believe that the central opaque zone of the
sagitta may represent the first 1-4 mo of life in C.
striata. This zone varied in length from 1.16 to 3.60
mm in the anteroposterior plane and from 0.56 to
1.54 mm in the dorsoventral plane (Fig. 4). We were
not always able to make counts along a continuous
728
WENNER ET AL.: LIFE HISTORY OF BLACK SEA BASS
DORSAL
ANTERIOR
i
POSTERIOR w
NUCLEUS
CENTRAL FIELD
VENTRAL
— length-
Figure 4.— Schematic representation of the left sagitta in young of the year Centropristis striata showing
the orientation and direction of growth ring-counts in the central opaque zone, a = anterior, d = dorsal, p
= posterior, v = ventral.
line because grinding did not expose all rings equally
in the central zone. Also, in some instances, count-
ing was halted at a distinct mark, such as a ring
more distinctive than others, and we followed this
mark around the sagitta to a site where rings were
again visible and resumed counting. The number of
rings in the central zone varied because of the oto-
lith asymmetry and with the direction of the count
(Table 2). For example, we obtained the following
counts from the central primordium in one specimen
(number 9 of Table 2): 90 rings to the dorsal edge
of the central field (d of Fig. 4); 95 rings to the ven-
tral edge (v of Fig. 4); 129 rings to the posterior edge
(p of Fig. 4).
Since marginal increments on the otoliths should
approach zero during the time of annulus formation,
we calculated their monthly means to determine if
one opaque band was laid down during each year
on the sagittae of C. striata. Generally, a single an-
nulus was formed during April and May in all age
groups (Fig. 5). We found that the ring was
deposited unevenly around the sagitta, with the dor-
sal margin of the annulus being the last to be
completed.
We identified 10 age groups in the South Atlan-
tic Bight population of C. striata, which exceeded
the previous reports of 7 (Cupka et al. 19735) and
8 (Mercer 1978) groups. Observed mean lengths and
weights increased with age; however, small sample
sizes in ages 8 through 10 masked this trend (Table
3). Regressions of weight on length (TL and SL) and
length on length are in Table 4.
5Cupka, D. M., R. K. Dias, and J. Tucker. 1973. Biology of
black sea bass, Centropristis striata from South Carolina waters.
Unpubl. manuscr. South Carolina Wildlife and Marine Resources
Department, P.O. Box 12559, Charleston, SC 29412.
Table 2.— Data from Centropristis striata examined for daily growth rings. Refer to Figure 2 for otolith morphology and terms
(d, v, p, and a) used in the counts. Numbers in parentheses are ranges of several counts; dashes indicate no counts made.
Fish
Otolith
Central field
Daily ring
counts
TL
SL
WT
Height
Length
Height
Length
No.
(mm)
(mm)
(g)
(mm)
(mm)
(mm)
(mm)
d
V
P
a
1
66
54
4
1.56
broken
0.92
1.76
—
(84-89)
—
2
60
48
2
1.52
3.08
0.56
1.16
28
(25-26)
(50-51)
—
3
95
74
11
2.24
4.44
1.54
3.25
—
(109-120)
—
—
4
125
98
30
2.92
4.88
1.54
3.60
—
135
—
—
5
78
61
4
1.82
broken
0.98
broken
105
—
—
—
6
76
58
5
1.84
3.44
1.08
2.68
106
—
121
—
7
78
60
4
1.78
3.40
1.12
2.88
(98-106)
—
—
—
8
81
63
5
1.92
3.60
1.52
3.40
51
—
—
81
9
—
64
6
1.84
3.52
1.16
3.08
90
95
—
129
729
6-i
5-
cr f>
o h 4.
-I
< K
< 3
s 2
<
UJ
2
3-
2-
(28)
(246)
FISHERY BULLETIN: VOL. 84, NO. 3
(167)
(2310
M
~i 1 r
M J J
MONTHS
Figure 5.— Mean marginal increment by month for otoliths of Centropristis striata.
Number in parentheses represent monthly number of otoliths examined.
Table 3.— Means (x), standard deviations and sample sizes for observed lengths
(mm) and weights (g) by age for Centropristis striata.
Total length
Standard length
n (x) SD
Weight
Age
n
(x)
SD
n
(*)
SD
0
185
94
25
186
73
20
186
17
16
1
818
163
27
830
127
21
822
70
38
2
2,712
215
28
2,714
167
21
2,688
152
65
3
4,271
249
34
4,263
192
24
4,246
228
102
4
2,376
291
40
2,371
222
28
2,350
348
142
5
951
337
46
950
256
32
904
520
206
6
497
375
48
497
284
35
460
711
266
7
138
395
50
139
299
38
121
823
280
8
48
394
50
48
301
38
43
838
289
9
10
406
58
10
305
46
7
816
383
10
4
404
45
4
303
35
3
685
85
Table 4. — Least square linear and geometric mean functional regression equations of weight (WT) on total
length (TL) and standard length (SL), and length-length for Centropristis striata. Weight units are grams and
lengths are millimeters. All least squares regressions were significant at o = 0.01.
Least squares equation
n
r2
GM functional equation
log10 WT = -4.375 + 2.800 log10 TL
log10 WT = -4.328 + 2.978 log10 SL
TL = -9 + 1.4 SL
SL = 12 + 0.7 TL
12,281
12,284
12,473
12,473
0.97
0.98
0.97
0.97
log10 WT = -4.478 + 2.844 log10 TL
log10 WT = -4.398 + 2.949 log10 SL
TL = -12 + 1.4 SL
SL = 9 + 0.7 TL
Least squares regressions of SL (mm) on otolith
radius (OR in ocular units) are
log10 SL = 0.668 + 1.056 log10 OR;
n = 12,011; r2 = 0.89.
The intercept of the SL-OR relationship was used
to obtain the mean back-calculated SL's at age which
were lower than observed SL's in all cases (Table
5). Weighted least square estimates of von Ber-
talanffy parameters, asymptotic 95% confidence
Table 5.— Observed and back-calculated mean standard length
in mm and von Bertalanffy standard length at age for Centropristis
striata.
Observed
Back-calculated
von Bertalanffy
Age
n
SL
SL
SL
1
830
127
88
88
2
2,714
167
142
141
3
4,263
192
180
182
4
2,371
222
212
215
5
950
256
244
241
6
496
284
271
261
7
139
299
283
278
8
48
301
289
291
9
10
305
296
301
10
4
303
303
309
730
WENNER ET AL.: LIFE HISTORY OF BLACK SEA BASS
limits and asymptotic standard errors were also
derived from these data (Table 6). Estimates of an
average asymptotic size (LJ depended not only on
the number of age groups present and the distribu-
tion of individuals within each group, but also on the
curvature of the age-size relationship. An average
asymptotic size of 341 mm SL appeared conser-
vative. The largest fish aged was 390 mm SL and
only 0.6% of all C. striata sampled were larger than
341 mm SL. The largest specimen caught off the
South Carolina coast was estimated to be about 490
mm SL (S.C. Wildlife and Marine Resources Depart-
ment6). Comparisons of von Bertalanffy back-
calculated and observed SL at age are in Table 5.
Table 6. — Estimated von Bertalanffy parameters describing the
growth of Centropristis striata. The weighted residual sums of
squares = 238.46. SE = standard error; C.L. = confidence limits.
Param-
eter
Estimate
Asymptotic
SE
Asymptotic
lower
95% C.L
upper
L
341
0.2309
-0.3010
17.818
0.0221
0.0560
298
0.1787
-0.4335
383
0.2831
-0.1685
Reproduction
The generalized ovarian structure of C. striata is
similar to that of Epinephelus fulva (Smith 1965),
E. morio (Moe 1969), and Hemanthias vivanus
(Hastings 1981). The bilobed organ is suspended by
mesenteries from the swim bladder in the posterior
region of the body cavity. The lobes fuse posteriad,
and their lumina form a common oviduct. Blood
vessels and nerves enter the ovary at the anterior
point of each lobe's suspension and continue pos-
teriad medial to the supportive mesenteries along
the dorsomedial surface of each lobe. The lumina are
lined with folded germinal epithelium (ovarian
lamellae), within which oocytes develop and mature.
The lamellae are first seen protruding from the dor-
sal region of the lumen at the boundary of the ovary
and the alamellar oviduct. They continue along both
sides of the lumen in the area of gonadal confluence
until only the ventralmost region of the ovary is
alamellar. This alamellar area is confluent with the
oviduct and extends anteriad to half of the lengths
of each ovarian lobe (Fig. 6 A). The alamellar regions
of female gonads were bordered throughout their
extent by testicular precursor cells (Figs. 6A, B; 7A).
Although these bands of cells were found in vary-
ing stages of development in all ovarian tissues, the
most active proliferation of identifiable sperma-
togenic tissue (as manifested by transitional gonads;
Table 7) occurred after the spring and fall spawn-
ing seasons (described later). Both increased ovarian
inactivity and degeneration coincided with the pro-
liferation of testicular tissue during sexual succes-
sion (simultaneous hermaphroditic development is
treated below). No instance of active ovarian devel-
opment concurrent with testicular degeneration was
observed.
Sexual transition commenced in the posterior
region of the ovary with the expansion of testicular
lobes into the ovarian lumen. This proliferation pro-
ceeds anteriad, with sperm sinus forming in the
ovarian tunic adjacent to the testes. Testicular
growth appears to be the result of mitotic sperma-
togonial development, although limited spermato-
genic processes, including spermatozoa formation,
are not uncommon (Fig. 7B). The sperm sinuses, as
well as the vas deferens (which form within the ovi-
ductal wall) apparently result from ruptures in their
respective surrounding tissues, as suggested by
Hastings (1981), because there was no cell lining
associated with these structures (Fig. 7B).
Simultaneously developed hermaphroditic gonads
were found in all maturity stages. However, only
3% of the fishes exhibited this phenomenon, and we
were unable to determine if the vas deferens had
an external opening; therefore, we lack definitive
proof that these fish were functional simultaneous
hermaphrodites.
Histological sections of immature ovaries con-
tained only oogonia and small basophilic, previtel-
logenic oocytes about 8-100 /^m in diameter. Matur-
ing ovaries had oocytes 100-500 ^m in diameter, in
Table 7.— Monthly sex composition data for Centropristis striata
along with x2 values for tests of a 1 :1 sex ratio. * * = P < 0.01 ,
1 df; * = P< 0.05, 1 df.
6Office of Conservation, Management, Marketing and Recrea-
tional Fisheries, S.C. Wildlife and Marine Resources Department.
1982. South Carolina Saltwater Sport Fishing Tournaments and
State Record Fish. S.C. Wildlife and Marine Resources Depart-
ment, P.O. Box 12559, Charleston, SC 29412.
Transi-
Transi-
tional
Month
Males
Females
tional
(%)
o-:9
x2
January
13
13
1
3.7
1
1
—
February
111
107
8
3.6
1
0.96
0.07
March
15
7
0
0
1
0.47
2.91
April
928
1,685
122
4.5
1
1.82
219.30**
May
404
497
145
13.9
1
1.23
9.60**
June
509
1,039
383
19.8
1
2.04
181.46**
July
132
368
84
14.4
1
2.79
111.39**
August
112
246
42
10.5
1
2.20
50.16**
September
668
1,109
262
12.8
1
1.66
109.44**
October
35
17
1
1.9
1
2.05
5.12*
November
64
150
27
11.2
1
2.34
34.56**
December
34
19
13
19.7
1
0.56
4.45
731
FISHERY BULLETIN: VOL. 84, NO. 3
Figure 6.— Schematic representation of a functionally female ovary from Centropristis striata. A)
Ventral view of ovary showing the alamellar region. Cross sections of the ovary were made in planes
I-I and II-II, and show the positioning of the primordial testicular tissue at the boundary of the alamellar
regions. B) An enlargement of the area indicated, showing the cellular relationships of the alamellar
area, testicular primordia and ovarian lamellae. AL = alamellar region, 0 = oocytes, OL = ovarian
lamellae, OT = ovarian tunic, SP = chords of spermatogonia, TP = testicular primordia.
Figure 7.— Photomicrographs of histological sections of gonads
from Centropristis striata. A) Cross section taken from the
posterior region of a functional ovary showing the alamellar region
and testicular primordia, 250 x magnification. B) Cross section
taken from the posterior region of a gonad undergoing transition,
250 x magnification. C) Cross section of immature testicular tissue
from a 133 mm SL fish, 100 x magnification. D) Cross section of
a simultaneous gonad showing active testicular and ovarian
development, 100 x magnification. AL = alamellar region, DO =
developing oocyte, OL = ovarian lamellae, OT = ovarian tunic,
S = spermatozoa, SP = spermatogonia, T = testicular tissue.
732
WENNER ET AL.: LIFE HISTORY OF BLACK SEA BASS
AL
/
N>t'
SP
A
fc,. * - '^ ■ ;* ■
<Tc
a^a^V
B
-
- ' - e* * ff .» - -a i^r ISO s^Js
733
FISHERY BULLETIN: VOL. 84, NO. 3
stages from yolk vesicle formation (Wallace and
Selman 1981) through late vitellogenesis. Oocytes
(500-740 nm in diameter) in ripe ovaries showed
coalescence of yolk globules and hydration. Gonads
from spent and resting females contained decreas-
ing amounts of unspawned, atretic oocytes and
empty, ruptured follicles.
Gonads from immature males were characterized
by primary and secondary spermatogonia (Fig. 7C),
and isolated, more fully developed seminiferous
crypts in some instances. In developing testes we
saw several stages that included gonadal tissue com-
posed mostly of primary and secondary spermato-
cytes, as well as sperm sinuses filled with mature
spermatozoa. Ripe testes had sperm sinuses and
ducts packed with spermatozoa; the remainder of
the gonad showed only a little spermatogenesis.
Spent testes showed both the lack of spermatogenic
activity and the presence of large amounts of unshed
sperm, whereas gonads in resting males showed
mitotic proliferation of next season's spermatogonia
and interstitial tissues.
Females comprised 52% of the sexed C. striata
and were mature in ages 1 through 8. We found
mature gonads in none of the females at age 0,
48.4% at age 1, 90.3% at age 2, 99.1% at age 3, and
100% at all older ages. Immature females were
50-180 mm SL, and the smallest mature specimen
was 110 mm SL. Males made up 30.6% of the fishes
sexed, and 1.3% of these males were immature and
were in ages 0-1 with lengths of 50-180 mm SL. The
smallest mature male was 100 mm SL.
Gonads of 14% of the C. striata examined histo-
logically showed these fishes undergoing sex suc-
cession. These were found primarily after the major
spawn (January- April), and during a brief period
after the lesser spawn during September-October
(Table 7). The smallest individuals exhibiting sex suc-
cession were in the 120-139 mm SL interval (Table
8); however, the greatest frequency of transitional
gonads (77%) occurred in fishes 160-259 mm SL.
Males made up 15.4% of the age 0 C. striata and
10.5% of fishes <120 mm SL (Tables 8, 9; Fig. 8).
The relative abundance of males increased with both
size and age, and fish containing transitional gonads
increased in abundance during the period of the
most rapid decline in the relative number of females
(Fig. 8).
Both male and female tissue developed simulta-
neously in the same gonad in 3% of the C. striata
examined histologically (Fig. 7D). This occurred in
immature, developing, spent, and resting fishes.
Both testicular and ovarian tissues showed equiv-
alent maturity stages within the same gonad; that
is, male and female germinal tissue developed con-
currently.
The overall sex ratio for C. striata in the South
Atlantic Bight was la: 1.719. We found significantly
more females than males from April through
November, and inconsistency in the ratio between
December and March probably reflected both in-
adequate and biased samples from these months.
Ratios were significantly different at all sizes from
an hypothesized 1:1 (Table 8) except at 200-219 mm
SL. The abundance of males begins to increase in
that size group and also in age class 4 (Table 9) as
the abundance of females declines, reflecting the in-
creased frequency of the sex succession process.
Centropristis striata has a major spawn from
January through April when 80-100% of the ovaries
were developing or ripe (Fig. 9). Although a second
period of ovarian activity was found in September,
it was interpreted as being of a lesser nature since
only 30% of the females were developing or ripe.
Table 8.— Sex composition and x2 values for tests of a 1:1 sex
ratio of Centropristis striata by 20 mm SL intervals. * * = P < 0.01 ,
1 df; * = P < 0.05, 1 df.
Transi-
Transi-
tional
SL
Males
Females
tional
(0/0)
cr.Q
x2
-119
16
136
0
0
1:8.50
94.74**
120-139
28
206
4
1.7
1
7.36
135.40**
140-159
74
525
46
7.1
1
7.10
339.57**
160-179
170
1,145
200
13.2
1
6.74
722.91**
180-199
301
796
289
20.8
1
2.64
223.36**
200-219
347
423
112
15.3
1
1.22
7.50*
220-239
335
185
94
14.8
1
0.55
43.27**
240-259
278
106
67
13.0
1
0.38
77.04**
260-279
179
41
33
4.2
1
0.23
86.56**
280-299
154
26
8
2.5
1
0.17
91.02**
300-319
111
5
3
3.3
1
0.04
96.86**
320-339
57
1
2
3.5
1
0.02
54.07**
>339
55
0
2
3.6
Total
2,105
3,595
1:1.70
Table 9.— Sex composition and x2 values for tests of a 1:1 sex
ratio of Centropristis striata by age. * * = P < 0.01 , 1 df .
Transi-
Transi-
tional
Age
Males
Females
tional
(0/0)
ct:9
x2
0
10
55
0
0
1:5.50
31.2**
1
42
315
20
5.3
1
7.50
208.8**
2
251
1,066
185
12.3
1
4.20
504.3**
3
561
1,449
447
18.2
1
2.60
392.3**
4
635
479
223
16.7
1
0.75
21.8**
5
274
84
59
5.0
1
0.31
100.8**
6
189
17
8
3.7
1
0.09
143.6**
7
54
2
2
3.4
1
0.04
48.3**
8
13
0
0
0
9
2
0
0
0
10
2
0
0
0
734
WENNER ET AL.: LIFE HISTORY OF BLACK SEA BASS
. "V..
\
to
<
20-
\
O
X
o
<
<
LjJ 100-
UJ °
o
tr
UJ
0- 60-
\
»-*->
— i — i 1 1 i —
100 150 200 250 300
SIZE CLASS(cm)
• — — • f»mol«8
x x transitional
r
yf
*
\
\
'■V S
60 ^
-I
o
40 X
o
<
UJ
X
V)
<
z
loo o
h-
80 |
cr
— i 1 1 1 1 1 1 —
12 3 4 5 6 7
AGE
Figure 8.— Percent female and transitional Centro-
pristis striata by size and age.
Fall spawning probably extended into October
because many fishes obtained in November had
recently spent ovaries.
Fecundity was significantly related to SL, TL,
weight, and age with the former three equations
having by far the highest r2 values (Table 10). The
Female • = Developing + Ripe
Maturity ■ = Spent + Resting
Stage
A M J J
MONTHS
Figure 9.— Maturity stages of female Centropristis striata by
month to illustrate bimodal spawning.
least squares linear regression model of fecundity
on age explained only 33% of the variation in fecun-
dity. Observed mean fecundity and its standard
error increased with age (Table 11). The lowest
observed fecundity (17,000) was in a 2-yr-old fish (SL
= 108 mm; TL = 140 mm; weight = 45 g) and the
largest (1,050,000) was in a 438 mm SL fish (TL =
454; weight = 1,371 g) of undetermined age.
Mortality
Instantaneous rates of total mortality, as derived
from catch curves, for C. striata ranged from 0.721
Table 10. — Least squares linear and geometric mean functional regression equations of fecundity (fee) on
total length (TL), standard length (SL), weight (WT), and age for Centropristis striata. Weight units are grams
and lengths are millimeters. All least squares regressions were significant at o = 0.01.
Least squares equation
GM functional equation
log10 fee = -0.605 + 2.335 (log10 TL)
log 10 fee = -0.309 + 2.318 (log10 SL)
log10 fee = 3.057 + 0.822 (log10 WT)
log 10 fee = 4.529 + 0.913 (log10 Age)
115
0.62
log10 fee =
-2.098 + 2.959 (log10 TL)
115
0.65
log10 fee =
-1.589 + 2.879 (log10 SL)
115
0.65
log10 fee =
2.587 + 1.022 (log10 WT)
110
0.33
log10 fee =
4.196 + 1.580 (log10 Age)
Table 1 1 . — Observed mean fecundity at age and its
standard error (S^) for Centropristis striata, in the
South Atlantic Bight.
Age
Mean fecundity
Sx
n
2
61,846
8,089
13
3
94,801
4,406
55
4
115,411
8,900
27
5
160,000
50,720
7
6
226,040
46,706
5
7
287,350
80,650
2
8
137,400
—
1
to 1.430, and actual mortality rates were from 0.513
to 0.761. Values increased from 1978 to 1981. For
example, values of A rose from 51.3 to 73.3% for
trap-caught fish and from 51.6 to 76.1% for hook-
and-line caught fish older than age 4 (Table 12). Mor-
tality values of trap-caught and hook-and-line caught
C. striata were similar within years for each estima-
tion procedure. Mortality values, moreover were
similar between estimation procedures. We found
a significant correlation between the instantaneous
735
FISHERY BULLETIN: VOL. 84, NO. 3
Table 12. — Instantaneous (Z) and actual (>A) rates of total mortality for Centropristis
striata in the South Atlantic Bight. Gear types: T = trap; H&L = hook and line.
Gear
Catch
Z
curve
A
Heinke
Z A
Chapmar
Z
-Robson
A
Means
Year
Z
A
1978
T
0.721
0.513
0.841
0.568
0.991
0.628
0.851
0.569
1979
T
0.906
0.595
0.819
0.559
0.872
0.582
0.866
0.579
1979
H&L
0.726
0.516
0.759
0.532
0.650
0.478
0.712
0.509
1980
T
1.030
0.643
1.020
0.639
1.181
0.693
1.077
0.658
1980
H&L
0.905
0.595
0.944
0.611
1.016
0.638
0.955
0.615
1981
T
1.320
0.733
1.347
0.740
1.328
0.735
1.332
0.736
1981
H&L
1.430
0.761
1.347
0.740
1.492
0.775
1.423
0.759
1982
T
1.279
0.722
1.382
0.749
1.443
0.764
1.368
0.745
1982
H&L
1.246
0.712
1.277
0.721
1.309
0.730
1.277
0.721
rate of total mortality from trap data and the South
Carolina commercial landings from 1978 to 1982
(Fig. 10).
Population Estimates at
Specific Sites
Mortality of C. striata attributable to tagging
occurred only once, during the 1983 experiment of
site 2 when 6% of the fishes (3 of 50) died during
the holding period. Therefore, we reduced the
number of tagged fish-at-large (M) by 6% to account
for this tagging related mortality.
Between 1981 and 1983, a decline in the order of
magnitude from 20,070 to 2,236 individuals (88.9%)
occurred in the estimated abundance of C. striata
at site 1. On this reef, the abundance declined 60.6%
from 1981 to 1982 and another 75.5% from 1982 to
1983 (Table 13). Abundance at site 2 declined 52.9%
between 1982 and 1983. Biomass of C. striata
declined by an order of magnitude on site 1 from
4,836 kg in 1981 to 491 kg in 1983 (Table 13). This
was an overall decrease of 89.9%. Site 2 had a 62%
decline in biomass from 2,150 kg in 1982 to 810 kg
in 1983. Our estimates are for fish >20 cm TL,
the only ones vulnerable to the traps. Therefore,
density and biomass estimates are minimum val-
ues.
In addition to the declines in population size and
biomass of C. striata, there were decreases in mean
size and age. Mean TL was 3 cm less in 1983 than
in 1981 at site 1, whereas C. striata were on average
2 cm smaller in 1983 than 1982 at site 2. Not only
were the means reduced, but also the frequency
distribution became more skewed towards the
smaller size intervals and the contributions of larger
Figure 10.— Plot of the instantaneous rate of
total mortality (Z) as determined from resource
survey data (1978-81) and the South Carolina
commercial landings of Centropristis striata
for that year.
736
Cfl 1 3
>>
O
o
o
CO
OS
.5-
r-0.970
100 200 300
South Carolina Commercial Landings(metric tons)
WENNER ET AL.: LIFE HISTORY OF BLACK SEA BASS
Table 13.— Summary of Petersen mark-recapture population estimates, biomass, and density (number and kg/ha) estimates
for black sea bass, Centropristis striata, on two sponge-coral habitat sites. 95% confidence limits (C.L.) of p(= RIC) were
determined by the methods of Cochran (1977).
Site 1
Site 2
1981
1982
1983
1982
1983
c
634
529
438
446
679
M
1,042
1,169
1,084
901
854
R
32
67
212
50
155
95% C.L of R
21.9-44.2
53.4-83.1
193.2-230.8
33.9-57.5
135.1-175.2
P
0.50
0.127
0.484
0.112
0.228
95% C.L. of p
0.035-0.070
0.101-0.157
0.441-0.527
0.076-0.129
0.199-0.258
AT1
20,070
9,119
2,236
7,906
3,727
95% C.L. of AT
14,653-28,921
7,347-1 1 ,399
2,055-2,453
6,892-11,553
3,300-4,272
M
0.032
0.058
0.196
0.056
0.182
95% C.L of h
0.022-0.043
0.046-0.072
0.179-0.213
0.039-0.065
0.159-0.206
Biomass (kg)
4,836
2,077
491
2,150
810
95% of biomass (kg)
3,530-6,959
1 ,673-2,595
451-539
1,874-3,142
717-928
Number/ha
125
57
14
66
31
95% C.L. of number/ha
92-181
46-71
13-15
57-96
28-36
kg/ha
30.2
13.0
3.1
17.9
6.7
95% C.L. of kg/ha
22.1-43.5
10.5-16.2
2.8-3.4
15.6-26.2
6.0-7.7
'Adjusted Petersen estimate (Ricker 1975).
fishes to the populations was greatly reduced (Fig. (Fig. 12). Fishes age 4 and older went from 42% of
11). Mean age declined 0.5 years at site 1, and the the population in 1981 to 25% in 1982 and 9% in
age composition shifted towards younger age classes 1983.
20
15-
10-
5-
20-i
JU-
18-
Sit* 2. 1S82
5 TL"26cm
10-
5-
' "l i i i i i i i i
Site 2, 1883
x TL-=24cm
1 I I I I I I I I I I I I i I I i I i r
20 25 30 35 40
TOTAL LENGTH(cm)
Figure 11.— Size-frequency distribution of
Centropristis striata from five discrete mark-
recapture tagging studies.
737
FISHERY BULLETIN: VOL. 84, NO. 3
Figure 12.— Age composition of Centropristis
striata at the two experimental mark-recapture
sites.
50
30
x Age 3.4
Site 1
1981
n
Site 1
1982
50-,
30
10
x Age3.3
Site 2
1982
a
>i _
50
30
10
x Age3.1
Site 2
1983
n
3
AGE
DISCUSSION
Age and Growth
The cause of the variation in size and shape of the
sagitta's central field in C. striata is unknown, how-
ever, differing size of the nuclei of Atlantic herring,
Clupea harengus, can be related to spawning season
(Postuma 1974). Further studies are needed to
determine if these differences can be related to
spawning time of C. striata in the South Atlantic
Bight.
Inadequate validation in many studies that esti-
mate age have been noted by Beamish and McFar-
lane (1983), and they have reemphasized the need
for verification of aging technique. Our attempts at
validation have shown that one annulus is formed
each year during April-May. Also, our counts of
presumed daily growth rings have provided circum-
stantial support for the formation of the first an-
nulus. A similar approach was used by Radtke et
al. (1985) in their study of the oyster toadfish, Op-
sanus tau.
Our mean back-calculated lengths agree well with
Mercer's (1978) data for C. striata from the South
Atlantic Bight up to age 5; however, ours are much
smaller than Cupka et al. (fn. 5). Our lengths at age
are consistently smaller than C. striata from the
Middle Atlantic Bight (Mercer 1978). Mercer (1978)
attributed size at age differences between the two
areas to gear selectivity, yet our results suggest that
C. striata from the South Atlantic Bight are smaller
than those of the Middle Atlantic Bight. The larger
size at age found by Cupka et al. (fn. 5) may reflect
the population of C. striata in the South Atlantic
Bight prior to heavy exploitation that began in 1969.
Since estimates of Lm, K, and t0 are affected by
several nonbiological, methodical factors, direct
comparisons of these growth parameters between
different studies are of limited value. However,
when viewed in relative terms, they can indicate
general differences or similarities between studies,
species, or areas. Our estimate of L^ (341 mm SL)
was much closer to Mercer's (1978) value (L^ =
352 mm SL) than that of Cupka et al. (fn. 5) (°°625
mm SL). Our growth coefficient (K) was higher, in-
dicating that C. striata achieves maximum attain-
able size more rapidly than previously reported.
These differences could have been caused by sam-
pling methodologies and/or conditions of the popula-
738
WENNER ET AL.: LIFE HISTORY OF BLACK SEA BASS
tion of South Atlantic Bight C. striata at the time
the studies were conducted.
Reproduction
Smith (1965) established a phylogeny of serranid
fishes based on three types of hermaphroditism.
Most primitive is the Serranus-type gonad found in
Serranus and Hypoplectus, genera which are simul-
taneously hermaphroditic with male and female ger-
minal tissues well separated by connective tissues.
The middle type of this trio is the protogynously her-
maphroditic Rypticus-Anthias-type gonad where
testicular takeover commences with proliferation of
preexisting spermatogonia located in crypts along
the alamellar regions of the ovary and gametogenic
tissues remain separated by connective tissue
throughout sexual transition. Most advanced is the
protogynous hermaphroditic Epinephelus-type
gonad where testicular tissue cannot be found before
sexual transition commences. During this process,
crypts of spermatogonia differentiate and prolifer-
ate within the ovarian lamellae where they are inter-
mixed with oogonia and oocytes.
Citing Lavenda (1949), Smith (1965) classified C.
striata within the Epinephelus-type, an error cor-
rected by Mercer's (1978) demonstration that mor-
phological events during sexual transition in C.
striata most resemble those of the Rypticus-
Anthias-type gonad. Sexual succession in C. striata
results from hypertrophy of bands of testicular
primordia that lie along borders of the alamellar
region of the ovary, not the proliferation of crypts
of tissue that Mercer (1978; see also Smith 1965)
reported. The arrangement of the primordial tes-
ticular ridges in C. striata is the same as in the pro-
togynous Hemanthias vivanus (Hastings 1981).
The testicular primordia in C. striata is located
in a similar region of the gonad as is the testicular
portion of the simultaneously functioning gonad of
Serranus tigrinus (Smith 1965). Though not stated
by Smith (1965), the testes of S. tigrinus might
border the alamellar region of the ovarian section
as does the testicular primordial cells in C. striata,
a gonadal similarity also noted between H. vivanus
and S. tigrinus (Hastings 1981). No phylogenetic in-
ferences should be drawn from these data, because
gonadal development varies even among the close-
ly related simultaneous hermaphrodites of the
genera Serranus and Diplectrum. Centropristis
striata, H. vivanus, and probably R. maculatus (see
Smith 1965) have similar gonadal morphologies and
strategies of sex succession, but these species are
usually not considered closely related. Gonadal mor-
phologies may one day be important in determin-
ing serranid phylogenetic relationships, but more
observations of all serranids are necessary.
The simultaneously functioning gonad of C.
striata has morphology similar to that of Serranus
(Smith 1965) in which discrete areas of testicular
tissue empty into peripherally located sinuses, and
oocytes discharge centrally. Sperm sinuses within
the wall of the simultaneous gonads are well
developed in C. striata, but it is not known if they
are functional, i.e., permit sperm to exit the body
along with the oocytes.
We found sizes and ages of C. striata undergoing
sex succession which were similar to those Mercer
(1978) reported in the South Atlantic Bight; how-
ever, we found a much higher incidence of transi-
tional fish. Since Mercer (1978) found only 4% of
C. striata from this area were undergoing sex suc-
cession, she offered two mechanisms for her abun-
dance (38%) of mature males: 1) development of
mature males from both immature males and
juvenile hermaphrodites was very important, or 2)
the rate of sexual transition was very rapid in this
species.
We feel that both of Mercer's arguments were at
best incomplete because of her small sample sizes
from the South Atlantic Bight. Since we found few
immature males and juvenile hermaphrodites in our
samples, the probability is low that mature males
develop solely from these. Also, we acknowledge the
presence of serranids which show rapid sex succes-
sion (Fishelson 1970; Fricke and Fricke 1977) and
believe the low frequency of individuals undergoing
sex succession seen in most Epinepheline groupers
probably reflects a similarly short-lived process.
However, the presence of C. striata undergoing sex
succession throughout the year, and their occur-
rence at sizes where the frequency of females
declines, leads us to conclude that the primary
source of mature males is through sex succession
from active females.
We found secondary testes (sensu Harrington
1971) in all male C. striata including immature
specimens. This morphology is not unique to C.
striata. Hastings (1981) observed no primary male
H. vivanus and suggested they all passed through
an initial female phase. This same secondary gonadal
morphology occurs in the secondarily gonochoristic
serranid Paralabrax clathratus (Smith and Young
1966), and Reinboth (1970) indicated all male ser-
ranids are derived from females.
Overall, sex ratios of C. striata were significantly
different from an hypothesized la:l9 in favor of
females. Females significantly outnumbered males
739
FISHERY BULLETIN: VOL. 84, NO. 3
up to an intermediate size and age, at which time
the significantly different ratios favored males.
Fishelson (1975) stated that sex ratios should ap-
proximate la: 19 at some stage if all protogynous
females undergo sex succession. Given the alter-
nating ratios of sexual abundance with size and age,
and considering that no female older than age 7 and
few larger than 330 mm SL were found in our
samples, leads us to conclude that all C. striata have
the potential to undergo sex succession.
Population Estimates
The underlying assumptions of the Petersen
method for population estimates were met in this
study. We found tag-related mortality in only one
experiment and adjusted the number of fish marked
for it. We feel all tags were accounted for and tag
loss was minimal, because tags were firmly anchored
to the fish and were bright orange. Tagged fish were
not randomly distributed over the study site, but
they were released during vessel drifts governed by
wind and surface currents and may be effectively
random. We assumed minimal immigration and
emigration because our experiments covered a brief
time period.
Powles and Barans (1980) estimated density of C.
striata in the sponge-coral habitat of the South
Atlantic Bight. The estimates of 51 fish/ha and 7.6
kg/ha derived from the data of Powles and Barans
(1980) were 37-66% and 23-44% of our mark-recap-
ture values. Powles and Barans (1980) indicated that
possible sources of error in their study were distance
determinations from loran-A, which are much less
precise than distances derived from loran-C read-
ings, and variable visibility.
ACKNOWLEDGMENTS
This work was funded by the National Marine
Fisheries Service under contract NA-84-WCC-06101
to the South Carolina Wildlife and Marine Resources
Department. We appreciate the Assistance of A. J.
Kemmerer and W. Nelson of NMFS.
We thank Captain John Causby and First Mate
Julian Mikell of the RV Oregon for the exceptional
navigational and vessel handling skills enabling us
to sample open ocean patch reefs not much larger
than a few football fields with a 90-ft vessel. The
difficulties involved can be appreciated only by one
who has been there. It would not have been possi-
ble to process the numerous histological samples
without the help of D. Stubbs. We are grateful to
the many individuals who participated in the field
effort, several of whom suffered punctures by fish
spines and lacerations by sea bass preopercles dur-
ing the tagging study. A. G. Gash provided assis-
tance with the computer analysis, K. Swanson drew
the figures and N. Beaumont and M. Lentz typed
the manuscript. Helpful critical reviews of the
manuscript were made by C. A. Barans, E. L. Wen-
ner, R. Warner, P. Hastings, G. Huntsman, P.
Eldridge, and two anonymous reviewers.
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Postuma, K. H.
1974. The nucleus of the herring otolith as a racial character.
J. Cons. Int. Explor. Mer 35:121-129.
Powles, H., and C. A. Barans.
1980. Groundfish monitoring in sponge-coral areas off the
southeastern United States. Mar. Fish. Rev. 42(5):21-
35.
Radtke, R. L., M. L. Fine, and J. Bell.
1985. Somatic and otolith growth in the oyster toadfish (Op-
sanus tau L.). J. Exp. Mar. Biol. Ecol. 90:259-275.
Reinboth, R.
1970. Intersexuality in fishes. Mem. Soc. Endocr. 18:515-
544.
RlCKER, 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.
Rivers, J. B.
1966. Gear and technique of the sea bass trap fishery in the
Carolinas. Commer. Fish. Rev. 28(4):15-20.
Smith, C. L.
1965. The patterns of sexuality and the classification of ser-
ranid fishes. Am. Mus. Novit. 2207, 20 p.
Smith, C. L., and P. H. Young.
1966. Gonad structure and the reproductive cycle of the kelp
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SOKAL, R. R., AND F. J. ROHLF.
1981. Biometry. 2d ed. W. H. Freeman & Co., N.Y., 859
P-
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.
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Wallace, R. A., and K. Selman.
1981. Cellular and dynamic aspects of oocyte growth in
teleosts. Am. Zool. 21:325-343.
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.
741
NOTES
COMPARISON OF VISCERAL FAT AND
GONADAL FAT VOLUMES OF YELLOWTAIL
ROCKFISH, SEBASTES FLAVIDUS, DURING
A NORMAL YEAR AND A YEAR OF
EL NINO CONDITIONS
One of the severest El Nino events of the century
occurred off California during late 1982 and most
of 1983 (Rasmusson 1984). Associated with the
warm water and lack of upwelling were impressions
by many fishermen and biologists that macroplank-
tonic organisms were at low densities and that fish
were thinner than normal. A semiquantitative sam-
pling program off of San Francisco indicated that
euphausiids, a major component of the macroplank-
ton, were considerably less common in 1983 than
in either 1982 or 1984 (Smith1).
Yellowtail rockfish are abundant off northern
California and are an important component of
recreational and commercial catches in some areas.
The species feeds mostly on macroplanktonic
organisms such as euphausiids, salps, and small fish
(Phillips 1964; Pereyra et al. 1969; Lorz et al. 1983).
Annual cycles of visceral fat volume and gonad
volume are documented in Guillemot (1982) and
Guillemot et al. (1985). The studies showed that
visceral fat volume in both sexes of yellowtail rock-
fish is at a maximum during fall. The viviparous
species (Boehlert and Yoklavich 1984) mates in early
fall (September) and releases larvae during winter
(January-March) (Wyllie Echeverria2). Guillemot
(1982) and Guillemot et al. (1985) showed that male
gonad volumes peak in fall and female gonad
volumes peak in winter.
The purpose of this study is to determine possi-
ble effects of El Nino conditions by comparing
visceral fat and gonad volumes during 1983, a year
of El Nino conditions, with data collected during
1980, a normal year (Guillemot 1982).
Methods and Materials
Guillemot (1982) and Guillemot et al. (1985) util-
ized data collected throughout the year. The 1983
data were collected only on 21 September, the ap-
proximate sexual activity peak for males, and 20
December, which slightly precedes the peak time of
larval release for females. Only 1980 data collected
within 20 d of the two 1983 collection dates and
samples collected from central California, between
Bodega Bay and Half Moon Bay, were used in this
study. In 1983 all specimens were collected from
landings made at Bodega Bay.
Specimens were sexed, measured to the nearest
millimeter for total length, and viscera were re-
moved and preserved in 10% buffered Formalin3 in
the field following the procedures of Guillemot et
al. (1985). After about 90 d of storage, visceral fat
and gonad volumes were measured to the nearest
milliliter by water displacement. Visceral fat of some
fish had dissolved to form a floating liquid. The
volume of this liquid was measured and added to the
total fat volume. Data from males larger than 379
mm, when 90% are mature, and from females larger
than 380 mm, when 85% are mature, were used
(Wyllie Echeverria fn. 2).
As in Guillemot (1982) and Guillemot et al. (1985)
we used the following power equation to describe
the relationship between fat or gonad volume and
length:
Y = aXP
where Y = fat or gonad volume, and
X = total length.
The parameters were estimated by first trans-
forming the variables to natural logarithms and then
using standard least squares linear regression
techniques. Analysis of covariance was used to
determine if separate lines for the two years
significantly reduced the variance from a common
line (Kleinbaum and Kupper 1978). This is a fairly
robust test in that if there is not a significant linear
relationship between the two variables for one or
both time periods, the test is nearly as powerful for
comparing the two means as an analysis of variance.
'Smith, S. Unpublished data. Tiburon Laboratory, Southwest
Fisheries Center, National Marine Fisheries Service, NOAA, 3150
Paradise Drive, Tiburon, CA 94920.
2Wyllie Echeverria, T. 1983. Reproductive seasonality and
maturity of the rockfishes (Scorpaenidae; Sebastes) off central
California. Unpubl. manuscr., 66 p. Southwest Fisheries Center,
Tiburon Laboratory, National Marine Fisheries Service, NOAA,
Tiburon, CA 94920.
3Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
743
Results
The regression lines for the male fat volume for
the two years intersect and are not significantly dif-
ferent (Table 1). The results of the analysis of
covariance for fat volume of females are highly
significant (Table 1). Females had significantly
higher fat volumes in 1980 for both months (Fig.
1).
The comparisons of gonad volumes produced
highly significant results in December for both
sexes, and for females in September (Table 2).
Female gonad volumes were higher in 1980 during
December and lines intersected in September (Fig.
2). Male gonad volumes were significantly higher in
December 1983 than in December 1980.
The seasonality of gonad development was similar
in the two years, but appeared to be delayed in 1983.
Table 1.— Results of analysis of covariance of fat volumes of yellowtail rockfish regressed
on length. Observations were transformed to natural logarithms for the analysis.
Month
1980
1983
Sex
Sample
size
Intercept
Slope
Sample
size
Intercept
Slope
F
Male
Male
Female
Female
September
December
September
December
20
17
25
19
-9.884
7.198
-9.327
21.813
2.011
-0.978
2.003
-3.262
38
35
46
50
22.272
35.402
5.443
1.609
-3.355
-5.693
-0.449
- 0.058
2.753
2.571
11.917**
5.889**
* "Significant at 99% level of confidence.
3.5
3.0
E 2.5
i
0
E
•2 2.0
o
>
5 1.5
1.0
0.5
a a Sep. 1980
a- -* Sep. 1983
• • Dec. 1980
•---• Dec. 1983
_L
_L
5.9 6.0 6.1 6.2 6.3
In (total length-mm)
Figure 1.— Relationships between In (visceral fat volume) and In
(total length) for female yellowtail rockfish in 1980 and 1983.
Males were 50% maturing and 50% resting in
September 1980, and 100% resting during Decem-
ber. In 1983 males were 100% maturing during
September, and 8% maturing and 92% resting dur-
ing December. Females were 35% maturing and
65% resting in September 1980, and 83% maturing
and 17% resting in December. In 1983 females were
100% maturing during September, and 97% matur-
ing and 2% resting during December. Data on
season or parturition for 1981-84 (Table 3) indicate
that parturition was delayed in 1983 and 1984 com-
pared with 1981 and 1982.
Discussion
The results tend to agree with expectations.
Female fat volumes were lower in 1983 than in 1980,
which is in agreement with the impressions of fisher-
men and the expectation that El Nino would pro-
duce relatively poor feeding conditions and conse-
quently result in thin fish.
Table 2.— Results of analysis of covariance of gonad volumes of yellowtail rockfish regressed
on length. Observations were transformed to natural logarithms for the analysis.
Month
1980
1983
Sex
Sample
size
Intercept
Slope
Sample
size
Intercept
Slope
F
Male
Male
Female
Female
September
December
September
December
20
17
25
19
-35.589
-50.003
- 54.09
- 56.674
6.161
8.290
9.171
9.855
38
35
46
50
-25.205
- 1 1 .037
-31.019
-45.723
4.450
1.962
5.406
7.908
0.274
8.170**
3.404*
12.224**
'•Significant at 99% level of confidence.
'Significant at 95% level of confidence.
744
co
<1>
E
o
>
<0
C
o
2.5
2.0
1.5
-^ Sep. 1980
*---* Sep. 1983
• • Dec. 1980
• • Dec. 1983
6.0 6.1
In (total length-mm)
6.2
1980 were not expected. December is later than the
normal period of sexual activity for males, but the
unexpected gonad volume results may be caused by
delayed mating. The gonad stage data indicated that
male sexual activity was later in 1983 than in 1980.
While fish condition and reproduction were dif-
ferent in 1983 than in the preceding non-El Nino
years, the documentation of such differences for
marine fish is uncommon. The season of parturition
of yellowtail rockfish is more variable than we
realized when the study was designed and the data
on fish condition and gonad volume should have been
collected over a wider period of time. The results
of our study indicate that the assumption of constant
adult fish condition and reproductive effort that is
usually made in models of the population dynamics
of fish is questionable.
5.0
■= 4.0
<D
E
o
>
■D
CO
c
o
3.0
2.0
1.0
* * Sep. 1980
*- — ■* Sep. 1983
• «Dec. 1980
• ^Dec. 1983
5.9 6.0 6.1 6.2 6.3
In (total length-mm)
Figure 2.— Relationships between In (gonad volume) and In (total
length) for yellowtail rockfish in 1980 and 1983. (Top) males;
(bottom) females.
Table 3.— Percent of yellowtail rockfish females with eyed-larvae
observed in samples collected in central and northern California,
1981-1984.
Year
January
February
March
April
May
June
1981
5
0
0
0
0
0
1982
0
15
0
0
0
0
1983
0
18
16
6
0
4
1984
3
10
15
0
0
0
The lower ovary volumes in 1983 than 1980 could
have been related to either delayed parturition
and/or lower reproductive effort. Wootton (1979)
described relationships between feeding conditions
and fish fecundity. The significantly higher gonad
volumes for males in December 1983 compared with
Literature Cited
BOEHLERT, G. W., AND M. M. YOKLAVICH.
1984. Reproduction, embryonic energetics, and the maternal-
fetal relationship in the viviparous genus Sebastes (Pisces:
Scorpaenidae). Biol. Bull. (Woods Hole) 167:354-370.
Guillemot, P. J.
1982. Seasonal cycles of fat content and gonad volume in
species of northern California rockfish (Scorpaenidae;
Sebastes). M.A. Thesis, San Francisco State Univ., San
Francisco, CA, 167 p.
Guillemot, P. J., R. J. Larson, and W. H. Lenarz.
1985. Seasonal cycles of fat and gonad volume in five species
of northern California rockfish (Scorpaenidae;
Sebastes). Fish. Bull., U.S. 83:299-311.
Kleinbaum, D. G., and L. L. Kupper.
1978. Applied regression analysis and other multivariable
methods. Duxbury Press, North Scituate, MA, 556 p.
Lorz, H. V., W. G. Pearcy, and M. Fraidenburg.
1983. Notes on the feeding habits of the yellowtail rockfish,
Sebastes flavidus, off Washington and in Queen Charlotte
Sound. Calif. Fish Game 69:33-38.
Pereyra, W. T., W. G. Pearcy, and F. E. Carvey, Jr.
1969. Sebastodes flavidus, a shelf rockfish feeding on meso-
pelagic fauna, with consideration of the ecological implica-
tions. J. Fish. Res. Board Can. 26:2211-2215.
Phillips, J. B.
1964. Life history studies on ten species of rockfish (genus
Sebastodes). Calif. Dep. Fish Game, Fish Bull. 126, 70 p.
Rasmusson, E. M.
1984. El Nino: the ocean/atmospheric connection. Oceanus
27 (2):5-12.
Wootton, R. J.
1979. Energy costs of egg production and environmental
determinants of fecundity in teleost fishes. Symp. Zool.
Soc. Lond. No. 44, p. 133-159.
William H. Lenarz
Tina Wyllie Echeverria
Southwest Fisheries Center Tiburon Laboratory
National Marine Fisheries Service, NOAA
3150 Paradise Drive
Tiburon, CA 94920
745
DIEL FORAGING ACTIVITY OF
AMERICAN EELS,
ANGUILLA ROSTRATA (LESUEUR),
IN A RHODE ISLAND ESTUARY
Although the American eel, Anguilla rostrata
(LeSueur), is abundant and commercially exploited
along the entire Atlantic coast of North America,
its basic biology is not well understood (Tesch 1977;
Fahay 1978; Helfman et al. 1984). Foraging activity
has not been studied. Helfman et al. (1983) examined
daily movement patterns in an estuary and found,
as had laboratory studies (Bohun and Winn 1966;
Edel 1976; van Veen et al. 1976; Westin and Nyman
1979), that American eel locomotor activity is noc-
turnal and suggested that American eel foraging
activity is also nocturnal. This study sought to
describe the diel foraging patterns of wild estuarine
American eels by monitoring capture rates in baited
eel traps on a 24-h basis.
Eight eel traps were set 10 m apart along a
transect in a tidal portion of the Pettaquamscutt
River estuary, R.I. The water was turbid (the bot-
tom could not be seen at midday in areas <1 m deep)
and the salinity ranged from 20 to 30%u, depend-
ing on the tide. Cylindrical traps are commercially
constructed of 0.64 cm2 wire mesh and are 78 cm
long and 20 cm in diameter with two single funnel
openings of 5 cm in diameter. The traps were baited
with 500-700 g pieces of freshly killed horseshoe
crab, Limulus polyphemus, an effective eel bait
(Bianchini et al. 1981).
Capture rates probably reflected contempor-
aneous foraging because the traps were thought to
have a high escape rate. A high escape rate was
suspected for two reasons: 1) When we changed
from checking the traps once every afternoon to
once every 3 h, the daily capture rate increased near-
ly 50 fold; and 2) when 40 eels were placed into 4
unbaited traps in the river, only 1 eel remained 24
h later. Feeding activity in the traps was evidenced
by several factors: an examination of the gut con-
tent of 10 captured eels found 6 to contain horse-
shoe crab and the rest to be empty, anesthetized
animals frequently regurgitated bait, eels were often
found burrowing in the bait, and unbaited traps rare-
ly caught anything.
Starting at 1200 e.d.t., traps were checked and
rebaited at 3-h intervals for six 24-h periods evenly
spaced over a 15-d span in early September 1982.
This design removed any possible tidal influence
because the lunar tidal period is 14.8 d. Within 10
min of their capture, eels were released 10 m to one
side of the transect' s center point. Traps were
rebaited every 6 h or whenever the bait was found
to have been consumed (which rarely occurred).
Baiting schedules were designed so that every other
trap was rebaited at each 3-h check, and all portions
of the crabs (heads and tails of both males and
females) were equally distributed with respect to
time and location. A total of 322 American eels were
captured (some were probably recaptures): 178 (55%
of the total) were caught just after sunset at 2000
e.d.t., 140 (44%) were caught during the remainder
of the night, and 4 (1%) were caught during daylight
(Fig. 1). Although daily capture rates were variable
and ranged from 113 to 22, all exhibited this pattern.
To determine when foraging activity commenced,
the traps were checked and rebaited at 30-min inter-
vals between 1715 e.d.t. (40 min before sunset) and
2015 e.d.t. for 6 evenings during a 15-d period in
early October. Eels were consistently first captured
just after sunset, with captures peaking 1 h after
sunset and declining thereafter (Fig. 2). Daily cap-
ture totals varied considerably but all exhibited this
60-
50-
X
o
I-
< 40
O
_J
<
h- 30H
I-
z
w 20
o
UJ
a.
10-
N = 322
11 14 17 20 23 2
TIME OF DAY
-1
11
Figure 1.— Percentage of total catch of American eels by time
of day for the 24-h experiment. The histograms cover the time
between checks; i.e., their right boundaries mark the times when
traps were checked. The bold section of the x-axis denotes the
period between sunset and sunrise.
746
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
pattern. A total of 588 American eels were captured,
83% more than in the 24-h experiment, possibly
reflecting the intensity of foraging activity just after
sunset. To characterize the population, eels caught
on the third evening were measured. They had an
average total length of 30.7 cm (SD = 5.4, n = 121),
and 10 of the 121 animals caught had the silvered
pigmentation pattern which characterizes maturing
individuals (Tesch 1977).
These data show that the foraging activity of
estuarine American eels in late summer through
autumn is nocturnal and peaks sharply at nightfall.
Whether the subsequent decline in captures was
caused by a decrease in foraging because of satia-
tion or by an unrelated decline in locomotor activity
cannot be determined. The swimming activity of
unfed eels in the laboratory often exhibits a dramatic
peak at lights-off (Bohun and Winn 1966; Edel 1976;
van Veen et al. 1976). Spring and autumn captures
of wild short-finned New Zealand eels, Anguilla
australis schmidtii, in baited traps displayed the
nocturnal activity pattern described here (Ryan
1984). However, capture patterns in the latter study
changed with the season, as did the locomotor pat-
terns of the yellow European eel, Anguilla anguilla,
studied by Westin and Nyman (1979). Further
research is required to understand the relationship
between foraging and locomotor activity patterns
40-|
X
o
< 30-
O
<
o
20-
UJ
O 10-
K
U
N = 588
17=45 18:45
TIME OF DAY
19 = 45
Figure 2.— Percentage of total catch of American
eels by time of day for the evening experiment. The
histograms cover the time between checks; i.e.,
right boundaries mark the times when traps were
checked. The bold section of the x-axis denotes the
period after sunset.
and how environmental and physiological factors
might influence them.
Literature Cited
BlANCHINI, M., P. W. SORENSEN, AND H. E. WlNN.
1981. Horseshoe crabs as bait for estuarine American eels,
Anguilla rostrata. J. World Maricul. Soc. 12:127-129.
Bohun, S., and H. E. Winn.
1966. Locomotor activity of the American eel (Anguilla
rostrata). Chesapeake Sci. 7:137-147.
Edel, R. K.
1976. Activity rhythms of maturing American eels (Anguilla
rostrata). Mar. Biol. 36:283-289.
Fahay, M. P.
1978. Biological fisheries data on American eel, Anguilla
rostrata (LeSueur). Natl. Mar. Fish. Serv. Sandy Hook
Lab., Highlands, NJ, Rep. 17, 87 p.
Helfman, G. S., D. L. Stoneburner, E. L. Bozeman, P. A.
Christian, and R. Whalen.
1983. Ultrasonic telemetry of American eel movements in a
tidal creek. Trans. Am. Fish. Soc. 112:105-110.
Helfman, G. S., E. L. Bozeman, and E. B. Brothers.
1984. Size, age and sex of American eels in a Georgia river.
Trans. Am. Fish. Soc. 113:132-141.
Ryan, P. A.
1984. Diet and seasonal feeding activity of the short-finned
eel, Anguilla australis schmidtii, in Lake Ellesmere, Canter-
bury, New Zealand. Environ. Biol. Fishes 11:229-234.
Tesch, F.-W.
1977. The eel. Chapman and Hall, Ltd., Lond./J. Wiley &
Sons, N.Y., 434 p. J. Greenwood, translator.
Van Veen, T., H. G. Hartwig, and K. Muller.
1976. Light-dependent motor activity and photonegative
behavior in the eel (Anguilla anguilla L.). J. Comp. Physiol.
111:209-219.
Westin, L., and L. Nyman.
1979. Activity, orientation, and migration of Baltic eel (An-
guilla anguilla L.). Rapp. P. -v. Reun. Cons. int. Explor.
Mer 174:115-123.
Peter W. Sorensen
Graduate School of Oceanography
University of Rhode Island
Narragansett, RI 02882
Present address:
Zoology Department
University of Alberta
Edmonton, Alberta T6G 2E9, Canada
Marco L. Bianchini
Graduate School of Oceanography
University of Rhode Island
Narragansett, RI 02882
Present address:
I.P.R.A., Consiglio Nazionale Delle Ricerche
Via Nizza 128
00188 Roma, Italy
Howard E. Winn
Graduate School of Oceanography
University of Rhode Island
Narragansett, RI 02882
747
FIRST RECORD OF
THE LONGFIN MAKO, ISURUS PAUCUS,
IN THE GULF OF MEXICO
The longfin mako, Isurus paucus, (Guitart-Manday
1966) is a large, pelagic shark that has been reported
from the western Indian, central Pacific, eastern
North Atlantic, and the western North Atlantic
Oceans (Compagno 1984). Guitart-Manday (1975,
cited by Dodrill and Gilmore 1979) described the
longfin mako as a relatively common catch of pelagic
longliners off northwest Cuba. They are usually cap-
tured off the continental shelf at depths of 60-120
fathoms and infrequently at 10-50 fathoms. Dodrill
and Gilmore (1979) reported the first North Ameri-
can continental longfin mako, found beached in the
surf at Melbourne Beach, FL. This paper reports
the first recorded occurrence of the longfin mako
in the Gulf of Mexico.
A large female /. paucus was collected 1 April
1985 by longline fisherman, 80 mi south of Panama
City, FL Gat. 28°55'N, long. 85°35'W) near the sur-
face, over 300 fathoms of water. Standard length
(precaudal length) measured 313.0 cm and fork
length measured 342.0 cm. Total length could not
be measured directly because of the sharks position
on the boat deck and was estimated using a ratio
of total length to fork length (TL/FL = 1.152) cal-
culated from 7 large /. paucus (Harold Pratt1). Using
this ratio, total length was estimated to be ca. 390
cm. Although no embryos were present in the ovi-
duct, this fish appeared reproductively mature. The
oviducts were 3-4 cm in diameter and ovarian eggs
measured 2-3 mm in diameter. Gilmore (1983) pro-
posed the reproductive strategy of /. paucus to be
oviphagous, as remnants of yolk were found in the
digestive tract and mouth of an examined embryo.
The ventral surface of the snout and gill areas of
our shark exhibited a dark grey coloration. Garrick
(1967) reported this coloration as an important
distinguishing characteristic between /. paucus and
the shortfin mako, /. oxyrinchus, which exhibits a
creamy white coloration in that area. Gilmore (1983)
reported the dusky coloration to be more extensive
in larger /. paucus.
Pectoral fin length of our shark measured 80.6 cm.
Gilmore (1983) compared an adult and embryo /.
paucus and found that the pectoral fin length
represented a greater percentage of SL in the em-
bryo (31% of SL) than in the adult (28% of SL). Our
Gulf of Mexico specimen was slightly larger than the
specimen reported by Gilmore (1983) (313.0 cm vs
303.5 cm SL), and the pectoral fin represented 26%
of SL. Guitart-Manday (1966) examined smaller /.
paucus— 195, 203, and 226 cm TL— and found pec-
toral fin length as percent total length to be 30.4%,
30.0%, and 29.2%, respectively. For this specimen,
pectoral fin length as percent TL was about 21%.
It appears that as /. paucus increase in length, the
pectoral fins do not increase proportionately, result-
ing in reduced pectoral length to total length ratios
in larger sharks.
This record suggests that the longfin mako at least
occurs infrequently in the northern Gulf of Mexico.
Three male /. paucus (191, 193, and 220 cm SL) cap-
tured 16 April 1985 off the Mississippi River (lat.
27°35'N, long. 89°55'W) further supports this sug-
gestion (Stephen Branstetter2). These captures ex-
tend the known range of this species well into the
northern Gulf of Mexico.
Acknowledgments
We would like to extend a most sincere thanks to
Lew Bullock of the Florida Department of Natural
Resources for his help in examining this shark. We
are grateful to Stephen Branstetter and Wes Pratt
for reviewing the manuscript and providing unpub-
lished data.
Literature Cited
Compagno, L. J. V.
1984. FAO species catalogue. Vol. 4. Sharks of the world. An
annotated and illustrated catalogue of sharks species known
to date. Part 1. Hexanchiformes to Lamniformes.
FAO Fish. Synop. 125, Vol. 4(Pt. 1), 249 p.
Dodrill, J. W., and R. G. Gilmore.
1979. First North American continental record of the longfin
mako (Isurus paucus Guitart-Manday). Fla. Sci. 42:52-58.
Garrick, J. A. F.
1967. Revision of sharks of genus Isurus with description of
a new species (Galeoidea, Lamnidae). Proc. U.S. Natl. Mus.
118:663-690.
Gilmore, R. G.
1983. Observations on the embryos of the longfin mako,
Isurus paucus and the bigeye thresher, Alopias super cili-
osus. Copeia 1983:375-382.
Guitart-Manday, D.
1966. Nuevo nombre para una especie de tibur6n del genero
Isurus (Elasmobranchii:Isuridae) de aguas Cubanas. Poe-
yana Ser. A, No. 15, 9 p.
1975. Las pesquerias pelagico-oceanicas de corto radio de ac-
tion en la region noroccidental de Cuba. Oceanogr. Inst.,
'Harold Pratt, Northeast Fishery Center Narragansett Labora-
tory, National Marine Fisheries Service, NOAA, South Ferry
Road, Narragansett, RI 02882-1199, pers. commun. June 1985.
2Stephen Branstetter, Department of Wildlife and Fisheries
Science, Texas A&M University, College Station, TX 77843-2258,
pers. commun. August 1985.
748
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
Acad. Sci., Havana, Cuba. Ser. Oceanologica, p. 1-41.
Kristie Killam
Glenn Parsons
Department of Marine Science
University of South Florida at St. Petersburg
HO 7th Avenue South
St. Petersburg, FL 33701
MOVEMENT OF SEA-RUN SEA LAMPREYS,
PETROMYZON MARINUS, DURING
THE SPAWNING MIGRATION IN
THE CONNECTICUT RIVER1
Adult sea lampreys, Petromyzon marinus, first
enter New England rivers in late March and early
April (Bigelow and Schroeder 1953). The only infor-
mation on river water temperatures during the
migration were collected in 1974 from the St. John
River, New Brunswick, where Beamish and Potter
(1975) captured the first prespawning adults in a fish
lift at Mactaquac Dam (river km 140) at 13° C in mid-
June and the run peaked at 17°-19°C. Because
thousands of sea lampreys are annually passed up-
stream of Holyoke Dam (river km 140) on the Con-
necticut River, the passage records provide an ideal
opportunity to characterize the run relative to tem-
perature. River flow was partially or totally con-
trolled by the hydroelectric facilities at the dam, so
we did not examine the effects of flow on the run.
The behavior and rate of movement of landlocked
sea lampreys in the Great Lakes was determined
using mark and recapture of adults at stream weirs
(Applegate 1950; Applegate and Smith 1950; Smith
and Elliot 1952; Moore et al. 1974). The only esti-
mate of the rate of movement of sea-run sea lam-
preys was done by Beamish (1979) who used the
energy expended during an upstream movement to
estimate the distance traveled and the rate of move-
ment of adults in the St. John River. Because this
estimate of the rate of movement was not verified
by direct observations on fish in the field, we be-
lieved that additional study was necessary. We
selected radio telemetry to determine the rate of
movement and diel behavior of sea lampreys. The
Contribution No. 101 of the Massachusetts Cooperative Fishery
Research Unit, which is supported by the U.S. Fish and Wildlife
Service, Massachusetts Division of Fisheries and Wildlife, Mass-
achusetts Division of Marine Fisheries, and the University of
Massachusetts.
abundance, size, and sex ratio of the Connecticut
River population were reported by Stier and Kynard
(1986).
Methods
Radio-tagged sea lampreys were observed in the
46 km stretch of the Connecticut River from Brun-
elle's Marina to Cabot Station, a hydroelectric facil-
ity located 4.5 km below Turners Falls Dam (Fig.
1). The downstream half of this stretch flows slow-
ly, creating a deep channel and shoals; the upstream
half flows swiftly with pools and riffles. Major
spawning areas are in the upper main-stem near
Cabot Station, Russelville Brook, and the Fort, Mill,
Sawmill, and Deerfield Rivers (Fig. 1).
The number of sea lampreys passed daily by the
fish lifts from 1980 to 1983 were counted by per-
sonnel of the Massachusetts Cooperative Fishery
Research Unit. Daily maximum river temperature
was recorded at Holyoke Dam.
Sea lampreys were captured in the trap at the fish
lifts during May and June 1982, measured for total
length, and held for <24 h in a 1,325 L circular tank
supplied with river water. We anesthetized fish with
MS-222 (1:20,000) and tagged them first with a Floy
tag inserted through the posterior dorsal fin, and
second with a transmitter placed on the left side of
the body along the first dorsal fin. Sex could not be
accurately determined visually.
Cylindrical radio transmitters were constructed
from the design of Knight (1975) and operated at
a frequency of 30.05-30.25 MHz. Tags measured 34
x 10 mm, weighed 3.5-4.5 g in air, and transmitted
for about 20 d. Each fish was identified by frequency
and pulse rate. We located fish to within about 10
m, using receivers equipped with an omnidirectional,
1/8- wave antenna and a directional, tuned-loop
antenna.
We released two to six^sea lampreys at a time and
observed them continuously for >6 h or until dark-
ness. Subsequently, sea lampreys were located each
day until they reached Cabot Station or entered a
tributary. During all surveys, we noted the locations
of fish to the nearest river kilometer. Diel movement
was monitored for five 24-h periods. Additional fish
were released during the day for this study.
Results and Discussion
The water temperatures, and the year in paren-
theses, when sea lampreys first entered the fish lifts
were 12.5°C (1980), 10.5°C (1981), 12.5°C (1982),
and 15.5°C (1983) (Fig. 2). The lifts sampled the en-
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
749
Turners Falls Dam
km 198
Figure 1.— Section of the Connecticut River from river km 140 to 198, showing the loca-
tions of the Holyoke and Turners Falls Dams, the release site for radio-tagged sea lampreys
at Brunelle's Marina, and the major spawning tributaries between the two dams.
tire run each year except in 1981 when sea lampreys
were present in the first lifts of the year (the lifts
began operating on 29 or 30 April of each year). Dur-
ing the peak 7 d, the temperature ranges, and year
in parentheses, were 16°-19°C (1980), 17°-19°C
(1981), 16°-17°C (1982), and 17°-21°C (1983).
Movement into the fish lift ceased at 24°C in 1983
and at 21°-22°C in the other years (Fig. 2).
Information on the maximum daily temperature
during the migration of landlocked sea lampreys in
a large river comes from the Ocqueoc River (Lake
Huron drainage) which for some years supported an
annual run of 25,000-40,000 (Applegate 1950; Apple-
gate and Smith 1950). The temperatures, and date
in parentheses, when the first sea lampreys entered
a weir near the mouth of the river were 10°C (27
April 1949) and 6°C (11 May 1950); and the run
peaked at 14°-17°C (first week of May 1949) and
18° -20°C (third week of May 1950). Most movement
at the weir ceased at 21 °C (about 11 July), but dur-
ing both years one or two sea lampreys per day con-
tinued to enter the weir throughout the summer at
22°-26°C.
The temperature regimes in the Ocqueoc and Con-
necticut Rivers during the peak and at the end of
the principal migration were in general agreement.
Runs peaked at 14° -20°C in the Ocqueoc River and
16° -21 °C in the Connecticut River; most of the run
ceased at 21 °C in the Ocqueoc River and at
21°-24°C in the Connecticut River. The migrations
differed because a few adults in the Ocqueoc River
continued to migrate throughout the summer,
whereas none were captured after 25 June during
3 yr in the Connecticut River. Therefore, even
750
15
h-
10
z
Ld
5
O
cr
0
Ld
Ql
35
i
30 5
APRIL
15 20 25 30
MAY
10 15 20 25 30 5 10
JUNE JULY
Figure 2.— Daily percent of total sea lampreys lifted at the Holyoke fish lifts each year, 1980-83. Temperatures are the daily
maximum river temperatures. The lifts began operating about 1 May in all years and ceased about 15 July. Wavy line near the
base of each panel identifies days on which the lifts were not operated.
751
though the data from the two runs differed greatly
in time and space, the general migration pattern in
relation to river temperature was remarkably
similar.
The behavior of the sea lampreys in the St. Johns
and Connecticut Rivers also appeared similar. In
1974, the first migrants were collected at 13°C at
the Mactaquac fish lift (Beamish and Potter 1975),
and from 1980 to 1983 the first migrants were
passed in the Holyoke fish lift at 10.5° -15.5°C. The
peak of the run was also similar— 17°-19°C in the
St. Johns River and 16°-21°C in the Connecticut
River.
Mean length of the 45 sea lampreys tagged was
73.2 cm (range, 63.0-80.0 cm). Five were not re-
located either because the tag failed or the fish
moved downstream over the dam. No tagged sea
lamprey died during the study. The remaining 40
fish were followed for a total of 224 h during 24 d
(12 May-4 June; Fig. 3). Since sea lampreys mi-
grated upstream at Holyoke until 30 June 1982 (Fig.
2), for the most part we observed the movement of
early migrants. During the study, water tempera-
ture increased from 13° to 22 °C; river discharge
gradually decreased from 60.4 m3/s on 12 May to
50.9 m3/s on 31 May. Twenty sea lampreys moved
>23 km and 4 reached Cabot Station. Nineteen were
last located near the mouths of the Fort or Mill
Rivers or Russelville Brook (Fig. 1). Spawning of
tagged fish was verified in the tributaries— an in-
dication that normal behavior resumed after the sea
lampreys were tagged.
Sea lampreys moved upstream at ground speeds
of 0.1-3.5 km/h. The daily mean rate of movement
including rest periods was 1.01 km/h ± 0.75 (mean
±SD; range, 0.1-2.7 km/h; N = 40) or 0.4 body
length/s. The mean rate, excluding rest periods, was
1.51 km/h ± 0.53 (range, 0.1-3.5 km/h; N = 39) or
0.6 body length/s. Early migrants moved a mean of
0.1-1.2 km/h; and three migrants that were observed
during the peak passage at the fish lift on 2 June
had the fastest mean daily rate of 2 km/h (Fig.
3).
Among landlocked sea lampreys, early migrants
have a slower rate of movement than peak migrants
because they rest more (Applegate 1950; Skidmore
1959; Larsen 1980). Our observations during the
peak period after 30 June did not indicate a sus-
tained increase in the rate of movement (Fig. 3).
Because we only observed a few peak migrants,
additional study is necessary to compare the rates
of movement between early and peak migrants.
The movement rates of sea lampreys in the Con-
necticut River were the highest reported for the
species. Landlocked sea lampreys moved at much
lower rates of 0.02-0.21 km/h (Applegate and Smith
1950; Skidmore 1959; Wigley 1959). Beamish (1974)
found a maximum swimming speed of 1.08 km/h (30
cm/s) for landlocked adults in the laboratory. Using
the energetics of adult sea-run sea lampreys dur-
ing a 35-d upstream move into the fish lift at Mac-
taquac Dam on the St. John River, Beamish (1979)
estimated the rate to be 0.23 km/h for males and
0.26 km/h for females, or 0.1 body length/s for both.
This rate was similar to that of the landlocked form.
Because the sea-run adults are much larger than
landlocked adults, they should swim faster. Our
results suggest that the 0.2 km/h rate which was
estimated for the St. John River adults may be in-
correct, possibly because the fish were delayed
ii
2
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E
Ld
cr o
23446474845222431 634312
t
\\\
-X l_l l_J_
X
J„
J i I i L_. L
12 14 16 18 20 22 24 26 28 30 I 3
MAY JUNE
Figure 3.— Daily mean rates of movement of radio-tagged sea lampreys (open circles). (Vertical lines
show standard errors; numbers of lampreys monitored are shown above each mean.)
752
several days before finding the entrance to the fish
lift at Mactaquac Dam.
Diel movement rates were monitored on 13 and
17 May (early migrants) and 26 and 30 May and 1
June (peak migrants). Movement was slowest from
1200 to 1700 h (Fig. 4). Nocturnal behavior was
strongest among the early migrants; peak migrants
had a higher rate of movement because they also
moved during the day (mornings only). A similar pat-
tern for landlocked adults was found by Kleerekoper
et al. (1961).
In summary, except for the longer summer migra-
tion and the slower rate of upstream movement, the
behavior of sea-run sea lampreys in the Connecticut
and St. Johns Rivers was similar to that of the land-
locked sea lampreys in the Ocqueoc River. The
timing of the runs in relation to temperature and
the diel movement patterns appears very stable,
probably with important survival or reproductive
advantages.
2400
0500
1200
1700
2000
to
to
to
to
to
0500
1200
1700
2000
2400
HOUR
Figure 4.— Mean movement rates of early migrants (solid circles)
monitored 13 and 17 May (N = 13), and peak migrants (open
circles) monitored 26 and 30 May and 1 June 1982 (N = 7). (Ver-
tical lines show standard errors.)
Acknowledgments
We thank D. Stier, A. Richmond, J. Nicholson, T.
Clifford, C. Hall, J. Burnett, J. Bain, and J. Idoine
for assistance with field work. The project was
funded by Federal Aid Project AFS-4-R-21 and
Dingell-Johnson Project 5-29328 to the Massachu-
setts Cooperative Fishery Research Unit. We thank
Holyoke Water Power Company for providing space
for the holding tanks.
Literature Cited
Applegate, V. C.
1950. Natural history of the sea lamprey, Petromyzon mari-
nus, in Michigan. U.S. Fish Wildl. Serv., Spec. Sci. Rep.
Fish. 55, 237 p.
Applegate, V. C, and B. R. Smith.
1950. Sea lamprey spawning runs in the Great Lakes in 1950.
U.S. Fish Wildl. Serv., Spec. Sci. Rep. Fish. 61, 49 p.
Beamish, F. W. H.
1974. Swimming performance of adult sea lamprey, Petro-
myzon marinus, in relation to weight and temperature.
Trans. Am. Fish. Soc. 103:355-358.
1979. Migration and spawning energetics of the anadromous
sea lamprey, Petromyzon marinus. Environ. Biol. Fishes
4:3-7.
Beamish, F. W. H., and I. C. Potter.
1975. The biology of the anadromous sea lamprey (Petro-
myzon marinus) in New Brunswick. J. Zool. (Lond.) 177:
57-72.
Bigelow, H. B., and W. C. Schroeder.
1953. Fishes of the Gulf of Maine. U.S. Fish Wildl. Serv.,
Fish. Bull. 53:1-577.
Kleerekoper, H., G. Taylor, and R. Wilton.
1961. Diurnal periodicity in the activity of Petromyzon mari-
nus and the effects of chemical stimulation. Trans. Am.
Fish. Soc. 90:73-78.
Knight, A. E.
1975. A tuned-antenna radio telemetry tag for fish. Under-
water Telem. Newsl. 5:13-16.
Larsen, L. 0.
1980. Physiology for adult lampreys, with special regard to
natural starvation, reproduction, and death after spawning.
Can. J. Fish. Aquat. Sci. 37:1762-1779.
Moore, H. H., F. H. Dahl, and A. K. Lamsa.
1974. Movement and recapture of parasitic phase sea lam-
preys (Petromyzon marinus) tagged in the St. Marys River
and Lakes Huron and Michigan, 1963-67. Great Lakes Fish.
Comm. Tech. Rep. 27, 19 p.
Skidmore, J. F.
1959. Biology of spawning-run sea lampreys (Petromyzon
marinus) in the Pancake River, Ontario. M.S. Thesis, Univ.
Western Ontario, London, Ont., 87 p.
Smith, B. R., and 0. R. Elliott.
1952. Movement of parasitic-phase sea lampreys in Lakes
Huron and Michigan. Trans. Am. Fish. Soc. 82:123-128.
Stier, K., and B. Kynard.
1986. Abundance, size, and sex ratio of adult sea-run sea lam-
prey, Petromyzon marinus, in the Connecticut River. Fish.
Bull., U.S. 84:476-480.
Wigley, R. L.
1959. Life history of the sea lamprey of Cayuga Lake, New
York. U.S. Fish Wildl. Serv., Fish. Bull. 59:559-617.
Kathleen Stier
Boyd Kynard
Massachusetts Cooperative Fishery Research Unit
University of Massachusetts
204 Holdsworth Hall
Amherst, MA 01003
753
VARIATIONS IN THE MORPHOLOGY OF
FISTULICOLA PLICATUS RUDOLPHI (1802)
(CESTODA:PSEUDOPHYLLIDEA) FROM
THE SWORDFISH, XIPHIAS GLADIUS L.,
IN THE NORTHWEST ATLANTIC OCEAN
During the course of a survey of the helminth
parasites of the swordfish, Xiphias glasius L., from
the Northwest Atlantic Ocean, several morpholo-
gical variations were observed in specimens of the
pseudophyllidean tapeworm, Fistulicola plicatus.
The most notable of these variations were pseudo-
scolex form and proglottid shape and size. Methods
of scolex attachment to the organ wall, descriptions
of pseudoscolex structures, and organ specific varia-
tions in the morphology of F. plicatus are given.
Materials and Methods
A sample of 303 gills and gastrointestinal tracts
of swordfish was collected from four geographical
areas in the Northwest Atlantic Ocean in the late
summer and early fall of 1980. The areas sampled
and the number of swordfish collected from each
geographical area are as follows: Cape Hatteras (74),
Georges Bank (90), Scotian Shelf (69), and Grand
Bank (70); all collected by longline gear and frozen
at sea. The swordfish were later dissected and ex-
amined for helminth parasites in the laboratory.
Pseudophyllidean cestodes were removed from
the infected organ and fixed whole in 70% alcohol
or 10% Formalin1. Several infected organs were
fixed whole in Bouin's fluid or 10% Formalin. Speci-
mens used for taxonomic examinations were stained
in Erlich's hematoxylin, Blachin's lactic acid car-
mine, or Semichon's aceto-carmine. Camera lucida
drawings were made from fixed, unstained speci-
mens.
Results
Fistulicola plicatus has been reported from the
swordfish by Linton (1901), Cooper (1918), Nigrelli
(1938), and lies (1970). In this study F. plicatus was
found in the intestines and recturns of swordfish
from all four sampling areas. Considerable morpho-
logical variation was found between individuals of
this species. Variations were in scolex form, overall
parasite length, and proglottid shape and size. About
50% of specimens recovered exhibited a scolex and
proglottid structure characteristic of specimens
'Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
described by Yamaguti (1959). Scolices from these
were arrow-shaped and possessed two simple, leaf-
shaped bothridia (Fig. 1). Any variation from this
scolex form were considered to be pseudoscolices.
Proglottids from specimens described by Yamaguti
(1959) were short and broad with foliate lateral
edges. Internal proglottid morphology was not easily
seen in any of the specimens examined during the
present study, although nerve trunk location (near
lateral margins), cirrus-sac and vagina location (on
opposite lateral margins), and egg shell structure
(thick-shelled and operculate) were occasionally
observable.
A total of 29 specimens recovered had penetrated
the wall of the infected organ. Occasionally the
tapeworms penetrated the organ wall and retained
typical scolex form, i.e., arrow-shaped with simple,
well-developed bothridia but, in the majority of
cases, complete perforation of the organ wall re-
sulted in the formation of a pseudoscolex. Attach-
ment to the organ wall (rectum and intestine) was
achieved in the following four ways:
1) By complete perforation of the organ wall, the
scolex and a portion of the neck encapsulated
in a rounded, host-produced cyst attached to
the organ serosa. Scolices recovered from
these cysts were usually arrow-shaped with
typical bothridia, or occasionally found as a
round, transparent, fluid-filled bag, which pos-
sessed rudimentary or no apparent bothridia
(Fig. 2).
2) By complete perforation of the organ wall, the
scolex and a portion of the neck encased in a
tubular, host-produced sheath, attached along
its entire length to the organ serosa. Occa-
sionally this sheath was entwined with the
mesenteries associated with the infected organ.
Pseudoscolices found within these sheaths
were long, rounded, and slender, and exhibited
no bothridia (Fig. 3).
3) By complete penetration of the organ wall, the
scolex markedly enlarged (up to 6 cm in
length), lying free, and unencapsulated in the
peritoneal cavity. Pseudoscolices of this type
were long, broad, pseudosegmented, and pos-
sessed well-developed bothridia (Fig. 4).
4) In this case the scolex did not fully penetrate
the organ wall, but perforated the wall to a
slight depth, and remained in that position.
Often specimens were found to exhibit this
slight organ wall penetration and re-emerge in-
to the lumen of the organ. In these cases the
754
FISHERY BULLETIN: VOL. 84, NO. 3, 1986.
4mm
0.5cm
L
1.0cm
Figure 1.— Typical scolex from Fistulicola plicatus, as described and figured by Yamaguti (1959).
Figure 2.— Pseudoscolex (1st type).
Figure 3.— Pseudoscolex (2d type).
Figure 4.— Pseudoscolex (3d type).
755
1) scolex type described by Yamaguti (1959) was
retained.
Fistulicola plicatus specimens recovered from the
lumen of the intestines were morphologically dif-
ferent from those collected from the rectum. They
were long, up to 1 m in length, and exhibited longer,
less-broad strobila than those characteristic of the
rectal forms. All specimens of F. plicatus recovered
from the anterior portion of the intestine exhibited
the previously described first type of scolex attach-
ment to the organ wall, i.e., the scolex perforated
the organ wall and was encapsulated in a rounded,
host-produced cyst attached to the intestinal serosa.
The scolex penetrated the anterior portion of the
intestine, with the strobila projecting posterior
through the length of the organ. Very small F.
plicatus were found in the posterior portion of the
intestine. These exhibited shallow penetration by an
unmodified scolex.
Fistulicola plicatus specimens found in the rec-
tum of swordfish were usually <20 cm in length and
possessed very broad strobila. These rectal forms
exhibited all of the previously described types of
scolex attachment and structure, penetrating the
organ wall near the rectal sphincter (Fig. 5). Occa-
sionally, several tapeworms were found with their
necks passing through a single perforation of the
rectal wall, their scolices jointly encapsulated in a
rounded serosal cyst.
Discussion
Apex type predators such as the swordfish eat and
digest large amounts of prey species and, conse-
quently, the intestines and rectums of these fish
exhibit high levels of muscular activity. Without per-
foration of the organ wall (by the scolex and neck),
many tapeworms would probably be voided with the
faeces. The development of the pseudoscolex is an
adaptation for anchoring the simple, unarmed scolex
to the organ wall. It is clear that F. plicatus secretes
a powerful digestive enzyme which enables the
scolex to penetrate the very muscular walls of the
intestine and rectum of swordfish. lies (1970) found
many examples of pseudoscolex variation in 24
specimens from swordfish in the Northwest Atlan-
tic Ocean. Several of these variations are similar to
those found in this study. It is obvious from this
study, and studies such as lies (1970), that F.
plicatus is a very adaptable tapeworm and will
develop any pseudoscolex structure which is neces-
Figure 5. —Fistulicola plicatus (in situ) from rectum of Xiphias gladius.
756
sary to anchor itself to the organ wall. Large
samples of swordfish intestines and rectums will in-
variably show many variations in the pseudoscolex
structure of F. plicatus.
Acknowledgments
We thank L. S. Uhazy for initiating the study of
these parasites, C. lies for comments on the manu-
script, P. W. G. McMullon for advice on figures, and
B. Garnett for preparing the typescript.
Literature Cited
Cooper, A. R.
1918. North American pseudophyllidean cestodes from fishes.
III. Biol. Monogr. 4:1-243.
Iles, C.
1970. A preliminary investigation of the parasites of the gills
and gastrointestinal tract of the swordfish Xiphias gladius
L. from the Northwest Atlantic. J. Fish. Res. Board Can.
MS Rep. Ser. 1092, 11 p.
Linton, E.
1901. Parasites of fishes of the Woods Hole region. Bull.
U.S. Fish. Comm. 19:405-492.
Nigrelli, R. F.
1938. Parasites of the swordfish, Xiphias gladius Linnaeus.
Am. Mus. Novit. 996:1-16.
Yamaguti, S.
1959. Systema helminthum. Vol. 2. The cestodes of verte-
brates. Intersci. Publ., N.Y., 860 p.
W. E. Hogans
Identification Centre
Department of Fisheries and Oceans
Biological Station
St. Andrews, Nova Scotia E0G 2X0, Canada
Marine Fish Division
Bedford Institute of Oceanograph
Department of Fisheries and Oceans
P.O. Box 1006
Dartmouth, Nova Scotia B2Y JfA2, Canada
P. C. F. Hurley
757
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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)
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Fishery Bulletin
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Contents— Continued
ROGERS, S. GORDON, HIRAM T. LANGSTON, and TIMOTHY E. TARGETT. Ana-
tomical trauma to sponge-coral reef fishes captured by trawling and angling .... 697
QUAST, JAY C. Annual production of eviscerated body weight, fat, and gonads by
Pacific herring, Clwpea harengus pallasi, near Auke Bay, southeastern Alaska. . . 705
WENNER, CHARLES A., WILLIAM A. ROUMILLAT, and C. WAYNE WALTZ. Con-
tributions to the life history of Black sea bass, Centropristis striata, off the south-
eastern United States 723
Notes
LENARZ, WILLIAM H., and TINA WYLLIE ECHE VERRIA. Comparison of visceral
fat and gonadal fat volumes of yellowtail rockfish, Sebastesjlavidus, during a normal
year and a year of El Nino conditions 743
SORENSEN, PETER W, MARCO L. BIANCHINI, and HOWARD E. WINN. Diel
foraging activity of American eels, Anguilla rostrata (Lesueur), in a Rhode Island
estuary 746
KILLAM, KRISTIE, and GLENN PARSONS. First record of the longfin mako, Isurus
paucus, in the Gulf of Mexico 748
STIER, KATHLEEN, and BOYD KYNARD. Movement of sea-run sea lampreys, Petro-
myzon marinus, during the spawning migration in the Connecticut River 749
HOGANS, W E., and P. C. F. HURLEY. Variations in the morphology of Fistulicola
plicatus Rudolphi (1802) (Cestoda:Pseudophyllidea) from the swordfish, Xiphias gladius
L., in the Northwest Atlantic Ocean 754
• GPO 593-096
^O'Cq,
S*TES O* *
Fishery Bulletin
LIBRA*
Vol. 84, No. 4
'i«L* !-; .
October 1986
POLOVINA, JEFFERY J., and STEPHEN RALSTON. An approach to yield assessment
for unexploited resources with application to the deep slope fishes of the Marianas. . 759
YANG, W. T, R. F. HIXON, P. E. TURK, M. E. KREJCI, W. H. HULET, and R T.
HANLON. Growth, behavior, and sexual maturation of the market squid, Loligo
opalescens, cultured through the life cycle 771
BODKIN, JAMES LEE. Fish assemblages in Macrocystis and Nereocystis kelp forests
of central California 799
STEPIEN, CAROL A. Life history and larval development of the giant kelpfish, Hetero-
stiehus rostratus Girard, 1854 809
PAULY, DANIEL. A simple method for estimating the food consumption of fish popu-
lations from growth data and food conversion experiments 827
FINUCANE, JOHN H., L. ALAN COLLINS, HAROLD A. BRUSHER, and CARL H.
SALOMAN. Reproductive biology of king mackerel, Scomberomorus cavalla, from the
southeastern United States 841
FARLEY, C. A., S. V. OTTO, and C. L. REINISCH. New occurrence of epizootic sarcoma
in Chesapeake Bay soft shell clams, Mya arenaria 851
FOLKVORD, ARILD, and JOHN R. HUNTER. Size-specific vulnerability of northern
anchovy, Engraulis mordax, larvae to predation by fishes 859
SMITH, JOSEPH W, and JOHN V. MERRINER Observations on the reproductive biology
of the cownose ray, Rhinoptera bonasus, in Chesapeake Bay 871
McGOWAN, MICHAEL F Northern anchovy, Engraulis mordax, spawning in San Fran-
cisco Bay, California, 1978-79, relative to hydrography and zooplankton prey of adults
and larvae 879
HUNTER, J. ROE, BEVERLY J. MACEWICZ, and JOHN R. SIBERT. The spawning
frequency of skipjack tuna, Katsuwonus pelamis, from the South Pacific 895
HOUDE, EDWARD D, and LAWRENCE LUBBERS III. Survival and growth of striped
bass, Morone saxatilis, and Morone hybrid larvae: laboratory and pond enclosure
experiments 905
DAILEY, MURRAY D, and STEPHEN RALSTON. Aspects of the reproductive biology,
spatial distribution, growth, and mortality of the deepwater caridean shrimp, Heterocarpus
laevigatas, in Hawaii 915
RALSTON, STEPHEN. An intensive fishing experiment for the caridean shrimp, Hetero-
carpus laevigatus, at Alamagan Island in the Mariana Archipelago 927
DITTY, JAMES G. Ichthyoplankton in neritic waters of the northern Gulf of Mexico off
Louisiana: composition, relative abundance, and seasonality 935
(Continued on back cover)
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Fishery Bulletin
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SCIENTIFIC EDITOR, Fishery Bulletin
Dr. William J. Richards
Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service, NOAA
Miami, FL 33149-1099
Editorial Committee
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National Marine Fisheries Service National Marine Fisheries Service
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Fishery Bulletin
CONTENTS
Vol. 84, No. 4 October 1986
POLOVINA, JEFFERY J., and STEPHEN RALSTON. An approach to yield assessment
for unexploited resources with application to the deep slope fishes of the Marianas. . 759
YANG, W. T, R. F. HIXON, P. E. TURK, M. E. KREJCI, W. H. HULET, and R. T.
HANLON. Growth, behavior, and sexual maturation of the market squid, Loligo
opalescens, cultured through the life cycle 771
BODKIN, JAMES LEE. Fish assemblages in Macrocystis and Nereocystis kelp forests
of central California 799
STEPIEN, CAROL A. Life history and larval development of the giant kelpfish, Hetero-
stichus rostratus Girard, 1854 809
PAULY, DANIEL. A simple method for estimating the food consumption of fish popu-
lations from growth data and food conversion experiments 827
FINUCANE, JOHN H., L. ALAN COLLINS, HAROLD A. BRUSHER, and CARL H.
SALOMAN. Reproductive biology of king mackerel, Scomberomorus cavalla, from the
southeastern United States 841
FARLEY, C. A., S. V. OTTO, and C. L. REINISCH. New occurrence of epizootic sarcoma
in Chesapeake Bay soft shell clams, Mya armaria 851
FOLKVORD, ARILD, and JOHN R. HUNTER. Size-specific vulnerability of northern
anchovy, Engraulis mordax, larvae to predation by fishes 859
SMITH, JOSEPH W., and JOHN V. MERRrNER. Observations on the reproductive biology
of the cownose ray, Rhinoptera bonasus, in Chesapeake Bay 871
McGOWAN, MICHAEL F Northern anchovy, Engraulis mordax, spawning in San Fran-
cisco Bay, California, 1978-79, relative to hydrography and zooplankton prey of adults
and larvae 879
HUNTER, J. ROE, BEVERLY J. MACEWICZ, and JOHN R. SIBERT The spawning
frequency of skipjack tuna, Katsuwonus pelamis, from the South Pacific 895
HOUDE, EDWARD D, and LAWRENCE LUBBERS III. Survival and growth of striped
bass, Morone saxatilis, and Morone hybrid larvae: laboratory and pond enclosure
experiments 905
DAILEY, MURRAY D, and STEPHEN RALSTON. Aspects of the reproductive biology,
spatial distribution, growth, and mortality of the deepwater caridean shrimp, Heterocarpus
laevigatus, in Hawaii 915
RALSTON, STEPHEN. An intensive fishing experiment for the caridean shrimp, Hetero-
carpus laevigatus, at Alamagan Island in the Mariana Archipelago 927
DITTY, JAMES G Ichthyoplankton in neritic waters of the northern Gulf of Mexico off
Louisiana: composition, relative abundance, and seasonality 935
(Continued on next page)
Seattle, Washington
1986
^■riaa B^W^jmJ I -*- *--
M9KN DM^ni UUUI41W
LIBRARY
JAN 29 1987
-oas 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
REXSTAD, ERIC A., and ELLEN K. PIKITCH. Stomach contents and food consump-
tion estimates of Pacific hake, Merluccius productus 947
PEREZ, MICHAEL A., and MICHAEL A. BIGG. Diet of northern fur seals, Callorhmus
ursinus, off western North America 957
TESTER, PATRICIA A., and ANDREW G. CAREY, JR. Instar identification and life
history aspects of juvenile deepwater spider crabs, Chionoecetes tanneri Rathbun . . . 973
Notes
CODY, TERRY J., and BILLY E. FULS. Comparison of catches in 4.3 m and 12.2 m shrimp
trawls in the Gulf of Mexico 981
POWELL, ALLYN B., and GERMANO PHONLOR. Early life history of Atlantic men-
haden, Brevoortia tyrannus, and gulf menhaden, B. patronus 991
PODNIESINSKI, GREG S., and BERNARD J. McALICE. Seasonality of blue mussel,
Mytilus edulis L., larvae in the Damariscotta River estuary, Maine, 1969-77 995
Index 1003
Notices 1017
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 ap-
proves, recommends or endorses any proprietary product or proprietary material
mentioned herein, or which has as its purpose an intent to cause directly or indirect-
ly the advertised product to be used or purchased because of this NMFS publication.
AN APPROACH TO YIELD ASSESSMENT FOR UNEXPLOITED RESOURCES
WITH APPLICATION TO THE DEEP SLOPE FISHES
OF THE MARIANAS
Jeffrey J. Polovina and Stephen Ralston1
ABSTRACT
A comprehensive approach to estimate the maximum sustainable yield (MSY) for a tropical multispecies
resource which lacks catch and effort data is presented. This yield assessment approach was used to
design a fishery resource assessment survey of the Mariana Archipelago. An application of the method
is presented to estimate the MSY for a multispecies bottom fish resource, based on data collected during
the survey. The annual MSY for the deep slope fishes (primarily snappers and groupers) of the Mariana
Archipelago is estimated to be 109 t, which for comparative purposes is equivalent to 222 kg/nmi of 200
m isobath or 0.3 t/km .
Assessment of tropical resources has always created
major problems in fisheries research (Saila and
Roedel 1979; Pauly and Murphy 1982). This has
been largely due to three factors: technical dif-
ficulties in aging, a high species diversity in tropical
communities, and what is typically a multiplicity of
artisanal gears used in these fisheries. The latter
problem has been especially difficult to surmount,
making it difficult to determine not only the level
of fishing effort but sometimes even the total
catch. Without these data many standard fish-
eries techniques such as stock-production methods
are inapplicable (but see Csirke and Caddy
1983).
In recent years, however, new methods and
modifications of existing methods have been pro-
posed to estimate growth and mortality parameters,
standing crop, and yield for fish stocks in the
absence of a time series of commercial catch and ef-
fort data (Beddington and Cooke 1983; Pauly 1983;
Polovina 1986a; Wetherall et al. in press). We will
show that several of these techniques can be com-
bined, producing an integrated approach to yield
assessment designed specifically for tropical
fisheries resources in situations where catch and ef-
fort data are lacking. The approach is then applied
to data gathered in a fishery survey of the Mariana
Archipelago to estimate maximum sustainable yield
(MSY) for a multispecies resource of deep slope
snappers and groupers.
'Southwest Fisheries Center Honolulu Laboratory, National
Marine Fisheries Service, NOAA, 2570 Dole Street, Honolulu, HI
96822-2396.
YIELD ASSESSMENT
The equilibrium yield assessment is presented
schematically in Figure 1. This approach assumes
that growth follows the deterministic von Berta-
lanffy curve with parameters K and Lx, that the
mortality of fish above the smallest length fully
represented in the catch (Lc) occurs at a constant
instantaneous rate (Z), and that recruitment is con-
stant with R recruits entering the first vulnerable
age class annually. It is also assumed that the
resource is essentially pristine, such that an estimate
of the biomass recruited to the fishery in the absence
of exploitation (B^) can be obtained from a catch-
per-unit-effort (CPUE) survey and an estimate of
catchability. In the discussion section, the effect of
relaxing some of these assumptions will be con-
sidered.
For each species under consideration, the data re-
quired for this program, at a minimum, consist of
a large length-frequency sample, otolith data and/or
a time series of length-frequency data, a systematic
CPUE survey, and an estimate of catchability, such
as that obtained from an intensive fishing experi-
ment. The large length-frequency sample is used to
jointly estimate the asymptotic length (Lm) and the
ratio of total instantaneous mortality (Z) to the von
Bertalanffy growth parameter (K) based on the
following relationship:
0 = ZIK = (Lm - 1)1 (T - Lc),
where Lc is a parameter defined above and I is the
mean length of all fish greater than Lr (Beverton
Manuscript accepted February 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
759
FISHERY BULLETIN: VOL. 84, NO. 4
Intensive Fishing
Length Frequency
©
Systematic Survey
of Relative Abundance
Otoliths
Time Series
Length Frequency
I
Yield and Relative
Spawning Stock Equations
f MSY j
Figure 1.— Schematic of the yield assessment approach. A more general approach to fishery
assessment which includes a treatment of catch and effort data as well is given in Munro (1983);
our Figure 1 represents a detailed subset of Munro's figure 1 (1983).
and Holt 1956). For a series of Lc values at inter-
vals beginning with the smallest Lc and going up to
L^, there will be a corresponding set of I values.
By solving the ZIK equation above for I as a func-
tion of Lc, the following relationship is obtained:
T = LJ(Q + 1) +Lc(0/(0 + 1)).
Thus, regressing a sequence of I values on the cor-
responding L( values will produce estimates for the
slope and intercept which can be solved for esti-
mates of Lx and ZIK (Wetherall et al. in press).
Once an estimate of L has been obtained by this
method, otolith data and/or a time series of length-
frequency data can be fit to the von Bertalanffy
growth curve to estimate the growth coefficient K.
Estimation of L^ from length-frequency data was
used for the Marianas bottom fish data because a
large length-frequency sample was available and
otolith readings were difficult to interpret for old
stages of growth. With an estimate for K, the total
mortality rate, Z, can then be estimated as the pro-
duct of K and the ratio of ZIK obtained in the
previous step. Alternatively, one can estimate Z
from a catch curve constructed from a length-
frequency sample which has been corrected for
nonlinear growth and converted to an age-frequency
sample (Pauly 1983).
If these techniques are applied to unexploited or
lightly exploited resources, the estimate of Z pro-
vides an estimate of the instantaneous rate of
natural mortality (Af ). However, if fishing mortal-
ity is believed significant, an equation to estimate
M as a function of K, L^, and mean annual water
temperature (T) (in °C) has been developed as
follows (Pauly 1983):
log10 M = -0.0066 - 0.279 log10 L^
+ 0.6543 log10 K + 0.4634 log10 T.
Given estimates of K, M, and age of entry to the
fishery (tc), the Beverton and Holt (1957) yield per
recruit (Y/R) equation can be used to compute the
ratio of equilibrium yield to unexploited recruited
biomass as a function of fishing mortality (F). The
760
POLOVINA and RALSTON: MSY FOR DEEP SLOPE FISHES
equilibrium yield (Y) can be expressed as
oo
Y = R F J exp {-tM - (t - tc) F) w(t) dt,
where w(t) = W^ (1 - exp(-Kt))b, and where W^
is the asymptotic weight and b is the exponent of
the length-weight relationship. The unexploited
recruited biomass (B ) can be expressed as
B
= R J w(t) exp ( -Mi) dt.
The ratio of equilibrium yield to unexploited re-
cruited biomass (Y/BJ) is then independent of Wx
and R, depending only on K, M, tc, F, and b. Tables
and computational formulae are readily available to
evaluate these integrals for Y and 5m as functions
of tc and F (Beverton and Holt 1966; Beddington
and Cooke 1983). Upon estimation of B^, the equi-
librium yield is estimated for a given level of F as
the product of YIB and B .
* oo oo
If a stock is unfished, Bm can be estimated by
mapping the relative abundance of the stock in
terms of CPUE from a systematic survey and then
converting estimates of relative abundance into
biomass with an estimate of catchability. There are
a number of methods which have been used to esti-
mate catchability (Ricker 1975). For work on Pacific
island fishery resources, an intensive fishing ap-
proach, which fishes a small isolated location heavily
and regresses CPUE on cumulative catch (Leslie
model), has been used successfully to estimate catch-
ability for bottom fishes and shrimp (Polovina 1986a;
Ralston 1986). If only one estimate of catchability
is obtained, then the standing stock per unit of area
is determined as the ratio of CPUE to catchability
in the appropriate units of weight or numbers. If
several estimates of catchability are available corre-
sponding to different levels of CPUE, then it might
be appropriate to fit a more general power function
relationship between CPUE and standing stock
(Bannerot and Austin 1983).
The product of YIB^ and B^ as a function of F
is the equilibrium yield based on the assumption of
constant recruitment. While this assumption will be
valid for low levels of exploitation, there will come
a point as F increases that recruitment will begin
to decline and sustainable yield may thus be less than
the yield predicted under the assumption of constant
recruitment. Estimating MSY yield as the maximum
equilibrium yield obtained over all F from the prod-
uct of Y/B^ and B^ may, therefore, overestimate
the actual MSY. There are two adjustments which
have been proposed to estimate MSY in the absence
of detailed knowledge of the spawner-recruit rela-
tionship. One approach is to estimate MSY from the
constant recruitment yield curve as that yield cor-
responding to that level of F where the addition of
one unit of mortality increases the yield by 10% of
the amount caught by the first unit of F (Gulland
1983, 1984). This level of mortality and correspond-
ing yield have been denoted as F01 and Y0A,
respectively. A second approach to estimating MSY
from the constant recruitment yield curve is to use
the Beverton and Holt equation to calculate the ratio
of the spawning stock biomass under exploitation
(S) to the spawning stock biomass in the absence
of exploitation (S0) and to use this ratio as an in-
dicator of the sustainability of a yield for a given
combination of F and tc . For simplicity, we assume
that the age of sexual maturity (tm) is identical for
both sexes. Then the unexploited spawning stock
biomass (50) is
S0 = R J exp(-Aft) w(t) dt,
and
S = R J exp(-M - (t-tc) F) w(t) dt.
Thus, the ratio of S/S0 depends only on M, K, tc, tm,
andF.
It has been suggested that the spawning stock
biomass of a species should not be reduced below
20% of its unexploited level if a substantial reduc-
tion in the recruitment is to be avoided (Beddington
and Cooke 1983). Thus, the estimate of MSY is
determined as the maximum yield from the constant
recruitment curve subject to the constraint that F
does not exceed the level which reduces the relative
spawning stock biomass below 0.20 of S0.
ASSESSMENT OF SNAPPERS AND
GROUPERS IN THE MARIANAS
The Mariana Archipelago consists of a chain of
islands and banks on a north-south axis beginning
with Galvez Banks and Santa Rosa Reef at the
southern end and extending northward to Farallon
de Pajaros (30 nmi north of Maug Island). A chain
of seamounts also runs on a north-south axis
761
FISHERY BULLETIN: VOL. 84, NO. 4
about 120 nmi west of the high island chain (Fig.
2).
Six resource assessment cruises of 40 d each were
conducted in the Marianas during the period from
May 1982 through June 1984. During these cruises,
the deepwater snapper and grouper community
along the outer slope was sampled at all 22 islands
and banks labeled in Figure 2. Thirteen of these 22
sampling sites were visited at least once during the
first three cruises and, again, during the second set
■Maug
a Asuncion
-20°-
-19°
o Bank C
OAgrihan
P Pagan I.
-18°-
BankO
<?Alamagan
I
°Guguan I.
■17°-
0 Pathfinder Reef
Arakane Reef
Bank A
°Sarigan I.
^Anatahan I.
Farallon de Medinilla-
38 fm Bank
l
Esmeralda Bank o
-16°
/ySaipan
"VTinian I."
° Aguijan I.
^Rota I.
-15°
-14°
GUAM
"Coco! I.
.iGalvez Banks —
'Santa Rosa Reef
143°
I
I44c
145°
146°
I47e
I
Figure 2.— The Mariana Archipelago with the 22 islands and banks sampled.
762
POLOVINA and RALSTON: MSY FOR DEEP SLOPE FISHES
of three cruises. Two sites, Pagan Island and
Esmeralda Bank, were sampled on each of the six
cruises to establish a time series of length-frequency
data.
The NOAA ship Townsend Cromwell was used as
the fishing vessel for all the cruises. The fishing was
conducted from four hydraulic gurdies equipped
with 365 m of braided 90 kg Dacron2 line. The ter-
minal rig consisted of four hooks spaced about 1 m
apart and of 2 kg weight.
At each island and bank, an attempt was made
to perform a systematic fishing survey of the bot-
tom fish community along the 200 m contour. Fish-
ing was conducted while the vessel drifted and
targeted the 125-275 m depth range. Fishing effort
was measured in line-hours, defined as the product
of the number of lines fished with the length of time,
in hours, that they are fished.
Seven species— one jack, Caranx lugubris, and six
snappers, Pristipomoides zonatus, P. auricilla, P.
filamentosus, P.flavipinnis, Etelis carbunculus, and
E. coruscans— accounted for about 92% of the catch
(Polovina 1986b). Large length-frequency samples
were collected for all seven species, primarily from
the unfished islands and banks, and were used to
jointly estimate MIK, the ratio of instantaneous
natural mortality (M) to the growth parameter of
the von Bertalanffy growth curve (K), and the
asymptotic length (LJ by regressing a sequence of
mean lengths on minimum lengths (Wetherall et al.
in press). Otoliths were collected for all seven species
and the growth coefficient K was estimated by fit-
ting a von Bertalanffy growth curve to otolith data
with L fixed at the value estimated from the
oo
length-frequency analysis (Ralston and Williams3).
Once K and the ratio of MIK were estimated, an
estimate of M was obtained from their product. The
size of entry to the fishery was estimated as the in-
tegrated midpoint of the ascending limb of the size-
frequency distribution (Gulland 1969). This size was
then converted to an age of entry into the fishery
(tc) by application of the von Bertalanffy growth
curve. The values of Lm, K, M, tm, and tc for the
seven species which are required by the yield
analysis are given in Table 1. The exponent of the
length-weight equation (b) for most of the species
is not significantly different from 3.0, so to simplify
the computation, it will be taken as 3.0 for all the
species (Ralston in press).
An estimate of the catchability of the bottom
fishes which was used to convert CPUE into stand-
ing stock was derived from an intensive fishing ex-
periment conducted at Pathfinder Reef (Polovina
1986a). Thirteen days of intensive handline fishing
with the Townsend Cromwell at Pathfinder Reef
produced a substantial and significant decline in
CPUE. Application of the Leslie model (Ricker
1975), which regresses CPUE against cumulative
catch, produced estimates of catchability for three
species— Pristipomoides zonatus, P. auricilla, and
Etelis carbunculus (Polovina 1986a). While interest-
ing differences in catchability among species were
found, the estimate of the total unexploited biomass
for the three species obtained from the species
specific Leslie model was not significantly different
from the total unexploited biomass computed from
the Leslie model applied to the catch and CPUE data
pooled over all three species. Catchability from the
pooled Leslie model is estimated to be 0.0066 nmi/
line-hour. This value was used as an estimate of total
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
3Ralston, S., and H. A. Williams. Age, growth, and mortality
of deep slope lutjanid fishes from the Mariana Archipelago.
Manuscr. in prep. Southwest Fisheries Center Honolulu Labor-
atory, National Marine Fisheries Service, NOAA, Honolulu, HI
96822-2396.
Table 1.— Population parameters for the seven major species caught by handlining
in the Marianas.
Instan-
Von Bertalanffy
taneous
natural
Age of
entry to
Age of
growth parameters
mortality
the catch
maturity
Species
L„ (cm)
K (1/yr)
(M)
tc w
tm (yO
Caranx lugubris
75.1
0.430
0.53
1.3
1.8
Pristipomoides
filamentosus
67.3
0.228
0.57
4.3
2.0
P. auricilla
42.6
0.335
0.81
3.6
2.4
P. flavipinnis
54.1
0.238
1.12
3.7
2.2
P. zonatus
47.0
0.245
0.63
4.65
3.25
Etelis coruscans
97.6
0.166
0.38
6.2
4.1
E. carbunculus
69.1
0.175
1.55
3.45
2.75
763
FISHERY BULLETIN: VOL. 84, NO. 4
bottom fish catchability and was used to estimate
standing stock from CPUE.
The systematic survey of relative abundance uses
the fishing drift as the basic sampling unit. A drift
is defined as the fishing which occurs during an un-
interrupted drift by the vessel while fishing contin-
uously in the 125-275 m depth range. The CPUE
measured is the number of fish per line-hour and can
be computed in two ways for each bank. Bank
CPUE will be defined as the total number of fish
caught at an island or bank divided by the total
number of line-hours fished. Bank mean drift CPUE
or simply mean drift CPUE will be defined as the
mean of all the individual drift CPUE values for a
bank, where the drift CPUE is computed as the
number of fish caught within a drift divided by the
drift line-hours. While the two measures of CPUE
are highly correlated, they are not identical. In our
analysis the mean drift CPUE was used as a mea-
sure of relative abundance because in a systematic
survey the drifts within a bank can be thought of
as replicates drawn from the total bank population
allowing estimation of within bank variation in
CPUE. For a bank, the total standing stock or
number of exploitable bottom fishes (N) can be
calculated from CPUE, the length (L ) of the 200 m
contour, and the catchability (q) expressed per
nautical mile of 200 m contour as follows:
N = (CPUE) (L/q).
The values of N, CPUE, and L for the banks sam-
pled are given in Table 2.
The catch at any bank can be grouped into eight
groups— the seven major species defined previous-
ly, plus a group called "others" for all other species.
The fraction of the catch (by number) of the total
bank catch as determined from fishing surveys, is
given in Table 3. The mean weight of each species
caught at each site is given in Table 4. For each
bank, the unexploited recruited biomass (BJ for
each of the eight groups is estimated by partition-
ing the total standing stock into a standing stock
for each species group from Tables 2 and 3 and then
converting the standing stock for each species group
into biomass for each group based on the mean
weights in Table 4. Estimates of B^ for the eight
species groups at each bank are given in Table 5 and
the total unexploited biomass is given in Table 6.
The estimates of biomass per nautical mile of 200
m contour at Saipan, Tinian, Rota, and Guam are
less than half the levels at most other banks. These
four islands are the only islands in the Marianas with
a substantial resident population. The local fisher-
men at these islands are known to exploit the bot-
tom fish stocks locally so that estimates of biomass
based on bank CPUE values are likely to under-
estimate unexploited levels. The mean of the bio-
mass per nautical mile of 200 m contour for the two
uninhabited islands and one bank in the southern
islands is 600 kg. This value was used for unex-
Table 2.— Mean drift catch per unit effort (CPUE) and the estimated number of
exploitable bottom fish recruited at each bank samples. SE indicates standard
error.
Mean drift
Length of
Total number
CPUE (fish/
200 m contour
of fish at
Banks and islands
line-hour)
SE
(nmi)
each bank
Maug
5.03
1.02
10.4
7,580
Asuncion
2.16
0.49
11.1
3,480
Agrihan
4.20
0.31
18.3
11,140
Pagan
4.57
0.40
30.0
19,870
Alamagan
2.37
0.19
11.3
3,881
Guguan
3.01
0.30
9.3
4,060
Sarigan
2.82
0.37
8.5
3,470
Anatahan
2.31
0.23
17.2
5,760
Farallon de Medinilla
3.29
0.65
76.9
36,670
Saipan
1.72
0.34
52.6
13,110
38-Fathom
3.12
0.26
2.8
1,270
Tinian
1.96
0.29
28.9
8,210
Aguijan
3.84
0.98
15.9
8,850
Esmeralda
2.29
0.15
12.3
4,080
Rota
1.91
0.40
31.7
8,780
Guam
1.53
0.35
85.2
18,890
Galvez-Santa Rosa
2.95
0.31
52.5
22,450
Bank C
5.91
1.57
3.0
2,570
Bank D
5.85
0.51
3.0
2,540
Pathfinder
4.58
0.23
3.0
1,990
Arakane
3.36
0.24
2.9
1,410
Bank A
3.71
0.57
3.6
1,940
764
POLOVINA and RALSTON: MSY FOR DEEP SLOPE FISHES
Table 3.— The fraction of the number of fish caught at each bank in the eight species
groups.
Banks and
islands
Caranx
lugubris
eo
ID
is
11
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CD
O
Maug
0.016
0.000
0.347
0.016
0.425
0.000
0.102
0.094
Asuncion
0.036
0.036
0.089
0.000
0.589
0.018
0.036
0.196
Agrihan
0.016
0.041
0.103
0.064
0.602
0.016
0.110
0.048
Pagan
0.007
0.002
0.089
0.013
0.699
0.023
0.126
0.042
Alamagan
0.010
0.013
0.232
0.011
0.495
0.143
0.059
0.037
Guguan
0.020
0.004
0.182
0.004
0.613
0.047
0.083
0.047
Sarigan
0.016
0.010
0.141
0.010
0.646
0.042
0.057
0.078
Anatahan
0.015
0.035
0.119
0.148
0.540
0.040
0.045
0.059
38-Fathom
0.064
0.028
0.228
0.047
0.434
0.019
0.045
0.136
Esmeralda
0.017
0.051
0.040
0.366
0.397
0.029
0.026
0.074
Farallon de
Medimlla
0.052
0.021
0.093
0.166
0.477
0.021
0.093
0.078
Saipan
0.013
0.138
0.087
0.338
0.225
0.000
0.075
0.125
Tinian
0.000
0.000
0.083
0.694
0.000
0.056
0.139
0.028
Aguijan
0.021
0.188
0.063
0.417
0.271
0.000
0.000
0.042
Rota
0.019
0.143
0.162
0.114
0.362
0.029
0.067
0.105
Guam
0.064
0.161
0.258
0.129
0.161
0.000
0.129
0.097
Galvez-
Santa Rosa
0.085
0.017
0.364
0.051
0.322
0.009
0.059
0.093
Bank C
0.000
0.017
0.390
0.000
0.356
0.017
0.212
0.009
Bank D
0.015
0.010
0.091
0.005
0.480
0.045
0.349
0.005
Pathfinder
0.059
0.011
0.172
0.004
0.506
0.000
0.215
0.032
Arakane
0.116
0.057
0.188
0.003
0.412
0.000
0.169
0.055
Bank A
0.008
0.004
0.184
0.008
0.607
0.000
0.159
0.029
Table 4. — Mean weight (kg) of the fish caught by bank and species group.
Banks and
islands
Caranx
lugubris
eo
CD
6 CO
E S
S c
.Q. CD
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c
a
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co
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Maug
3.784
1.930
0.815
1.585
0.977
6.113
0.893
2.559
Asuncion
3.784
1.930
0.848
1.265
1.344
6.113
0.670
4.595
Agrihan
3.784
1.930
0.784
1.235
1.169
6.113
0.741
7.787
Pagan
3.784
1.930
0.651
1.169
1.094
6.113
0.652
5.068
Alamagan
3.784
1.930
0.834
1.354
1.326
6.113
1.010
2.992
Guguan
3.784
1.930
0.773
1.780
1.216
6.113
0.815
2.400
Sarigan
3.784
1.930
0.642
1.025
1.204
6.113
0.811
5.279
Anatahan
3.784
1.930
0.556
1.169
0.874
6.113
0.586
2.631
38-Fathom
3.784
1.930
0.532
1.193
0.874
6.113
0.798
2.523
Esmeralda
3.784
1.930
0.567
1.014
0.782
6.113
0.702
8.409
Farallon de
Medinilla
3.784
1.930
0.439
1.265
0.891
6.113
0.575
1.963
Saipan
3.784
1.930
0.577
0.992
0.837
6.113
0.773
1.353
Tinian
3.784
1.930
0.653
1.003
1.017
6.113
0.422
0.520
Aguijan
3.784
1.930
0.480
0.927
0.760
6.113
0.753
0.770
Rota
3.784
1.930
0.542
1.222
0.667
6.113
0.506
3.168
Guam
3.784
1.930
0.606
1.112
0.780
6.113
0.673
0.600
Galvez-
Santa Rosa
3.784
1.930
0.522
1.206
0.979
6.113
0.801
2.085
Bank C
3.784
1.930
0.761
1.265
1.267
6.113
0.923
0.920
Bank D
3.784
1.930
0.961
1.710
1.169
6.113
0.983
1.070
Pathfinder
3.784
1.930
1.953
1.381
1.218
6.113
0.875
7.348
Arakane
3.784
1.930
0.860
1.350
0.949
6.113
0.791
2.338
Bank A
3.784
1.930
0.636
1.605
0.984
6.113
0.811
5.504
765
FISHERY BULLETIN: VOL. 84, NO. 4
Table 5.— The unexploited recruited biomass by bank for each species groups in
metric tons.
Banks and
islands
Caranx
lugubris
Pristipomoides
filamentosus
-5
co
.co
c
c
S.
CD
1
CO
c
o
N
CL
co
c
CO
o
CO w
11
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c
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o
uj
i2
0)
O
Maug
0.5
0
2.2
0.2
3.3
0
0.7
1.9
Asuncion
0.5
0.2
0.3
0
2.9
0.4
0.1
3.3
Agrihan
0.7
0.9
0.9
0.9
8.2
1.1
0.9
4.4
Pagan
0.6
0.1
1.2
0.3
15.9
2.9
1.7
4.4
Alamagan
0.1
0.1
0.8
0.1
2.7
3.5
0.2
0.5
Guguan
0.3
<0.1
0.6
<0.1
3.2
1.2
0.3
0.5
Sarigan
0.2
0.1
0.3
<0.1
2.8
0.9
0.2
1.5
Anatahan
0.3
0.4
0.4
1.0
2.8
1.5
0.2
0.9
38-Fathom
0.3
0.1
0.2
0.1
0.5
0.2
<0.1
0.5
Esmeralda
0.3
0.4
0.1
1.6
1.3
0.7
0.1
2.7
Farallon de
Medinilla
7.5
1.5
1.6
8.0
16.3
4.9
2.1
5.8
Saipan
0.6
3.6
0.7
4.6
2.6
0
0.8
2.3
Tinian
0
0
0.5
6.0
0
2.9
0.3
0.1
Aguijan
0.7
3.3
0.3
3.6
1.9
0
0
0.3
Rota
0.7
2.6
0.8
1.3
2.2
1.6
0.5
3.1
Guam
4.8
6.1
3.1
2.8
2.5
0
1.7
1.1
Galvez-
Santa Rosa
7.5
0.8
4.5
1.4
7.4
1.2
1.1
4.6
Bank C
0
0.1
0.8
0
1.2
0.3
0.5
<0.1
Bank D
0.2
0.1
0.2
<0.1
1.5
0.7
0.9
<0.1
Pathfinder
0.5
<0.1
0.4
<0.1
0.3
0
0.4
0.5
Arakane
0.6
0.2
0.2
<0.1
0.6
0
0.2
0.2
Bank A
0.1
<0.1
0.2
<0.1
1.2
0
0.3
0.3
Total
32.5
32.0
24.5
43.1
85.4
26.2
15.9
42.8
Table 6.— The total unexploited recruited biomass (BJ in metric tons (t) and
the total unexploited recruited biomass per nautical mile (nmi) of 200-m con-
tour in kilograms (kg) by bank.
Total
unexploited
Biomass per nmi of
Banks and islands
recruited biomass (t)
200 i
m contour (kg)
Northern banks and islands
Maug
8.8
850.3
Asuncion
7.7
689.7
Agrihan
18.1
991.1
Pagan
27.0
900.7
Alamagan
8.0
706.8
Guguan
6.1
659.7
Sarigan
6.1
714.0
Anatahan
7.6
440.6
38-Fathom
1.8
637.1
Esmeralda
7.2
584.1
Total
98.4
Mean
717.4
Southern banks and islands
Farallon de Medinilla
47.7
620.2
Saipan
15.3
290.9
Tinian
10.0
346.0
Aguijan
10.1
637.0
Rota
12.4
391.2
Guam
22.2
260.6
Galvez-Santa Rosa
28.5
542.4
Total
146.2
Mean
441.2
Western seamounts
Bank C
2.9
973.0
Bank D
3.6
1,207.0
Pathfinder
3.1
1,024.0
Arakane
2.0
695.9
Bank A
2.1
594.7
Total
13.7
Mean
898.9
766
POLOVINA and RALSTON: MSY FOR DEEP SLOPE FISHES
ploited biomass per nautical mile of 200 m contour
in the subsequent yield estimation, in place of the
values computed from the bank CPUE values for
the inhabited southern islands (Saipan, Tinian, Rota,
and Guam).
For each species group with values of K, M, tc,
and F, the ratio of fishery yield to unexploited
recruited biomass {YIBJ can be computed from the
Beverton and Holt yield equations (Beddington and
Cooke 1983). The product of YIB^ with the species
group unexploited recruited biomass estimates
(Table 5) results in estimates of equilibrium yield for
the seven species for which estimates of K and M
are available. For the eighth group, which consists
of all other species, the ratio of yield to B^ is taken
as the ratio of total yield for the seven species
divided by their total Bm. For a fixed F, the sum of
the equilibrium yield of the eight species groups at
a bank is the bank equilibrium yield, and the sum
of the equilibrium yields for a species group over
all the banks is the species group equilibrium yield.
The equilibrium yield for the multispecies bottom
fish complex fished with handline gear in the 125-
275 m depth range for the 22 islands and banks of
the Mariana Archipelago increases rapidly as a func-
tion of F to a level of about 90 t and beyond that
exhibits a gradual increase with increased fishing
mortality (Table 7). The MSY estimation approach
estimates MSY as the yield from the constant re-
cruitment yield curve corresponding to that level of
mortality where a marginal increase in one unit of
Table 7. — Total annual sustainable
handline yield in metric tons (t) for a
range of fishing mortalities.
Fishing mortality (F)
Total yield (t)
0.1
23
0.5
64
11.0
182
1.5
89
2.0
92
2.5
94
mortality increases the catch by 0.1 of the amount
caught by the first unit of F. The value of F0A for
the bottom fish resource in the Marianas is esti-
mated to be F = 1.0 and the corresponding annual
equilibrium yield is 82 t (Table 7).
The equilibrium yield value of 82 t, which cor-
responds to a fishing mortality of 1.0, is based on
the current estimated age of entry to the fishery and
not necessarily the age of entry which maximizes
the YIR. For a fishery mortality of 1.0, the estimated
age of entry which maximizes YIR is computed from
the Beverton and Holt equation and compared with
the current age of entry for each species (Table 8).
With the exception of the jack, Caranx lugubris, the
age of entry which maximized YIR is less than the
current age of entry (Table 8). Based on the age of
entry which maximized the YIR, new levels of sus-
tainable yield for each species group as a function
of F can be computed as the product of the yield
for the current age of entry with the ratio of YIR
maximized over age of entry to the YIR for the cur-
rent age of entry. The values of F01 and Y01 for
the ages of entry which maximize the YIR are 1.0
and 109 t, respectively (Table 9). An approximate
confidence interval (C.I.) for this yield estimate can
be obtained from a Taylor series expansion which
incorporates the variance estimate for catchability
(Polovina 1986a) and a sampling variance of the
bank CPUE values (Table 2). The standard error of
the yield estimate is 14 t, and thus a 95% C.I. for
the yield at F01 for the archipelago is 81-137 t
annually.
The estimation of MSY based on the relative
spawning stock approach requires estimates of the
age of sexual maturity (tm). A relationship express-
ing the length at sexual maturity (Lm) as a fraction
of the length of the upper one percentile (Lmax) for
tropical bottom fishes is as follows (Anonymous
1977, from Brouard and Grandperrin 1984):
Lm = 0.576 Lmax.
1F01 and /01 as defined by Gulland (1983).
Table 8.— Current age at entry and age at entry which maximizes the yield
per recruit (YIR) at F = 1.0.
Current age at
entry
Age
at entry which
Species
tc (yr)
maximizes YIR (yr)
Caranx lugubris
1.3
1.75
Pristipomoides filamentosus
4.3
2.75
P. auricilla
3.6
2.25
P. flavipinnis
3.7
2.00
P. zonatus
4.65
3.00
Etelis coruscans
6.2
4.50
E. carbunculus
3.45
2.50
Table 9.— Annual sustainable handline
yield in metric tons (t) for the age at
entry which maximizes the yield per
recruit for each species.
Fishing mortality (F)
Total yield (t)
0.1
35
0.5
91
11.0
1109
1.5
114
2.0
116
2.5
116
1F01 and y0.
as defined by Gulland (1983).
767
FISHERY BULLETIN: VOL. 84, NO. 4
The tm can then be computed from Lm with the von
Bertalanffy growth equation. The tm for the seven
species, which is assumed to be the same for both
sexes of a species, is given in Table 1, and the ratio
of spawning stock biomass under exploitation to the
unexploited spawning stock biomass is presented for
three levels of F (Table 10). As expected, the ratio
decreases as F increases. However, without the
spawner-recruit relationship, it is difficult to deter-
mine the extent that the spawning stock biomass
can be reduced before recruitment is substantially
affected. It has been suggested that as a lower
bound, the spawning stock biomass should not be
reduced below 20% of its unexploited level before
there is a deleterious reduction in recruitment
(Beddington and Cooke 1983). The level of F = 1.0
is the largest level of F which insures that the
relative spawning stock biomass for all the species
does not fall below 20% and hence the spawning
stock approach also estimates the MSY for the bot-
tom fish in the Marianas at 109 t/year.
Table 10. — The ratio of spawning stock biomass to unexploited
spawning stock biomass for three levels of fishing mortality (F) at
the age of entry which maximizes the yield per recruit.
Species
F = 0.5
F = 1.0
F = 2.0
Caranx lugubris
0.44
0.26
0.12
Pristipomoides filamentosus
0.46
0.33
0.25
P. auricilla
0.45
0.29
0.19
P. flavipinnis
0.45
0.26
0.12
P. zonatus
0.39
0.24
0.14
Etelis coruscans
0.31
0.20
0.13
E. carbunculus
0.58
0.42
0.30
DISCUSSION
The assessment proposed here is a multispecies
approach which is most suitable for resources where
prey-predator interactions are negligible. Two
assumptions initially required to implement this
program, i.e., constant recruitment and that the
resource be essentially unexploited, can in some
instances be relaxed. Simulation results suggest that
if recruitment is seasonal and a pooled length fre-
quency is constructed from individual length-
frequency samples collected over the year, the
length-frequency based method used here to esti-
mate mortality produces an essentially unbiased
estimate (Ralston4). Furthermore, the assumption
that stocks be unexploited can be relaxed if an
estimate of the average of F for the archipelago can
be obtained. Then M can be estimated by the dif-
ference between F and total mortality, and instead
of estimating unexploited recruited biomass from
the CPUE survey, the biomass under F will be
estimated, and yields calculated as the product of
exploited biomass with the ratio of yield/biomass
resulting from F computed from the Beverton and
Holt yield equation.
The estimate of maximum equilibrium yield from
the Beverton and Holt (1957) equation for the deep
slope snappers and groupers from 22 banks in the
Mariana Archipelago is 109 1 annually with a fishing
mortality of 1.0. About 70% of this yield would be
expected to come from the southern islands of the
chain, including Guam and Saipan. Another 27%
would come from the northern islands and only 3%
from the seamounts (Table 11).
The mean of the annual sustainable yield levels
per nautical mile of 200 m contour for the northern
banks, southern banks, and western seamounts are
212.9, 228.5, and 264.4 kg, respectively, with a ratio
of total yield for the archipelago to the total length
of the 200 m contour of 222.4 kg/nmi (95%) C.I. of
165.3-279.6) (Table 11). Detailed bathymetry data
to establish a correspondence between contour
length and area are available from Guguan Island
in the northern Marianas, and it is estimated that
1 nmi of 200 m isobath corresponds to 0.23 nmi2 of
habitat in the 125-275 m depth range (Polovina and
Roush5). Based on this correspondence the unit MSY
of 222.4 kg/nmi of 200 m contour for the Marianas
is equivalent to about 1.0 t/nmi2 or 0.3 t/km2.
These values suggest that the Marianas may be
slightly less productive for bottom fishes than the
Hawaiian Archipelago where a lower bound esti-
mate for MSY of 272 kg/nmi of 200 m contour was
obtained from a stock production model applied to
commercial catch and effort data that did not include
the recreational fishing component of snappers and
groupers. Also, an estimate of 286 kg/nmi of 200
m contour was derived from an ecosystem model ap-
plied to an island system in the Northwestern
Hawaiian Islands (Ralston and Polovina 1982;
Polovina 1984).
The species composition of the catch should
depend to some extent on levels of F and tc. As F
increases and tc decreases, the contribution of
4Ralston, S. The effect of pooling length-frequency distributions
on mortality estimation in seasonally breeding fish populations:
A Monte Carlo simulation. Manuscr. in prep. Southwest Fish-
eries Center Honolulu Laboratory, National Marine Fisheries Ser-
vice, NOAA, Honolulu, HI 96822-2396.
6Polovina, J. J., and R. C. Roush. 1982. Chartlets of selected
fishing banks and pinnacles in the Mariana Archipelago. South-
west Fish. Cent. Honolulu Lab., Natl. Mar. Fish. Serv., NOAA,
Admin. Rep. H-82-19, 7 p.
768
POLOVINA and RALSTON: MSY FOR DEEP SLOPE FISHES
Table 11.— Annual sustainable yield in metric tons (t) and yield in kilograms
(kg) per nautical mile (nmi) of 200 m contour for the age at entry which max-
imizes the yield per recruit at a level of fishery mortality of F = 1.0.
Total yield
Yield
(kg per nmi of
Banks and islands
(t/yr)
200
m contour/yr
Northern banks and islands
Maug
2.7
262
Asuncion
2.1
188
Agrihan
5.6
304
Pagan
7.7
255
Alamagan
2.0
178
Guguan
1.7
179
Sarigan
1.6
194
Anatahan
2.5
144
38-Fathom
0.5
187
Esmeralda
2.9
237
Total
29.3
Mean
213
Southern banks and islands
Farallon de Medinilla
16.7
217
Saipan
13.4
254
Tinian
8.8
304
Aguijan
4.2
267
Rota
6.1
192
Guam
17.2
202
Galvez-Santa Rosa
8.6
164
Total
76.0
Mean
229
Western seamounts
Bank C
0.9
288
Bank D
1.1
351
Pathfinder
0.9
304
Arakane
0.6
200
Bank A
0.6
180
Total
4.1
Mean
264
Total yield from all banks
s: 109
t/yr.
Total yield/length of 200
m contour = 222.3
kg/nmi.
those species to the catch with the high MIK values,
particularly P. flavipinnis andE1. carbunculus tends
to increase (Table 12). A form of succession is,
therefore, predicted as exploitation proceeds.
There are two approximations which have been
used to determine MSY which express it as a frac-
tion of the unexploited biomass. Gulland's formula
estimates MSY as 0.5 MB, where M is the instan-
taneous rate of natural mortality and B is the unex-
ploited biomass. An approach proposed by Pauly
estimates MSY as B 2.3w~02S, where w is the mean
of the weight (in grams) at sexual maturity and the
asymptotic weight (Gulland 1983; Pauly 1983). A
comparison of these two estimators with the values
obtained here shows that for four out of seven
species the YIB values estimated with the Bever-
ton and Holt equation lie between the values ob-
tained from the Pauly and Gulland approximations.
Table 12.— The percentage of annual sustainable yield by species groups for two ages
at entry with two levels of fishing mortality.
Percentage of total catch by i
weight
Age at
entry which
maximizes yield
Current
F = 0.10
age of entry
F = 1.50
per
recruit
Species groups
F = 0.10
F = 1.0
Caranx lugubris
10.0
5.5
7.3
8.3
Pristipomoides filamentosus
10.3
8.5
9.4
8.2
P. auricilla
8.5
9.4
7.4
7.3
P. flavipinnis
15.6
21.7
24.3
28.7
P. zonatus
28.1
26.7
26.1
23.1
Etelis coruscans
7.6
5.1
7.1
5.0
E. carbunculus
5.9
9.2
4.6
5.9
Others
14.0
13.8
13.8
13.5
769
FISHERY BULLETIN: VOL. 84, NO. 4
For the other three species, the YIB values fall
slightly below the Pauly and Gulland approximations
for two species and substantially above for the third
species. The mean YIB values obtained by the Pauly
and Gulland approximations are, moreover, in
substantial agreement with the mean value of YIB
obtained with the approach proposed here (Table
13).
Table 13. — Annual maximum sustainable yield as a fraction of
unexploited recruited biomass (YIB J at F = 1 .0 together with 0.5
M and 2.3 w"026.
Species groups
YIB
0.5 M 2.3 w-026
Caranx lugubris
0.261
0.335
0.252
Pristipomoides filamentosus
0.262
0.270
0.296
P. auricilla
0.306
0.325
0.403
P. flavipinnis
0.680
0.475
0.348
P. zonatus
0.280
0.270
0.363
Etelis coruscans
0.201
0.175
0.226
E. carbunculus
0.375
0.515
0.289
Mean
0.338
0.338
0.311
ACKNOWLEDGMENT
This paper is the result of the Resource Assess-
ment Investigation of the Mariana Archipelago at
the Southwest Fisheries Center Honolulu Labora-
tory, NOAA.
LITERATURE CITED
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1977. Inventaire critique des donnees utilisees pour l'etude
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Beddington, J. R., and J. G. Cooke.
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Brouard, F., and R. Grandperrin.
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Gulland, J. A.
1969. Manual of methods for fish stock assessment. Part 1.
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1984. Advice on target fishery rates. ICLARM Fishbyte
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Munro, J. L.
1983. A cost-effective data acquisition system for assessment
and management of typical multispecies, multi-gear fish-
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Pauly, D.
1983. Some simple methods for the assessment of tropical
fish stocks. FAO Fish. Tech. Pap. (234), 52 p.
Pauly, D., and G. I. Murphy (editors).
1982. Theory and management of tropical fisheries.
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pines, and Division of Fisheries Research, CSIRO, Cronulla,
Australia.
POLOVINA, J. J.
1984. Model of a coral reef ecosystem. I. The ECOPATH
model and its application to French Frigate Shoals. Coral
Reefs 3:1-11.
1986a. A variable catchability version of the Leslie model
with application to an intensive fishing experiment on a
multispecies stock. Fish. Bull, U.S. 84:423-428.
1986b. Variation in catch rates and species composition in
handline catches of deepwater snappers and groupers in the
Mariana archipelago. Proc. 5th Int. Coral Reef Congr.
1985, Tahiti.
Ralston, S.
1986. An intensive fishing experiment for the caridean
shrimp, Heterocarpus laevigatas, at Alamagan Island in the
Mariana Archipelago Fish. Bull., U.S. 84:927-934.
In press. Length-weight regressions and condition indices of
lutjanids and other deep slope fishes from the Mariana
Archipelago. Micronesica.
Ralston, S., and J. J. Polovina.
1982. A multispecies analysis of the commercial deep-sea
handline fishery in Hawaii. Fish. Bull., U.S. 80:435-448.
RlCKER, W. E.
1975. Computation and interpretation of biological statistics
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Saila, S. B., and P. M. Roedel (editors).
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Wetherall, J. A., J. J. Polovina, and S. Ralston.
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770
GROWTH, BEHAVIOR, AND SEXUAL MATURATION OF
THE MARKET SQUID, LOLIGO OPALESCENS,
CULTURED THROUGH THE LIFE CYCLE
W. T. Yang, R. F. Hixon, P. E. Turk, M. E. Krejci,
W. H. Hulet, and R. T. Hanlon1
ABSTRACT
Loligo opalescens, a commercially important species of the eastern Pacific, is the first pelagic cephalopod
to be cultured through the entire life cycle. Squid were cultured twice to viable second generation progeny
in closed seawater systems using artificial and natural seawater. The reasons for success compared with
previous attempts were 1) increased depth in the culture tank, 2) improvements in water conditioning
methods, and 3) an increase in availability, density, and species diversity of food organisms. The diet
consisted of live zooplankton (predominantly copepods), mysid and palaemonid shrimp, and estuarine
fishes. Mean daily group feeding rates of subadults and adults were 14.9% and 18.0% of body weight.
Growth was fast, increasing exponentially the first 2 months of the life cycle (8.35% increase in body
weight per day) then slowing to a logarithmic rate thereafter (5.6-1.6% increase per day). Growth rings
in statoliths corresponded to one per day for the first 65 days. Maximum life span was 235 and 248 days
in the two experiments, with a maximum size of 116 mm dorsal mantle length. Viable eggs were pro-
duced within 172 and 196 days, respectively. Eggs developed in 30 days at 15°C. Survival through the
life cycle was low, with the highest mortality occurring in the first few weeks when squid made the transi-
tion from feeding on yolk to active predation on fast-moving plankton. Fin or skin damage and senescence
after reproduction accounted for late mortality. The laboratory life cycle of less than a year is compati-
ble with existing field data that propose either a 1- or 2-year life cycle, depending upon the season of
hatching.
Since 1975 we have been studying loliginid squid to
develop methods of providing a consistent supply
for neuroscience research. These studies include
aspects of fishery biology (Rathjen et al. 1979; Hix-
on 1980a, b, 1983; Hixon et al. 1980), capture and
maintenance methods (Hanlon et al. 1978, 1983;
Hulet et al. 1979; Hanlon and Hixon 1983), behavior
(Hanlon 1978, 1982), and mass-culture methods
(Hanlon et al. 1979; Yang et al. 1980a, b, 1983a, b).
Much of the baseline information acquired through
these controlled culture experiments will also be im-
portant to the fisheries biology of commercially ex-
ploited loliginid squids (cf., Roper et al. 1983).
About 20 major attempts have been made to
culture loliginid squids through the life cycle, but
none have been successful (see review in Yang et
al. 1980b), even though wild-caught mature females
of Loligo and Doryteuthis spawn readily in captiv-
ity (Hamabe 1960; Fields 1965; Takeuchi 1969, 1976;
Hurley 1977; Arnold et al. 1974; Hanlon et al. 1983).
Fields (1965) attempted unsuccessfully to culture
Loligo opalescens as early as 1947. Hurley (1976)
'The Marine Biomedical Institute, The University of Texas
Medical Branch, 200 University Boulevard, Galveston, TX 77550-
2772.
reared L. opalescens for 100 d to a mantle length
(ML) of 13 mm. Hanlon et al. (1979) reared this
species to 17 mm ML in 79 d and, based upon that
work, reared L. opalescens from hatching to sub-
adults (Yang et al. 1980b, 1983a). We have now im-
proved previous culture methods by increasing the
rearing population density and by improving the
space requirements for young and adult squid. With
a more consistent supply of foods and improvement
of water management, we have now successfully
cultured this squid twice from egg to second genera-
tion, thus closing the life cycle.
MATERIALS AND METHODS
Two culture experiments are reported herein:
L.0. 1981 (full life cycle partly published in Japanese
by Yang et al., 1983b); and L.O. 1982 (full life cy-
cle). A third experiment, L.O. 1980, was published
by Yang et al. (1980b, 1983a) and is referenced for
comparison in the Discussion and figures.
For L.O. 1981, freshly laid eggs were obtained
from wild-caught squid kept in holding tanks at Sea
Life Supply (Sand City, CA 93955). Eggs were col-
lected from spawning grounds in Monterey Bay, CA
for experiment L.O. 1982. Eggs were air-shipped
Manuscript accepted February 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
771
FISHERY BULLETIN: VOL. 84, NO. 4
to Galveston (Yang et al., 1980b; 1983a, b). Only
early stage eggs were shipped and cultured (never
beyond stage 19, Arnold 1965). The eggs were ac-
climated gradually to the temperature and salinity
of the culture tank water; incubation temperature
was maintained around 15°C while salinity ranged
between 34 and 36%o. Bundles of a few capsules
each were suspended from a rack at the water sur-
face to ensure oxygenation and uniform develop-
ment of eggs. Styrofoam panels covered the rear-
ing tank and the illumination level was kept below
1 lux to prevent the growth of benthic diatoms on
egg capsules.
A circular tank (CT) system consisting of two cir-
cular tanks (each 1,300 L) was used for incubation
and early rearing of hatchlings and juvenile squid.
Water circulation was modified in L.O. 1982 when
compared with earlier culture experiments (Yang
et al. 1980b: fig. 1, 1983a: fig 1). Prior to L.O. 1982,
a laboratory-constructed particle/carbon filter was
used with circulation first passing through an ultra-
violet (UV) sterilizer. L.O. 1982 used modular type
particle and carbon filters, with the UV sterilizer
in the last position in the water conditioning pro-
cess. The raceway (RW) system (RW culture tank
volume-10,970 L in L.O. 1981, and 13,180 L in L.O.
1982) was used for final grow-out after transferring
the squid from the CT culture tanks. The transfer
was necessary to give the squid greater horizontal
swimming space. The initial RW system in experi-
ment L.O. 1981 had been modified from previous
experiments (Yang et al. 1980b, 1983a) to improve
water quality by 1) adding a rectangular, 960 L
capacity water conditioning tank (0.46 x 1.22 x
1.83 m, water depth 0.43 m) with water circulation
of 54 L/minute, 2) adding another cooling unit,
3) adding three protein skimmers, 4) adding three
UV light sterilizers (each 30 W, total 90 W), 5) modi-
fying the water uptake system in the RW with a
float near the center to remove near-surface water
without sucking up squid or food organisms and to
increase the lateral swimming space for the squid,
6) painting an irregular mottled pattern on the sides
of the RW to make the walls more visible to the
squid, and 7) most importantly, by increasing RW
water depth gradually from 24 cm initially to 40 cm
(average depth 38.8 cm) to provide swimming space
for the squid and to increase the average culture
water volume in the RW from 5,990 to 8,610 L.
A further improved RW system (Fig. 1) was used
in experiment L.O. 1982. It consisted of two bio-
logical filter tanks (A, C) with oyster shell subgravel
filters and airlifts for water circulation, a tank for
growing macroalgae (B), the RW where the squid
were cultured (D), and a separate tank where pro-
tein skimmers were operated continuously (E). The
surface water was taken from the RW through pipes
suspended in a screened floating core. Water within
the system was recirculated by three routes. First,
water was pumped to filter tank A that contained
approximately 0.15 m3 of oyster shell over a false
bottom. Water passed through the filter bed, then
flowed through a constant-level siphon to tank B
where algae were illuminated by two 400-W metal
halide lamps. Water flowed by gravity into the sec-
ond filter tank C that contained 0.18 m3 of oyster
shell substrate and two 1-hp cooling units, and final-
ly returned by gravity to the RW proper. Second,
water was pumped through two sets of six modular
filters: four modules containing pleated 20 ^m fiber
particle filters and two containing activated carbon.
From the modular filters, water either flowed direct-
ly into the RW or through a 60 W UV sterilizer
before returning to the RW. Third, water was
pumped at 36 L/minute to a tank that contained five
protein skimmers and then flowed back into the RW.
The outflow of the three recirculating routes created
a clockwise water flow in the RW proper. This mo-
tion accumulated dead squid and food organisms in
one place on the bottom. The bottom was painted
solid black with nontoxic Thixochlor2 paint and the
sides were painted with an irregular mottled pat-
tern. Three 11 x 28 cm windows were mounted in
one side of the RW for observing the squid's feeding
and behavior. The tanks were insulated with poly-
styrene sheeting and 2.3 cm thick polystyrene
covers.
To ensure activation of the biological filter for both
CT and RW systems, filter beds were inoculated 2
to 3 wk beforehand with nitrifying bacteria on oyster
shell from other systems. Fish and shrimp were
placed in the water conditioning tank to build up the
bacterial population. Thus the filter beds were estab-
lished by organic conditioning methods (Moe 1982)
instead of by directly adding ammonia source
chemicals.
A set of black silk nets was used to transfer squid
from the CT system into the RW system. A tri-
angular lift net was laid on the bottom of the tank
while two rectangular net curtains were slowly
drawn from the left and right sides of the tank to
concentrate the small squid above the lift net. The
lift net was gradually raised, a wash tub placed
underneath, and both were moved to the RW tank
where the squid were gently released into the tank.
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
772
YANG ET AL.: CULTURE EXPERIMENTS OF LOLIGO OPALESCENS
Lamps
1 meter
Cooling
units
'w///;;////////////////;/////;////////////////////////////?/
Length x Width x Depth (m)
A = 1.8x1.2x0.5
B = 1.2 x 0.5 x0.3
C = 1.8 (diameter) x 0.8
D = 6.1 x2.4 xO 9
E = 1.8x0.6x0.6
Protein skimmers
Filter module
(4 particle + 2 carbon)
Ultraviolet
sterilizer
Figure 1.— Raceway (RW) system (L.O. 1982) with recirculating culture seawater (17,000 L total) for grow-out of juvenile and
adult squid.
In L.O. 1981, 129 squid were not transferred from
the CT tank and they continued to grow in the CT,
thereby allowing comparisons of temperature toler-
ance and survival in small versus large culture
systems.
Natural seawater and artificial sea salts (Instant
Ocean) dissolved in deionized water were used in CT
systems for L.O. 1982 and L.O. 1981, respectively,
and artificial seawater was used exclusively in the
RW system in both experiments. Salinity was main-
tained between 34 and 37°/<x>. Trace elements were
supplemented regularly with Wimex Trace Ele-
ments. Temperature was maintained at 15°C unless
otherwise noted. The pH was maintained between
7.8 and 8.2, and low pH was corrected by the
gradual addition of sodium bicarbonate.
Temperature and salinity were measured daily,
pH every other day, and metabolic waste products
(ammonia, nitrite, and nitrate) were measured week-
ly. Ammonia-nitrogen levels were determined by the
Solorzano method (Strickland and Parsons 1972),
and nitrite-nitrogen was determined by the Shinn
method (applied to seawater by Bendschneider and
Robinson in Strickland and Parsons 1972). Nitrate-
nitrogen levels were determined using a prepacked
Hach reagent kit.
Various live food organisms were fed to the squid
several times daily throughout the experiments.
Live planktonic organisms such as zooplankton
(mainly copepods) and small mysidacean shrimp
(Mysidopsis almyra) were the primary foods dur-
ing the first 60 d in the CT system. Brine shrimp,
Artemia salina; larval red drum, Sciaenops
ocellatus; and mysis stage penaeid shrimp were fed
as supplemental foods. Food organisms were added
to the CT system four or five times daily. Thereafter
773
in the RW system, adult mysids; palaemonid shrimp,
Palaemonetes pugio; and a variety of marine or
estuarine fishes were fed to the squid at least twice
daily.
Zooplankton were washed carefully in clean sea-
water. Mysids and palaemonid shrimp were treated
overnight with quinacrine, while erythromycin
and/or tetracycline were used to treat fish (Yang
et al. 1980b, 1983a, b). Before feeding, all foods
were counted or weighed and slowly acclimated
to the temperature and salinity of the cultured
water.
Dead squid and dead food organisms from
previous feedings were removed by siphoning once
or twice daily from the CT or RW systems. Daily
food consumption in the RW was derived by sub-
tracting the weight of uneaten food remains siph-
oned each day from the weight of food organisms
added daily to each culture system. Daily feeding
rate (wet weight) is expressed as the percentage of
food consumed by the total estimated biomass of the
squid. Daily biomass of squid was estimated by
multiplying the number of live squid on a given day
by the average weight of an individual squid on that
day. Daily squid weight estimates were projected
from linear regression of the weights of freshly dead
squid against time. All measurements and wet
weights (WW) were usually made with freshly dead
squid although live squid were occasionally used.
Badly damaged or partially cannibalized squid were
not measured or weighed for this analysis. The ini-
tial squid population was derived from the number
of dead or sacrificed specimens removed from the
culture systems.
Overhead fluorescent lights provided illumination.
In the CT systems for both experiments there was
constant light that measured 11 to 15 lux in the mid-
dle of the water column. In the RW systems there
was also constant light although light only filtered
in through plastic-covered holes in the polystyrene
tops. In L.O. 1981 it measured 17 lux in the center
of the RW and 0.5 to 0.7 lux at each end. In L.O.
1982 it measured 4 to 7 lux near the ends under the
opaque top and 11 lux near the center where light
passed through the clear plastic.
Statoliths from hatchlings of known age in L.O.
1982 were dissected from the squid and decalcified
in a 1:1 mixture of 4% EDTA in distilled water and
0.2 H sodium cacodylate buffer (pH 7.4). Decalcifica-
tion facilitated the counting of rings in statoliths
from squid age 65 d or younger, but older statoliths
were distorted by the process. The rings were
counted from photographs taken with a Leitz Com-
biphot II and Kodak copy film #4125.
FISHERY BULLETIN: VOL. 84, NO. 4
RESULTS
Water Quality
There were no obvious differences in growth or
survival between squid cultured in artificial sea-
water (L.O. 1981) and filtered natural seawater
(L.O. 1982). Water quality in the CT systems was
maintained in very good condition due to the short
culture period, while water quality in the RW system
was more difficult to maintain because of the long
grow-out period and the greater biomass of squid
and food organisms. In L.O. 1981 (Fig. 2) from days
180 to 190 the estimated total biomass reached the
maximum peak of 1,706 g (cf., Fig. 7), which is
equivalent to 155 g/m3 of rearing water volume.
After the 160th day, food organism biomass in-
creased to between 300 and 400 g/day. As a result,
the amount of nitrate-nitrogen gradually accu-
mulated to over 23.0 mg/L during the period from
day 180 to day 193 (Fig. 2). On day 164, 1,900 L
(17% of total volume) of fresh Instant Ocean was
replaced in this system. However, the nitrate-
nitrogen level did not drop in proportion to the per-
cent water change. Concurrently, pH dropped to
7.75 by day 169 and dissolved sodium bicarbonate
(Atz 1964; Bower et al. 1981) was introduced to the
system to adjust the pH above 7.9. The sodium bicar-
bonate solution required very strong aeration to be
effective when it was put into the culture water. A
similar trend of slightly increased nitrate-nitrogen
and decreased pH occurred (about day 200) in L.O.
1982 (Fig. 2). This was corrected in the same
manner.
The vegetative macroalgae, Gracilaria tikvahiae,
was cultured in the water conditioning tank of the
RW system in L.O. 1982 to remove ammonia and
prevent the accumulation of nitrate-nitrogen, but
its effectiveness was not clear.
Incubation and Hatching of Eggs
Average hatchling size in both experiments was
2.7 mm ML (range 2.3-2.8 mm ML) with a hatching
success of over 90%. In L.O. 1981, hatching began
on 14 October and lasted until 17 October. Embry-
onic development required 27 to 30 d at 15 °C. The
hatching period lasted 4 d, compared with L.O. 1982
that took 5 to 6 d. The period of embryonic develop-
ment in L.O. 1982 was not precisely known because
the eggs were collected in nature. Development of
eggs within the same egg cluster was different de-
pending upon the capsule position within the cluster.
Moreover, hatching time within the same capsule
774
YANG ET AL.: CULTURE EXPERIMENTS OF LOLIGO OPALESCENS
differed, since distal embryos usually hatched first.
Since we used early stage eggs removed from their
habitat in California, no polychaete worms (Capitella
ovincola) were observed in the egg capsules (cf.,
McGowan 1954), although we had observed worms
in other late stage California egg capsules.
During embryonic development, granules or
crystals appeared in the perivitelline fluid of some
eggs, but no significance to survival or development
could be associated with this condition. The outer
tunics of the egg capsules incubated in Instant
Ocean were more elastic until the later stages
(around stage 27) than those incubated in natural
seawater. More bacteria and other benthic or-
ganisms grow on the capsules incubated in natural
seawater. These differences did not influence devel-
opment or hatching success. Embryos near hatch-
ing (stage 29) generally moved little or were nearly
static, but in most individuals the external yolk sac
was already broken off within the egg. External yolk
sacs were observed on a few hatchlings. In L.O.
1981, bright illumination stimulated hatching in very
late stage eggs and therefore light levels were in-
creased during later stages of egg development in
L.O. 1982.
Foods and Feeding
The species and size of food organisms were
similar in the two experiments. The general progres-
sion of food types began with zooplankton, then
mysidean shrimps, then palaemonid shrimp larvae
and adults, and finally fishes (Fig. 3). The use of
brine shrimp has been curtailed since they were
found to be unattractive to the hatchlings.
The size range of food organisms fed in the first
30 d is large, especially when compared with the size
of 1-d-old hatchlings (2.3-2.8 mm ML, Fig. 4). How-
ever, as shown in Figure 4, the hatchlings have only
small fins and are not strong swimmers; therefore,
feeding on active prey at this stage is not excellent.
A summary of the types and quantities of food of-
fered in the experiments (L.O. 1981 is used as an
example) is given in Figure 5. Large amounts of food
were available to the squid; this was important dur-
ing the first weeks when hatchlings could only cap-
ture food organisms drifting very close to them. The
relationship of hatchling to food organism density
during the first 59-d period in each experiment is
summarized in Table 1. Unfortunately there was no
clear relationship between densities and survival.
For example, in L.O. 1982, there were twice as
many food organisms per squid as in L.O. 1981, but
survival (cf., Fig. 13) was not better. Figure 5 shows
more specifically the number of food organisms fed
daily in L.O. 1981.
The early rearing period in L.O. 1981 and 1982
coincided with the spawning of mysid shrimp in the
Galveston estuaries. Therefore, small mysids with
a total length of about 2.0 mm (Fig. 4B) were abun-
dantly supplied. This was particularly important
since small mysids swim more frequently in the
water column than do adults. Young mysid hatch-
lings were given as food by day 12 in L.O. 1981 and
immediately in L.O. 1982 (Fig. 3). Small mysids
distribute themselves more evenly in the culture
tanks and are easier for hatchlings to capture.
Palaemonetes spp. were fed to juvenile and adult
squid (Fig. 3). Shrimp ranged in size from 2.0 to 25.0
mm. They were graded by size and fed based on size
and availability. Daily siphoned remains indicated
that only the abdominal flesh was consumed, with
the thorax and carapace discarded.
Fish were generally used for juvenile or older
squid. However, fertilized red drum eggs were
available in L.O. 1981, and larvae up to 13-d old (Fig.
4E) were given to the hatchlings. In the two ex-
periments, a total of over 14 fish species of 10
families were fed (Table 2). To determine the diet
preference for fish species, the actual consumption
of fish (i.e., total weight of fish put in tank minus
total weight of fish remains) was compared for a
total of 5 kg fish fed in L.O. 1982 (Fig. 6). The
cyprinodont fish were most preferred (consumption
of 83%). Only small Fundulus spp., smaller than 31
mm (Cyprinidontidae), were fed because large Fun-
Table 1.— The mean density of squid and food organisms per liter of culture water from days
0-30 and 30-59.
Initial
hatchling
population
Day 0-30
Day 30-59
Exp. No.
Squid
No./L
Food
organisms
No./L
Ratio of food
organisms
to squid
Squid
No./L
Food
organisms
No./L
Ratio of food
organisms
to squid
L.O. 1980
L.O. 1981
LO. 1982
864
2,061
1,704
0.46
0.93
0.27
14.2
24.0
14.6
30:1
25:1
54:1
0.35
0.54
0.14
9.4
12.4
5.6
26:1
23:1
40:1
775
FISHERY BULLETIN: VOL. 84, NO. 4
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YANG ET AL.: CULTURE EXPERIMENTS OF LOLIGO OPALESCENS
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778
YANG ET AL.: CULTURE EXPERIMENTS OF LOLIGO OPALESCENS
E'
Figure 4.— Size relationship of hatchling Loligo opalescens and various food organisms fed squid for the first 30-d posthatching. A,
copepod Acartia tonsa; A', copepod Labidocera aestiva. B, hatchling Mysidopsis almyra; B', adult M. almyra. C, mysis stage of
Penaeus spp. D, adult Artemia salina. E, 1-d-old larva of red drum Sciaenops ocellatus, E', 13-d-old larva of S. ocellatus.
dulus spp. competed with the squid for crustaceans
in the tank. Uneaten mullet (Mugilidae) accumulated
to form small schools, that the squid would not ap-
proach or feed upon as readily as fish that swam in-
dividually. Squid consumed 44% of the mullet even
though the amount fed was equal to amounts of
Poecilidae and Sciaenidae, which were consumed
more (72% and 68%, respectively). The food remains
indicated that the squid ate only the flesh of fish,
leaving the head and vertebrae.
Figure 7 gives the estimated daily group feeding
rate (L.O. 1981) based upon the daily biomass of
squid and the daily food consumption from day 108
to day 232. Daily group feeding rate averaged 14.9%
(range 4-29%). Squid biomass reached a maximum
on day 183 and continued high for 11 d before the
779
FISHERY BULLETIN: VOL. 84, NO. 4
GRAMS OF FOOD ORGANISMS (x102)
FED FROM DAY 60 TO 248
CTs
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780
YANG ET AL.: CULTURE EXPERIMENTS OF LOLIGO OPALESCENS
Table 2. — Fish species and size range given as food in all three experiments.
Size
(TL in mm)
L.O.
experiment
Family and species
1980
1981
1982
Family: Clupeidae
Brevoortia spp.
15.0-31.0
—
—
X
Family: Engraulididae
Anchoa mitchilli (Valenciennes)
20.0-25.0
—
—
X
Family: Cyprinodontidae
Adinia xenica
—
—
—
X
Cyprinodon variegatus Lacepede
10.0-28.0
X
X
X
Fundulus spp.
15.0-31.0
X
X
X
Family: Poeciliidae
Gambusia affinis (Baird and Girard)
12.0-28.0
X
X
X
Poecilia latipinna (Lesueur)
22.0-41.0
X
X
X
Family: Atherinidae
Menidia beryllina (Cope)
18.0-52.0
X
X
X
Family: Carangidae
Hemicaranx amblyrhynchus (Cuvier)
—
—
—
—
Family: Gerreidae
Eucinostomus gula (Quoy and
—
—
X
X
Gaimard)
Family: Sparidae
Lagodon rhomboides (Linnaeus)
—
—
X
X
Family: Sciaenidae1
Sciaenops ocellatus (Linnaeus)
1.5-14.5
—
X
X
Pogonias cromis (Linnaeus)
10.0-15.0
—
X
X
Family: Mugilidae
Mugil spp.
18.0-38.0
X
X
X
'There were about six more species of Sciaenidae: minority species were not identified.
-™ FISH MEAT
^^ CONSUMED
□
UNEATEN
REMAINS
<
o
z j CYPRINODONTIDAE^';< ^?^,^^->^w;r :v
iCLUPEIDAE==c
0 10 20 30 40 50 60 70 80 90 100
PERCENT
Figure 6.— Food preference for fishes by squid in experiment L.O. 1982. Total fish weight
fed to the squid was 5.0 kg.
initiation of spawning; biomass then decreased
because of the mortality accompanying spawning.
Squid in L.O. 1982 were fed ad libitum and daily
group feeding rates could not be determined. How-
ever, the average group feeding rate calculated
weekly for L.O. 1982 allowed an estimate of 18.0%
for the daily feeding rate.
781
FISHERY BULLETIN: VOL. 84, NO. 4
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SQUID WEIGHT
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782
YANG ET AL.: CULTURE EXPERIMENTS OF LOLIGO OPALESCENS
Growth
Figure 8 illustrates growth data through the life
cycle for both experiments. At hatching, Loligo
opalescens has a mean mantle length of 2.7 mm, a
wet weight of 0.001 g, and has approximately 100
chromatophores on its body. In L.O. 1981, the
largest reared squid was a male of 113 mm ML and
58 g. In L.O. 1982, the largest reared squid was a
female of 116 mm ML and 63 g. Mean sizes for
adults from the two experiments were 87 mm ML
(Sx = 2.7) and 23.8 g (Sx = 1.9) for 35 males, and
83 mm ML (Sx = 1.9) and 21.2 g (Sx = 1.5) for
58 females.
Growth equations for the squid in L.O. 1981 clear-
ly describe two separate phases of growth. The man-
tle length of squid cultured in the CT system (days
1-56) increased at an exponential rate (ML = 2.121
eo.o2398«. r2 _ o 92) or 2.4% increase per day, while
those cultured in the RW system (days 56-248) grew
logarithmically (ML = 0.2884 t1A95; r2 = 0.97).
Weights were only measured on squid from the RW
(23)
60
50
CT
X 40
O
LU
LU
30
20
10
0
L O 1981
c )- n
- Range
*T~' Standard Deviation
Mean
(3
(1
7)
5)
(22) (7)
L.O 1982
(8)
(20)
12)
T
i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — i — |
50 100 150 200 250
DAYS
"i i i i i i i i i i — i — i — r — i — i — i — i — i — i — | — i — i — n — |
50 100 150 200 250
" L.O. 1981
(51)
C )— n
E
E,
100
- p — Range
_ -I^> Standard Deviation
Mean
(8
5)
1
|
(20)
\ '
1
o
(42) J
11
z
i
LU
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t
LU
50
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r-
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z
(129) 1 I
<
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T
(90) i
0
-(258)1 I
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t — r t i i i i i
L.O. 1982
(62)
(18) J
:18)
(30)
(30) (13)
(20)
;io>
i
i — i — i — i — | — n — i — i — | — i — i — i — i — | — n — i — i — | — n — i — i — |
50 100 150 200 250 50 100 150 200 250
DAYS
Figure 8.— Comparison of growth (wet body weight and mantle length) in experiments L.O. 1981 and L.O. 1982.
783
FISHERY BULLETIN: VOL. 84, NO. 4
system (days 108-248) and the growth curve showed
a logarithmic increase (W = 6.283 x 10"7 tSM0; r2
= 0.92). Hence, younger squid grew at an exponen-
tial rate and growth slowed to a logarithmic rate
in older squid.
Squid exhibited fast exponential growth for the
first 2 mo in L.O. 1982 and slower logarithmic
growth thereafter (Fig. 9). Wet weight data from
live animals in L.O. 1982 indicated a mean growth
rate of 8.35% increase in body weight per day for
the first 2 mo. Mantle length increased 3.19%/day
or the equivalent of 8 mm/month. The squid were
doubling their weight every 8 d and doubling their
length every 21 d. Growth rates declined from
5.6%/day WW at day 60 (and 2.2%/day mm ML) to
1.6%/day WW (and 0.63%/day mm ML) at day 240.
B
.25
3 20
X
a .15
UJ
uJ .10
.05
L.O. 1 982 Live Loligo opalescens
W = 0.0023e° °835 ' r2 = 0 98
V/-I—
20
30 40
DAYS
50
60
50
40
H 30
X
CD
UJ
UJ
20
10
L.O. 1982 Dead Loligo opalescens
W = 0.3894 x 10"7 t3827; r2 = 0.98
E
£
x
h-
o
z
UJ
_J
UJ
<
2
15 - L= 2.73
10
L.O. 1 982 Live Loligo opalescens
,00319 1
V
20
— i —
30
40
DAYS
— i —
50
60
E
E
X
\-
o
z
UJ
<
2
100
50
10
L0. 1982 Dead Loligo opalescens
*#
i —
50
100
150
DAYS
200
235
Figure 9.— Early exponential growth of Loligo opalescens in experiment L.O. 1982: A, Live wet weight, illustrating exponential growth
through day 60. B, Dead wet weight, illustrating logarithmic growth from day 60 to maturity. C, Live mantle length measurements,
showing exponential growth as in A. D, Dead mantle length measurements, showing logarithmic growth to maturity as in B. Numbers
above rectangles indicate actual number of squid measured for that mean.
784
YANG ET AL.: CULTURE EXPERIMENTS OF LOLIGO OPALESCENS
Mean growth was 16 mm/month for this period.
Doubling times for weight increased from 12 d at
day 60 to 42 d at day 240, and for length from 31
d at day 60 to 109 d at day 240.
The length-weight relationships of squid in L.O.
1981 and 1982 are illustrated in Figure 10 and are
compared with data on wild squid (Fields 1965). The
slopes of the curves are slightly higher in laboratory-
reared animals, indicating that these squid are
heavier per unit length than wild squid. Table 3 illus-
trates differences in predicted weights for repre-
sentative mantle lengths from L.O. 1982 data versus
Fields' (1965) data. The length-weight relationship
for males vs. females in L.O. 1981 is shown in Figure
11; no significant differences between sexes were
detected (P > 0.05).
Statoliths from 55 early hatchlings (L.O. 1982)
aged 21 to 79 d (± 5 d) were examined to correlate
statolith ring numbers with the age of individual
70
•3
LU
LU
60
50
40
30
20
10
•••••• L.O. 1981
W = 0.0002 L2-56 r2 = 0.96
n= 104
— L.O. 1982
W = 0.0002 L2-60 r2 = 0.98
n = 81 1
— Wild Loligo opalescens
(Fields, 1965)
W= 0.0013 L2-15
0 — i — i — i — i — i — i — i — i — i — i — i — i
0 20 40 60 80 100 120
MANTLE LENGTH (mm)
Figure 10.— Comparison of length-weight relationship of squid
cultured in L.O. 1981 and 1982, and squid collected in the field
at Monterey Bay, CA by Fields (1965).
Table 3.— Examples of length-weight differences between L.O.
1982 and the data of Fields (1965). Reference Figure 10. ML =
mantle length; WW = wet weight.
L.O. 1982:
Fields
(1965)
ML (mm)
WW (g)
WW(g)
25
50
75
100
125
0.86
1.31
5.22
5.80
15.00
13.90
31.70
25.90
56.60
41.90
squid (Fig. 12). The linear relationship between the
number of rings (R) and the age in days (D) for 43
statoliths aged 21 to 65 d was R = -7.24 + 1.13
D, with an r2 value of 0.90. Counts of rings dif-
fered from the actual age by an average of ±4.2 d
(range -12 to +8 d).
Survival
Figure 13 compares survival in the two experi-
ments. The longest lived squid were 248 d in L.O.
1981 and 235 d in L.O. 1982. Survival dropped below
50% on day 15 in L.O. 1981 and on day 2 in L.O.
1982. In L.O. 1982, the early rapid population reduc-
tion was due to the removal of newly hatched squid
for a different experiment. Mortality rates slowed
after the early heavy population reduction; 10% sur-
vival occurred on day 120 in L.O. 1981 and on day
49 in L.O. 1982. In all cases, mortality gradually
slowed after 60- to 70-d posthatching. Survival
reduction after day 180 in both experiments was
considered to be related to spawning (Figs. 13A, B).
In L.O. 1981 experiment (Fig. 13A), 50% survival
of 391 squid transferred to the large RW system oc-
curred at day 114, but at day 84 for the 129 squid
left in the same small CT system. For example, 10
d after transfer the squid in the CT system had 30%
mortality whereas those in the RW system experi-
enced only 20% mortality. Thus, transferring squid
at about 60 d gave better results by reducing the
mortality from fin and skin damage that accrues in
the smaller CT system.
In the middle of L.O. 1981 (day 108) cannibalism
was observed. The fins and/or posterior mantle were
clearly eaten in some squid; these squid differed
from those that died from fin damage or from
scraping on the bottom of the tank since the latter
developed lesions near the tip of the mantle (Fig.
14). From days 108 to 206 there were 16 partly
eaten squid in the RW system (7% of the popula-
tion on day 108), compared with two squid (of 10
total) in the CT system between days 157 and
172. Slightly higher levels of cannibalism (19%
between days 97 and 191) were observed in L.O.
1982.
785
FISHERY BULLETIN: VOL. 84, NO. 4
Figure 11.— Length-weight relationship of
males versus females in L.O. 1981, compared
with the data of Fields (1965).
35
30
25
20
s 15
h-
X
CD
LLI
LU
10
/ Wild Loligo opalescens (Fields. 1965)
/ W=.0013L215
1 Hi
ob.
h 1-
0 33 40
L.O. 1981
Laboratory reared female Loligo opalescens
W = .0007 L2 31 r2 = 0.88 n = 40
Laboratory reared male Loligo opalescens
W = .0002 L2 59 r2 = 0.96 n = 18
"60~
80 1 00 1 20
MANTLE LENGTH (mm)
Figure 12.— Increase in statolith rings with age (L.O. 1982).
Closed circles represent ring counts of 55 statoliths from L.
opalescens of known-age (21-79 d). Each statolith was counted twice
from different photographs. Unclear exposures (16) were not
counted. The solid line represents a linear relationship of age and
ring numbers. The space between the solid and dashed lines reflects
the 5 d of hatching.
80 r
70
(/)
CD
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60
cc
O
50
DC
III
CQ
40
30-
20
20 30 40 50 60 70 80
ACTUAL AGE (DAYS)
786
YANG ET AL.: CULTURE EXPERIMENTS OF LOLIGO OPALESCENS
NUMBER OF EGG CAPSULES
SPAWNED PER DAY
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787
FISHERY BULLETIN: VOL. 84, NO. 4
Other causes of injury and death in the later part
of RW culture were 1) swimming into the water in-
take pipes, 2) jetting out of the water and hitting
the bottom of the polystyrene tank covers, and
3) colliding occasionally with the walls and slowly
accruing fin damage. The resulting abrasions on the
body and fins (Fig. 14) were probably the main fac-
tor influencing mortality after about 60 d of cul-
ture.
1 or 2 d. They usually had some obvious skin damage
and were probably unable to maintain disciplined
swimming with the school.
Sexual Maturation, Mating,
and Egg Laying
In L.0. 1981, the first signs of sexual maturation
were when chromatophore patterns associated with
Figure 14.— Fin and skin damage that resulted in mortality of cultured squid. A, Epidermis and dermis missing on periphery of fins,
with fin margin thickened from scar tissue. B, More extreme case with damage extended to mantle. C, Excessive skin damage on
ventral mantle caused by scrapping the tank bottom. A hole (arrow) was produced in the mantle wall and prevented jet-propulsed swimming.
Schooling Behavior
The squid were able to hold a swimming position
in the tank between days 41 and 44 in both L.0. 1981
and 1982, corresponding to a mantle length of about
10 mm. In the early phase of RW culture in L.O.
1981 and 1982, squid swam in two or three loose
groups throughout the RW. Later, they schooled
together at both ends. The reasons for this behavior
are unknown, but it may have been related to lower
illumination levels at the RW ends or to the well-
aerated seawater entering the RW at these points.
Individuals not schooling were often found dead in
courting were observed in males. On day 174 two
males showed the "Shaded testis" component of pat-
terning similar to that described in Loligo plei
(Hanlon 1982). Later, other chromatic components
of patterns seen in mature males of Loligo plei were
observed: faint, lateral stripes on the mantle
("Lateral flame"); a discontinuous suture line along
the fin margin ("Stitch work fins"); a clear area in
the dorsal portion of the mantle above the testis
("Accentuated testis").
Maturation and spawning occurred earlier in L.O.
1982 than L.O. 1981 (Fig. 13). The penis was first
recognizable in a 100-d-old male (25 mm ML) and
788
YANG ET AL.: CULTURE EXPERIMENTS OF LOLIGO OPALESCENS
the nidamental gland was observed in a 101-d-old
female (23 mm ML) in L.0. 1981. The penis was first
recognizable in a 93-d-old male (29 mm ML, 1.15 g
WW), and the nidamental gland was observed in a
92-d-old female (33 mm ML, 1.71 g WW) in L.0.
1982. Figure 15 shows that females become mature
at approximately 60 mm ML. This maturation in-
dex is based upon reports by Hixon (1980a) and
Macy (1982) in which the ratio of nidamental gland
length to mantle length is >0.20. Squid this size
could produce fully formed egg capsules. The
smallest male with spermatophores was 71 mm ML
in L.O. 1982.
In L.O. 1981, first mating activity was observed
on day 193. A pair was swimming together, a sec-
ond male interrupted, and a third male grasped the
female in the midmantle area but she jetted away.
On day 197 another pair was swimming together at
the end of the RW and a brief head-to-head mating
was observed. They separated for about 1 min, then
40 r
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*-» I I I I 1 1 1 1 1 1 1 1
0 20 40 60 80 100 120
MANTLE LENGTH (mm)
Figure 15.— Maturation index for females from pooled data of
L.O. 1981 and 1982. Dots with circles indicate sexually mature
females in which the ratio of nidamental gland length to mantle
length is >0.20. See text.
the male grabbed the female by the arms for a sec-
ond time. Drew (1911) illustrated this copulating
position in Loligo pealei. A second mating position
was observed on day 226. A male grasped a female's
mantle one-third of the way from the posterior tip
of the mantle, then he gradually moved to the
female's head near the mantle opening and then let
go. This was done very swiftly and it was impossible
to see if a spermatophore was passed. Freshly dead
females had spermatophores attached around the
sperm receptacle below the mouth after head-to-
head matings. Mating activity was not as closely
monitored in L.O. 1982, but first observations were
several weeks earlier (before day 175).
Spawning started on day 196 and lasted till day
239 in L.O. 1981. Of 151 egg capsules, 24 (16%) were
unfertilized (Table 4). Squid kept in the CT system
(3°C higher temperature from day 125) spawned
first on day 185, 11 d earlier than the RW system,
but none were fertile. Spawning occurred earlier in
L.O. 1982, beginning day 175 and ending day 222.
All of the 199 spawned capsules were infertile. The
maximum number of spawned capsules in a single
day was 27 on day 203 (Fig. 13B). Most eggs were
collected in the morning indicating that spawning
Table 4.
—Spawning date and n
umber of egg
capsules
spawned
in the raceway system (L.O.
1981).
Capsules
Month/
Age/
Capsules
without
day
day
spawned
eggs
05/01
196
3
0
05/03
198
2
0
05/04
199
5
0
05/05
200
6
0
05/06
201
1
0
05/08
203
1
0
05/09
204
6
0
05/10
205
5
0
05/16
211
5
1
05/17
212
8
0
05/19
214
5
2
05/20
215
3
3
05/21
216
17
8
05/22
217
17
2
05/23
218
14
0
05/24
219
7
0
05/25
220
3
0
05/26
221
6
0
05/27
222
3
0
05/28
223
7
2
05/29
224
6
1
05/30
225
1
0
05/31
226
2
1
06/02
228
5
2
06/03
229
4
2
06/11
237
5
0
06/12
238
4
0
Total 151
24(16%)
789
FISHERY BULLETIN: VOL. 84, NO. 4
took place mainly at night, but some individuals
spawned during the day. Egg capsules in the early
portion of the spawning period were small, with a
length of 2.2 to 4.7 cm when laid. Superficially there
were no differences with normal capsules, but usual-
ly the early ones contained only a few eggs while
a few had none. Typical newly laid egg capsules
were between 6.0 and 9.0 cm and contained an
average of 156 eggs (range 107-199). These egg cap-
sules were normal in length and egg number com-
pared with L. opalescens in nature (Hixon 1983).
A large number of typical egg capsules were in-
cubated and a normal second generation hatched.
The average mantle length of second generation
hatchlings was 2.3 mm ML (range 1.9-2.7 mm ML,
n = 13). This was smaller compared with first
generation hatchlings (average 2.7 mm ML) but
there was no difficulty in rearing them on copepods
for 10 d. Since initial survival was confirmed, fur-
ther rearing ceased.
In L.O. 1982, three patches of artificial egg cap-
sules made of silicon glue were placed on the bot-
tom of the RW tank to stimulate spawning. The
squid spawned 15 fertilized egg capsules around the
artificial capsules (Fig. 16).
DISCUSSION
Water Quality and System Design
Water quality was consistently good throughout
both experiments and was probably a major con-
tributor to culture success. The CT systems were
particularly clean (Fig. 2) because the water volume
was relatively large for the small biomass of animals.
In the large RW system, water quality changed only
slightly when the biomass of squid and food or-
ganisms reached its maximum from approximately
days 150 to 220 (Figs. 2, 5, 7). The highest total
biomass level was 1,706 g between days 180 and 190
in L.O. 1981, which is equivalent to approximately
155 g/m3 of water. At this point, the nitrate-
nitrogen level reached 23 mg/L, which is still low
[Spotte (1979a) gave a conservative safe level of 20
mg/L for most marine organisms]. Ammonia-nitro-
gen and nitrite-nitrogen levels always stayed below
the recommended safe level of 0.1 mg/L (Spotte
1979a) in both experiments. We know from our re-
cent unpublished data that a drop in pH (which ac-
companies nitrogen level increase; Hirayama 1966)
is more dangerous to squid; therefore, addition of
sodium bicarbonate was necessary to keep the pH
near 8.0. Several improvements in system design
helped improve water quality over our L. opalescens
experiment in 1980 (Yang et al. 1983a), when nitrite-
nitrogen reached 1.22 mg/L and nitrate-nitrogen
reached 39.20 mg/L. These included increased
culture water depth and volume in the RW (5,990
to 8,610 L), increased number of protein skimmers
from 2 to 5 and generally more oyster shell substrate
area for increased biological filtration. Furthermore,
regular addition of trace metals assured high levels
since losses occur through foam fractionation in pro-
tein skimmers (Spotte 1979b) and metabolism of
filter bed bacteria, squid, and food organisms.
Growth and Survival
Growth in L. opalescens is very fast (Figs. 8, 9)
and conforms to a general trend among cephalopods
in which the early life cycle is characterized by rapid
exponential growth, followed by slower logarithmic
growth until reproduction and death (Boyle 1983;
Forsythe and Van Heukelem in press).
Egg development is temperature-dependent and
takes 19 to 25 d at 16.5°C (Fields 1965), 27 to 30
d at 15°C (L.O. 1981, this report) and 30 to 35 d
at 13.6°C (McGowan 1954). Hatching success was
high, and young squid survived several days on in-
ternal yolk. Many squid will feed before internal yolk
is absorbed (Boletzky 1975). The young will feed on
a variety and wide size range of crustaceans and
fishes (Fig. 4). Zooplankton, but especially copepods,
are readily attacked and eaten by very young squid.
It is noteworthy that relatively large mysids could
be fed successfully to hatchlings within the first
week (Fig. 3: L.O. 1982) and for 3 to 4 mo there-
after as a primary food. Mysids are easier to col-
lect and acclimate to laboratory conditions and are
thus attractive to the culturist for pragmatic
reasons. Loligo opalescens hatchlings (2.3-2.8 mm
ML) are much larger than those of L. pealei (1.7 mm
ML) or L. plei (1.6 mm ML) (McConathy et al. 1980)
and are consequently easier to rear because larger
food organisms can be used immediately. Larval fish
were attractive to young squid but are difficult to
provide.
Major mortality occurred within 10 d posthatch-
ing. Although high food densities and variety were
provided (Tables 1,2; Figs. 3, 4, 5), many squid ap-
peared to have difficulty making the transition from
passive yolk absorption to active feeding on live
organisms. A learning process may be involved,
because capturing copepods was initially difficult
(squid have been observed to miss 40 times con-
secutively) and improved when squid attacked from
behind. Past experience (cf., Yang et al., 1983a) sug-
gested that increasing food abundance relative to
790
YANG ET AL.: CULTURE EXPERIMENTS OF LOLIGO OPALESCENS
Figure 16.— Fertilized egg capsules laid at the base of artificial silicon egg capsules (erected).
791
FISHERY BULLETIN: VOL. 84, NO. 4
squid abundance would enhance survival, but no
change has been observed. Further experimentation
is required, but a central question is whether many
squid are genetically unfit to survive or whether we
have not yet provided the proper foods and environ-
ment for good survival. Although the former pros-
pect seems unlikely from the evolutionary viewpoint,
our experimental design has certainly promoted
outstanding growth in surviving squid.
With the growth data from live squid in L.0. 1982,
we confirmed that squid grow exponentially both by
weight and length during the first 2 months (Fig.
9). Weight increases at a rate of 8.35% body
weight/day (doubling their weight every 8 d) and this
compares very favorably with octopods (4-7%), other
squid (5-7%), and cuttlefishes (5-12%) (Forsythe and
Van Heukelem in press). Logarithmic growth dur-
ing the rest of the life cycle also conforms general-
ly to other cephalopods, except that some cepha-
lopods have a longer exponential growth period up
to one-half their life cycle (Forsythe and Van
Heukelem in press). The length-weight relationship
(Figs. 10, 11) generally conforms to those of wild-
caught squid, but indicates that laboratory-reared
squid weigh more per unit length (Table 3), possibly,
as a result of reduced swimming. The slopes of the
lines (all <3.0) indicate allometric growth (Forsythe
and Van Heukelem in press). The estimated feeding
rates of 18.0% body weight/day (days 121-176) in
L.O. 1982 and 14.9% (days 108-230) in L.O. 1981
compare well with the estimate of 14.4% (on a dry
weight basis) for L. opalescens of a similar size in
the natural population (Karpov and Cailliet 1978).
Younger L. opalescens (48-56 d) fed on Artemia
were estimated by Hurley (1976) to feed at rates of
36 to 80%/day (dry weight). Another loliginid squid,
Sepioteuthis sepioidea, had feeding rates of 20 to
25% (wet weight) between days 70 and 105 (La Roe
1971). Other squids of similar size show comparable
rates: Loligo plei, 10 to 18% (Hanlon et al. 1983);
L. pealei, ca. 11% (Macy 1980); Illex illecebrosits, ca.
10% (Hirtle et al. 1981); and Todarodes pacificus,
ca. 24% (Soichi 1976).
Maximal survival and size in our three major ex-
periments were L.O. 1980 - 233 d, 77 mm ML (Yang
et al. 1983a); L.O. 1981 - 248 d, 113 mm ML; L.O.
1982 - 235 d, 116 mm ML. Figure 13 illustrates sur-
vival throughout these experiments and shows that
there was a long, steady mortality after the initial
high mortality of the first 2 wk. Once in the RW
systems (i.e., after 2 mo) most mortality was attrib-
uted to fin and skin damage (Hulet et al. 1979; Fig.
14) that accrued slowly from colliding with the sides
of the tank. The painted designs on the walls were
clearly helpful in reducing wall collisions but damage
over time was lethal in many squid. Cannibalism ac-
counted for a minor number of deaths (ca. 7-10%)
Most mortality after day 170 in L.O. 1981 and L.O.
1982 was due to 1) sexual maturation and spawn-
ing and 2) an unusual situation where fully mature
females scraped the bottom of the tank often enough
to wear a large lesion through the ventral mantle
(Fig. 14C).
It should be noted that survival rate was greater
where large tanks such as the RW were used. In
L.O. 1981 (Fig. 13A), 50% survival of squid left in
the smaller CT system occurred only on day 84
compared with day 114 for those transferred to the
RW.
In summary, growth was excellent, indicating that
estuarine foods were sufficient and that system
design and water quality were conducive to growth,
especially in the first 2 mo. Survival was good from
the historical perspective (cf., Arnold et al. 1974;
Yang et al. 1983b) but rather poor from the produc-
tion standpoint. A recent hypothesis concerning
temperature effects on growth (O'Dor and Wells in
press) indicates that higher temperature in the first
half of the life cycle and lower temperature in the
latter half may enhance growth and survival of
laboratory-reared squid. In future work it would be
desirable to enhance growth during the latter half
of the life cycle and to provide an environment in
which somatic growth continues for a longer period
before sexual maturation occurs.
Behavior
Squid are generally sensitive laboratory animals,
responding very quickly with their sophisticated sen-
sory systems to any fast environmental change.
They habituate to many daily disturbances in the
tank system (e.g., tank cleaning, etc.) provided
everything is done slowly. Later in the life cycle they
become slightly less sensitive.
Hatchlings were positively phototaxic and often
swam at the water surface. In nature, young squid
have been caught mainly by plankton nets mounted
on a sled and towed along the bottom (Recksiek and
Kashiwada 1979). It is not possible at this time to
explain the movements of hatchlings in nature based
upon laboratory observations of positive phototaxis.
A key component in feeding behavior was move-
ment by the prey, regardless of the size or age of
the squid or food organisms. Young squid preferred
copepods but ate a variety and a very wide size
range of organisms (Fig. 4). In general, the squid
preferred crustaceans over fish, but the relatively
792
YANG ET AL.: CULTURE EXPERIMENTS OF LOLIGO OPALESCENS
restricted diet offered to them may have influenced
that. Fields (1965) and Karpov and Cailliet (1978)
agreed that L. opalescens adults prefer fish over
crustaceans but there was no clear-cut preference
in younger squid. It is clear from laboratory obser-
vations that squid learned to associate certain events
with feeding (e.g., opening the tank top), and the
general level of activity increased markedly during
these periods. We were also able to stimulate
feeding in the CT systems by dimming and bright-
ening the lights to attract the planktonic food
organisms into the water column near the squid.
Schooling behavior was correlated with size.
Larger body size and growth of the fins were re-
quired before squid could swim in place against a
current; this occurred at about 10 mm ML (41-44
d in L.O. 1981 and 1982). Hurley (1976) reported
that L. opalescens 4 to 5 mm ML could briefly form
loose schools when disturbed, but this may have
been in static water. At 15 mm ML, L. opalescens
were powerful enough to form distinct schools (Yang
et al. 1983a), indicating the size at which one could
expect schooling to appear in nature. How and why
squid begin schooling in nature has not been
investigated.
Cannibalism was not seen in L.O. 1980 (Yang et
al. 1980b, 1983a) and accounted for 7 to 19% of mor-
talities in experiments L.O. 1981 and 1982. Lack of
food did not precipitate this behavior. On the spawn-
ing grounds in Monterey, CA, mature squid often
have cephalopod remains in their stomachs (Lou-
kashkin 1977; Karpov and Cailliet 1978); in one case
as many as 75% of males had squid remains in their
stomachs (Fields 1965). This could be a behavioral
response to overcrowding (Fields 1965) or to restrict
prey organisms on the spawning grounds. We anti-
cipate that cannibalism in tanks would be a signi-
ficant problem only during prolonged food shortage
or if squid of a very wide size range were in the same
system (cf., Hanlon et al. 1983).
Body patterning was not studied in great detail
but several observations are noteworthy. Young
animals are capable only of simple chromatic expres-
sion such as "All dark" or "Clear". When excited,
L. opalescens of all sizes show some degree of dark-
ening; this is similar to other loliginid squids (cf.,
Hanlon 1982; Hanlon et al. 1983). By the time the
squid are approximately 80 to 100 mm ML they can
show a repertoire that includes about a dozen
chromatic components of patterning (e.g., Dark arm
tips, Ring on the mantle, etc.). This places L.
opalescens in a category of rather simple pattern-
ing, making it comparable to L. pealei and L.
vulgaris, slightly more complex than Lolliguncula
brevis (Dubas et al. 1986), but simpler than Loligo
plei (Hanlon 1982; Hanlon et al. 1983). Further
analysis is warranted because much behavior is ex-
pressed through patterning and may yield impor-
tant behavioral clues.
Social behavior was first manifest in schooling (see
above) then much later in mild intraspecific aggres-
sion. Occasionally two squid would fight over one
fish, but the first firm observations came at the time
of sexual maturation when mating was seen. As
Hurley (1977) noted, there were no obvious inter-
actions among males to form a dominance hierarchy
for mate selection. Mating was initiated by males,
and both typical forms of mating were observed:
"head-to-head" matings in which spermatophores
were stored in the bursa copulatrix; and male-
underneath matings in which spermatophores were
deposited in the mantle near the oviduct (cf., Drew
1911; McGowan 1954; Hurley 1977). Females mated
promiscuously as they do in nature, and females
were also stimulated visually to lay eggs around ar-
tificial facsimiles of egg mops (Fig. 16). Males were
not observed to guard or defend egg capsules as
described by Hurley (1977), but this may have been
because relatively few egg capsules were left in the
tank each day.
Reproduction
In L.O. 1980 only the subadult stage was reached
in 233 d (Yang et al. 1980b, 1983a). Full sexual
maturity was achieved in L.O. 1981 and 1982 and
spawning of viable eggs occurred from days 196 to
239 and 175 to 226, respectively (Fig. 13). Relatively
few egg capsules were laid per female, and these
capsules were generally shorter and contained
slightly fewer eggs per capsule than those reported
from natural populations, but this was probably due
to the smaller size of these spawning females (Hixon
1983).
Laboratory cultured Loligo opalescens matured
precociously and since they are terminal spawners
this prevented attainment of full adult size. In the
laboratory, males as small as 71 mm ML had fully
formed spermatophores and females became sexual-
ly mature beginning at about 60 mm ML (Fig. 15).
In nature, the average adult size is 150 mm ML for
males and 140 mm ML for females, although size
at onset of maturity is variable and can be as low
as 72 mm ML for males and 81 mm ML for females
(Fields 1965; Hixon 1983). Precocious maturation
has also been reported in other squid maintained in
the laboratory (cf., Durward et al. 1980; Hanlon et
793
FISHERY BULLETIN: VOL. 84, NO. 4
al. 1983). The stimuli (or stressors) that cause this
are unknown.
Van Heukelem (1979) reviewed environmental fac-
tors that influence maturation in cephalopods and
reported that light, temperature, and nutrition are
the key stimuli. In our experiments, light was con-
stant (24 h on), temperature was consistent (ca.
15°C) and food was relatively constant and highly
available compared with natural populations. How-
ever, all three conditions are different from nature.
The most interesting result concerns light, which
is thought to have a major effect on maturation
through the light-optic gland-gonad pathway (cf.,
Mangold and Froesch 1977; Wells and Wells 1977).
Long daylength of high intensity is thought to delay
maturation; in our experiments daylength was 24
h but intensity (ca. 4-17 lux) was low compared with
full sunlight. However, we do not know what light
intensity subadult L. opalescens are subject to in
nature. Clearly, long daylength alone does not delay
maturation in L. opalescens. Future experimenta-
tion will be necessary to identify the combinations
of environmental factors that affect maturation in
the laboratory.
Life Cycle Comparisons:
Laboratory vs. Fishery Data
In general, five major rearing attempts have been
successful in varying degrees: 1) Hurley (1976), to
100 d; 2) Hanlon et al. (1979), to 79 d; 3) L.0. 1980,
to 233 d and subadult stage (Yang et al, 1980b,
1983a); 4) and 5) L.O. 1981 and 1982, to sexual
maturity and egg laying within 8 mo (this report).
From this it is clear that the life cycle can be <1 yr
under laboratory conditions.
Fields (1965) stated, based upon fishery data, that
"Almost all females spawn at the age of 3
years...." However, more recent field (cf.,
Recksiek and Frey 1978) and laboratory studies of
L. opalescens (above) indicate that life span
estimates beyond 2 years are excessive. Further-
more, recent books on cephalopod life cycles (Boyle
1983, in press) indicate that few squid live beyond
2 years.
Growth information on laboratory populations is
now quite good. The present data allow an accurate
assessment by weight from hatching onwards (Fig.
9) and firmly verify that young squid are capable
of dramatically fast, exponential growth when food
is not limiting. This indicates that in nature squid
are capable of exploiting plankton blooms and other
instances of greater food availability; the highest
feeding rates we estimated (29%) also confirm field
observations that squid will eat large quantities of
food when available and when necessary. Field
estimates of growth by Fields (1965) and Spratt
(1978) are compared with laboratory data in Figure
17. Field's data are very conservative (averaging 4
mm/month) and based only upon monthly modal
length-frequency diagrams from squid on or near
spawning grounds. Spratt (1978) estimated growth
from statolith rings and hypothesized that growth
is rapid during the first few months then decreases
with age. Laboratory growth was much faster, but
animals were not subject to environmental fluctua-
tions. We estimate that growth in nature approx-
imates something between the laboratory data and
Spratt' s data, and that date of hatching, seasonal
temperature fluctuations, and food availability result
in life cycle variations between 1 and 2 years. One
would expect to observe exponential growth of
young squid during spring and summer when tem-
peratures and food availability are high, slower
logarithmic growth in fall and winter, and spawn-
ing the following spring.
Field evidence (McGowan 1954; Fields 1965) and
reproductive physiology studies (Grieb and Beeman
1978; Knipe and Beeman 1978) indicate that L.
opalescens is a terminal spawner (Hixon 1983), and
our laboratory observations verify this since all
animals died shortly after spawning (Fig. 13).
Rings in statoliths may eventually be used as a
reliable age marker to determine growth rate and
life span. Our preliminary results in this paper from
43 statoliths of known age support Spratt's (1978)
conclusion that ring deposition occurs roughly on
a daily basis during the first 65 d. However, our
laboratory data indicate that the relationship does
not hold well beyond that age, although Spratt sug-
gested that daily ring deposition occurs up to 150
d. Thereafter, Spratt (1978) hypothesized lunar
(monthly) rings on statoliths but there are no lab-
oratory data for comparison. Daily, fortnightly, or
monthly growth rings have been hypothesized in the
squid Gonatus fabricii (Kristensen 1980), Todarodes
sagittatus (Rosenberg et al. 1981), Illex illecebrosus
(Hurley and Beck 1980), and Loligoforbesi (Martins
1982), but there are no hard data to confirm these
estimates. The mechanism of ring formation is
unclear but may be related to feeding, since in this
part of our laboratory study the squid received food
during 12 h and none for the next 12, while concur-
rently there was constant light and no temperature
fluctuation (Hixon and Villoch 1984). Hurley et al.
(1985) and Dawe et al. (1985) found evidence of daily
rings in statoliths by inoculating squid with tetra-
cycline or strontium. Further work is required to
794
YANG ET AL.: CULTURE EXPERIMENTS OF LOLIGO OPALESCENS
175 -i
150-
125-
| 100-
2
75-
50-
25
Yang, unpublished
Yang eta/. (1980)
Spratt (1978)
Fields (1965)
—r-
9
—i —
12
— i —
15
18
21
— i —
24
Age (mths)
Figure 17.— From estimates of growth rate in mantle length oiLoligo opalescens. Fields (1965) used
population data. Spratt (1978) combined age (statolith ring counts) and ML data and calculated a
mean (horizontal line), range (vertical line) and standard deviation (vertical bar) values for 3-month
intervals throughout the life cycle. Yang et al. data are from laboratory rearing studies (1980b, 1983a,
this report) (modified from figure 7.1, Hixon 1983).
determine if and how statolith rings are correlated
with age.
A major gap in fisheries studies concerns where
the hatchlings go from the spawning grounds. Very
few young squid have been captured (Okutani and
McGowan 1969; Recksiek and Kashiwada 1979) even
in the vicinity of spawning grounds. Hatchlings are
positively phototaxic and this may serve to disperse
them immediately from the spawning grounds.
Thereafter their movements are unknown, although
rarely young squid 3.5 to 7.0 mm ML have been
caught in neritic plankton samples, usually at depths
of 25 to 40 m nearshore in water between 12.5° and
21.0°C (Okutani and McGowan 1969). Detailed
knowledge of water currents between spawning
grounds and nearshore, combined with monitoring
of plankton abundance (especially copepods and lar-
val fish) by surface, bottom and oblique tows may
provide important clues about movements and feed-
ing patterns of young-of-the-year squid. Laboratory
studies indicate that squid can swim well enough to
hold their position against a current by 10 mm ML,
or about 40 to 45 d posthatching. By 15 mm ML (ca.
60-80 d) they can form and maintain well-formed
schools. The functions of schooling in nature prob-
ably relate to defense, feeding and migratory
behavior.
The California squid fishery has nearly collapsed
since El Nino of 1983, and the squid population has
been generally displaced northward as far as south-
ern Canada. Some small spawning populations are
still present in southern and central California. It
may be rewarding to investigate feeding and migra-
tory patterns of young and adult squid to better
understand population recruitment into this ecologi-
cally and economically important fishery resource.
Biomedical Research Applications
Loligo opalescens has proved to be a suitable model
for giant axon preparations (e.g., Llano and
Bezanilla 1980). However, for most axon experi-
ments the largest axons (>400 fim diameter) are
needed; this requires the largest squid taken in the
fishery, usually 150 mm ML and larger. Our largest
squid, 116 mm ML, had an axon about 240 ^m in
795
FISHERY BULLETIN: VOL. 84, NO. 4
diameter. Unknown factors in our laboratory en-
vironment resulted in precocious sexual maturation
and thus smaller animals. Therefore, we are now
evaluating the culture potential of Loligo forbesi, a
much larger squid from the eastern Atlantic, since
precocious maturation in that species would still
result in axons >500 /urn. Preliminary experiments
bear out this proposition as we have recently
cultured L. forbesi to 140 mm ML and 400 \xm
diameter axons. However, L. opalescens would be
an excellent model for the giant synapse preparation
in which smaller squid are most suitable. Therefore,
L. opalescens, with a now substantial amount of
culture information, may be a highly suitable species
in the United States for providing squid on a con-
sistent basis for neuroscience research. Moreover,
the recent disappearance of L. opalescens (1983-85)
from traditional fishing grounds in California make
laboratory culture an attractive alternative for
animal supply.
ACKNOWLEDGMENTS
We acknowledge funding from DHHS grant
RR01024, Division of Research Resources, National
Institutes of Health, and from the Marine Medicine
General Budget 7-11500-765111 of The Marine Bio-
medical Institute, The University of Texas Medical
Branch. We especially appreciate the assistance of
John W. Forsythe on the rearing experiments and
the growth data analyses. We also thank Joseph P.
Hendrix Jr. for assistance in rearing and Lea A.
Bradford for water analyses and data gathering.
Connie Arnold and Joan Holt of the Port Aransas
Laboratory, University of Texas, kindly supplied the
red drum eggs. We are grateful to Aquabiology
(Seibutsu Kenkyusha Publishing Co., Tokyo) for per-
mission to reprint several figures. Academic Press
Inc. kindly gave us permission to use a modification
on Figure 17. Phillip G. Lee kindly read and im-
proved the final draft.
Note: We dedicate this paper to our coauthor and
dear friend Dr. Raymond F. Hixon, who passed
away on 19 March 1984 as he valiantly fought to
recover from chronic myelogenous leukemia.
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798
FISH ASSEMBLAGES IN MACROCYSTIS AND NEREOCYSTIS
KELP FORESTS OFF CENTRAL CALIFORNIA
James Lee Bodkin1
ABSTRACT
The abundance and species composition of conspicuous fishes were compared within two canopy forming
kelp forests (giant kelp, Macrocystis pyrifera, and bull kelp, Nereocystis luetkeana) in Central Califor-
nia. The primary investigative method was a subtidal belt transect, in which visual observation was used.
The species composition of fish assemblages in the two canopy types was similar. Densities of fish were
generally greater in Macrocystis than in Nereocystis forests. The major difference was the density of
midwater species of the genus Sebastes. The blue rockfish, Sebastes mystinus, was the numerically domi-
nant species in both canopy types. Estimates of the biomass of fish were about 2.4 times greater in
Macrocystis beds than in Nereocystis beds.
Many species of fish exhibit an affinity for substrate
and cover within their habitat, such as rock or coral
reefs or kelp beds, as well as man-made objects such
as piers, jetties, and offshore oil platforms. This
structure may provide shelter, a base for foraging
activity, or nursery habitat for young fish. Within
the temperate nearshore marine environment,
macroalgae may provide a large portion of this
substrate and cover. Kelp forests are one of the
major features of the nearshore environment along
the west coast of North America. The two most con-
spicuous canopy-forming kelps are the giant kelp,
Macrocystis pyrifera, a perennial, and the bull kelp,
Nereocystis luetkeana, an annual (Abbott and
Hollenberg 1976). Besides the difference in peren-
nial versus annual growth pattern, Macrocystis and
Nereocystis differ markedly in physical structure
(Fig. 1) and seasonal patterns of abundance. Macro-
cystis plants typically have many stipes originating
from a single large holdfast, and large fronds at-
tached to each stipe throughout its length. Nereo-
cystis plants consist of a single stipe, with large
fronds only at the distal end. During periods of full
development (typically late summer), Macrocystis
can develop a completely closed canopy, whereas
Nereocystis typically has a broken canopy. Winter
storms usually remove large portions of the Macro-
cystis canopy, but many plants remain secured to
the substrate and provide structure within the water
column to varying depths throughout the year.
Nereocystis canopies are also typically removed dur-
iU.S. Fish and Wildlife Service, P.O. Box 70, San Simeon, CA
93452.
ing these storms, and, because Nereocystis is an
annual, it provides little or no structure from mid-
winter through late spring.
Nereocystis may be more abundant than Macro-
cystis in the presence of severe and persistent
disturbances such as continued exposure to large
swells or heavy grazing pressure (Dayton et al.
1980). In the absence of this pressure, Macrocystis
may be competitively dominant, in that it forms a
dense and often complete surface canopy earlier in
the year, and thus may exclude or limit Nereocystis
which has light-sensitive germination requirements
(Dayton et al. 1980, 1984).
This study was designed to test the hypothesis
that the fish component of the Macrocystis pyrifera
community differs from that of the Nereocystis luet-
keana community in Central California.
METHODS
Studies were conducted from 6 km south to 15 km
north of Point Piedras Blancas, San Luis Obispo
County, CA (lat. 35°40'N, long. 121°17'W) (Fig. 2).
Additional studies were also done near Big Creek,
Monterey County, CA Gat. 36°04'N, long. 121°36'W).
The surface canopies of kelp beds consist almost ex-
clusively of Nereocystis from Point Piedras Blancas
north to Ragged Point, an area about 13 km long,
but are dominated by Macrocystis south of Piedras
Blancas. I searched 74 transects in the Piedras
Blancas study area and 4 in the Big Creek area: 26
transects in Macrocystis forests and 14 in Nereo-
cystis in 1982 and 17 in Macrocystis and 21 in Nereo-
cystis in 1983. Field studies extended from June
Manuscript accepted March 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
799
FISHERY BULLETIN: VOL. 84, NO. 4
01
he
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BODKIN: MACROCYSTIS AND NEREOCYSTIS KELP FORESTS
N
Ragged Pt.
Pt. Sierra Nevada
Pt. Piedras Blancas
Figure 2 . — Location of areas sampled . Piedras
Blancas Pt., south, to San Simeon Pt.: kelp
canopies are dominated by Macrocystis pyrifera.
Piedras Blancas Pt. north, to Ragged Pt.: kelp
canopies are dominated by Nereocystis luetkeana.
Big Creek (not shown) is about 38 km north of
Ragged Pt.
'■:■■ *&K--
• San Simeon
10 km
1982 to October 1983. Transects were apportioned
evenly throughout early summer to late fall in each
of the forest types.
A belt transect, as described by Brock (1954) and
modified by Quast (1968), was used with the aid of
scuba to conduct subtidal fish surveys. Each survey
consisted of two components, benthic and midwater.
A 50 m fiberglass tape was extended across the
ocean floor in differing compass courses, extending
from eye bolts permanently embedded in the sub-
strate, or from the anchor of a dive boat on hap-
hazardly located transect sites. The width of the
midwater transect was determined by measuring
the horizontal water visibility 2 m above the sub-
strate. This was done by sighting down the transect
line (fiberglass tape) toward the zero end, where a
small bicolored float (13.5 x 5.5 cm) was suspended
2 m off the bottom. The observer moved away from
the float along the line. When the float could not
be readily discerned, the position on the tape was
recorded. This value was doubled (to include obser-
vations on either side of the transect line) to obtain
the width of the midwater transect. This survey
technique may lead to a slight underestimation of
fish densities due to decreasing searching efficiency
with increasing distances from observer to observed
(Caughley 1977). Surveys were conducted only when
visibility exceeded 4.4 m. Horizontal water visibil-
ity ranged from 4.4 to 12.1 m (Macrocystis x =
6.6 m, SE = 2.6; Nereocystis x = 7.4 m, SE =
0.49). The width of the benthic survey was 4 m (2
m on each side of the transect tape). All sampling
801
FISHERY BULLETIN: VOL. 84, NO. 4
wasconducted beneath and within either of the two
forest types, in water 6 to 22 m deep. Underwater
observations were recorded on formated data sheets
using plastic paper.
In conducting the benthic survey, I slowly swam
from one end of the transect to the other and iden-
tified and enumerated the fish that were observed.
A fish was included in the benthic survey if it was
observed within 0.5 m of the bottom and was not
a member of a school of typically midwater fish
located momentarily near the bottom. A fish ob-
served swimming through the transect in front of
the diver was included. An effort was made to in-
spect all crevices, caves, and ledges, and to move
aside algae to locate fish. A description of unfamiliar
fish was made in the field and its identity later deter-
mined in field guides if possible. Small, relatively
cryptic species were probably underestimated in the
process of these visual surveys (Brock 1982).
The midwater transect was searched about 3 m
above the tape. Repetitive ascents and descents
were made at 5 m intervals to detect fish occurring
throughout the water column. The sizes of very
large schools were estimated. All fish observed
within the length of the 50 m tape were recorded.
Unidentified species were treated as they were dur-
ing the benthic survey.
After the survey was completed, an index of the
bottom profile was recorded by measuring the water
depth at each meter mark along the tape. Two
methods of determining bottom profile were used:
first, an objective, and later, a subjective measure.
The objective relief index was the sum of the dif-
ferences between each of the 50 consecutive depth
measurements along the 50 m transect. During the
second half of this study (1983) a subjective relief
index was assigned to the general vicinity of each
transect; this was determined by the greatest ver-
tical relief observed along the transect line: 0 = flat,
no relief; 1 = low relief <1 m); 2 = moderate relief
(1 to 2 m); 3 = high relief (2 to 4 m); and 4 = ex-
treme relief (more than 4 m).
Two measures of species diversity were used to
compare the fish assemblages in Macrocystis and
Nereocystis forests: 1) total number of species found
on all transects within one canopy type and 2) the
Shannon-Weaver index of diversity, H' (Pielou
1966).
Because of heterogeneity between sample vari-
ances, fish density distributions were compared with
the nonparametric Mann- Whitney test. A minimum
acceptable level of significance of 0.05 was assigned.
RESULTS
Twenty-seven species of fish were identified
within the spatial limits of the transects (Tables 1,
2, 3). An additional 8 species were identified within
the kelp forest, but outside the transect limits.
Juvenile rockfish were considered a single group,
and occasionally an unidentified fish was observed.
In Macrocystis forests, 26 species were identified
within the transects and 10 species outside the
transects; in Nereocystis forests, the respective
totals were 23 and 4 species. Three additional types
of fish were observed that could be identified only
to the family level (Table 3). Four species observed
only in Macrocystis forests were white seaperch,
Phanerodon furcatus; rainbow seaperch, Hypsurus
caryi; China rockfish, Sebastes nebulosus; and black-
eye goby, Coryphopterus nicholsi. One species was
observed only in Nereocystis beds, the jacksmelt,
Atherinopsis calif orniensis. Species not observed
within both transect types were relatively uncom-
mon, but were observed in and around both forest
types during this study.
Fishes that could not be identified to species or
family level were rare, occurring on only 6 (8%) of
the transects (Table 3).
Table 1.— Summary of presence/absence of fish species
encountered [midwater (M) and benthic (B), years pooled]
throughout study.
Macro-
Nereo-
Principal
Species
cystis
cystis
habitat
Sebastes mystinus
X
X
M
Sebastes serranoides
X
X
M
Sebastes atrovirens
X
X
M
Sebastes melanops
X
X
M
Sebastes chrysomelas
X
X
B
Sebastes carnatus
X
X
B
Sebastes miniatus
X
X
B
Sebastes rastrelliger
X
X
B
Sebastes caurinus
X
X
B
Sebastes nebulosus
X
B
Sebastes sp. (juveniles)
X
X
M/B
Oxyjulis califomica
X
X
M
Aulorhynchus flavidus
X
X
M
Atherinopsis californiensis
X
M
Phanerodon furcatus
X
M
Oxylebius pictus
X
X
B
Hexagrammos decagrammus
X
X
B
Embiotoca lateralis
X
X
B
Embiotoca jacksoni
X
X
B
Orthonopias triads
X
X
B
Scorpaenichthys marmoratus
X
X
B
Ophiodon elongatus
X
X
B
Rhachochilus vacca
X
X
B
Coryphopterus nicholsi
X
B
Anarrhichthys ocellatus
X
X
B
Jordania zonope
X
X
B
Hypsurus caryi
X
B
802
BODKIN: MACROCYSTIS AND NEREOCYSTIS KELP FORESTS
Midwater Transects
Differences in abundance of fish in the Macro-
cystis and Nereocystis forests were most apparent
among the midwater species, primarily within the
genus Sebastes. Of the nine species of midwater fish
(juvenile Sebastes treated as a single "species"),
three were significantly more abundant in Macro-
cystis than in Nereocystis forests: blue rockfish, S.
mystinus; kelp rockfish, S. atrovirens; and olive
rockfish, 5. serranoides (Tables 1, 2). A fourth
species, the black rockfish, S. melanops, was not ob-
served on Nereocystis transects, though it was only
occasionally seen in Macrocystis.
Although there were no general changes in fish
abundance between 1982 and 1983 among the mid-
water species, some individual species differences
were noted. Densities of blue rockfish were signifi-
cantly lower in 1983 than in 1982 (Table 2). During
this same period there was an insignificant increase
in the density of juvenile rockfish. Densities of the
senorita, Oxyjulis californica, appeared to increase
within both forest types in 1983, but the increase
was significant only when canopy types were com-
bined for each year. This annual variation should be
considered in light of the extremely anomolous El
Nino event which occurred during this period (Cane
1983), and may be atypical.
Benthic Transects
Among the 19 principally benthic species found
in both the Macrocystis and Nereocystis benthic
transects, three (16%) were significantly more abun-
dant in Macrocystis forests: Striped seaperch,
Embiotoca lateralis, painted greenling, Oxylebius
pictus, and the gopher rockfish, Sebastes carnatus
(Tables 1, 3). One other species, the kelp rockfish,
which occurred on benthic transects, was considered
as primarily a midwater species. Gopher rockfish are
bathymetrically segregated from the sibling species,
S. chrysomelas (black-and-yellow rockfish). Gopher
rockfish are relatively more abundant at depths >12
to 14 m (Larson 1980). In my study, the densities
of black-and-yellow rockfish increased significant-
ly in the second year while during the same period,
densities of gopher rockfish decreased.
Due to sampling methodology and the occurrence
Table 2.— Mean densities (no. fish/100 m2) and frequency of occurrence of fishes on midwater transects through
kelp (standard error of mean in parenthesis).
Mean densities (fish/100 m2)
Freque
sncv of
i
Macrocystis
Nereocystis
occurrence
Species
1982
1983
1982-83
1982
1983
1982-83
Macrocystis
Nereocystis
Sebastes mystinus"12
19.4
8.25
15.0
6.68
2.09
3.9
1.00
0.82
Blue rockfish
(1.8)
(1.0)
Sebastes serranoides1
0.51
0.36
0.45
0.17
0.07
0.11
0.74
0.34
Olive rockfish
(0.09)
(0.03)
Sebastes atrovirens1
0.19
0.16
0.18
0.007
0.005
0.006
0.44
0.06
Kelp rockfish
(0.05)
(0.004)
Sebastes melanops1
0.03
0.01
0.02
0
0
0
0.16
0
Black rockfish
(0.009)
Sebastes sp.
3.4
7.7
5.1
0.06
0.95
0.59
0.19
0.11
Juvenile rockfish
(3.1)
(0.5)
Oxyjulis californica2
3.1
26.6
12.4
1.6
18.7
11.9
0.40
0.40
Senorita
(6.6)
(6.2)
Aulorhynchus flavidus
0.43
0.014
0.07
0.06
Tube-snout
(0.4)
(0.01)
Atherinopsis californiensis
0
6.0
0
0.20
Jacksmelt
(6.5)
Phanerodon furcatus
1.37
0
0.05
0
White seaperch
(1.4)
Species observed incidental to transects
Scomber japonicus
0
0.09
Chub mackerel
Myliobatis californica
0
0.03
Bat ray
Sphyraena argentea
0.02
0
Pacific barracuda
Torpedo californica
0.02
0
Pacific electric ray
1 Difference significant between Macrocystis and Nereocystis, years combined.
2 Difference significant between years, kelp canopies combined.
803
FISHERY BULLETIN: VOL. 84, NO. 4
Table 3.— Mean densities (no. fish/100 m2) and frequency of occurrence of fishes on benthic transects through
kelp forests (standard error of mean in parenthesis).
Mean densities (fish/100 m2)
Frequency of
Macrocystis
Nereocystis
occurrence
Species
1982
1983
1982-83
1982
1983
1982-83
Macrocystis
Nereocystis
Sebastes chrysomelas1
1.52
1.91
1.67
1.11
2.21
1.77
0.74
0.91
Black-and-yellow rockfish
(0.25)
(0.26)
Oxylebius pictus2,3
1.13
1.35
1.2
0.21
0.79
0.56
0.86
0.51
Painted greenling
(0.1)
(0.1)
Hexagrammos decagrammus
0.33
0.35
0.34
0.36
0.43
0.40
0.44
0.57
Kelp greenling
(0.07)
(0.07)
Sebastes carnatus^2
1.29
0.76
1.04
0.75
0.22
0.43
0.61
0.31
Gopher rockfish
(0.2)
(0.15)
Embiotoca lateralis2
0.63
1.1
0.84
0.25
0.12
0.17
0.58
0.20
Striped seaperch
(0.2)
(0.08)
Sebastes atrovirens2
0.52
0.97
0.70
0.04
0.15
0.11
0.58
0.14
Kelp rockfish
(0.1)
(0.05)
Sebastes sp.
0.87
0.21
0.62
0.23
0.14
0.17
0.42
0.26
Juvenile rockfish
(0.2)
(0.07)
Embiotoca jacksoni
0.39
0.44
0.41
0
0.27
0.16
0.42
0.17
Black perch
(0.1)
(0.06)
Orthonopias triads
0.20
0.23
0.21
0.04
0.13
0.09
0.33
0.14
Snubnose sculpin
(0.06)
(0.04)
Sebastes mystinus
0.08
0.26
0.15
0.04
0.17
0.15
0.23
0.17
Blue rockfish
(0.05)
(0.05)
Scorpaenichthys marmoratus
0.107
0.11
0.16
0.20
Cabezon
(0.04)
(0.04)
Ophiodon elongatus
0.13
0.09
0.21
0.09
Ling cod
(0.04)
(0.04)
Sebastes melanops2
0.209
0.029
0.23
0.06
Black rockfish
(0.06)
(0.02)
Rhachochilus vacca
0.135
0.0149
0.21
0.06
Pile perch
(0.04)
(0.01)
Sebastes miniatus
0.042
0.094
0.07
0.14
Vermilion rockfish
(0.03)
(0.04)
Coryphopterus nicholsi
0.198
0
0.21
0
Blackeye goby
(0.09)
Sebastes rastrelliger
0.0116
0.0143
0.05
0.11
Grass rockfish
(0.01)
(0.01)
Sebastes caurinus
0.035
0.0143
0.07
0.03
Copper rockfish
(0.02)
(0.01)
Anarrhichthys ocellatus
0.023
0.0143
0.05
0.03
Wolf-eel
(0.02)
(0.01)
Jordania zonope
0.014
0.0143
0.02
0.03
Longfin sculpin
(0.01)
(0.01)
Hypsurus caryi
0.034
0
0.05
0
Rainbow seaperch
(0.01)
Sebastes nebulosus
0.019
0
0.02
0
China rockfish
(0.02)
Unidentified fish
0.128
(0.09)
0.29
(0.3)
0.05
0.11
Species observed incidental to transects
Sebastes serriceps
0.02
0.03
Treefish
Cephaloscyllium ventriosum
0.05
0
Swellshark
Sebastes auriculatus
0.02
0
Brown rockfish
Sebastes pinniger
0.02
0
Canary rockfish
Clinidae
0.12
0
Clinids
Cottidae
0.07
0
Sculpins
Gobiesocidae
0.02
0
Cling fishes
Unidentified fish
0.12
0.06
'Difference significant between years, kelp canopies combined.
2 Difference significant between Macrocystis and Nereocystis years combined.
3 Difference significant between years, Nereocystis.
804
BODKIN: MACROCYSTIS AND NEREOCYSTIS KELP FORESTS
of Macrocystis in water up to 4 m deeper than that
occupied by Nereocystis within the study area, the
mean water depth at which surveys were made dif-
fered between sites (Macrocystis mean depth =12.2
m; Nereocystis mean depth = 10. 5m, t = 2.73, P
= 0.008 (two sample £-test)). When the five transects
in Macrocystis which occurred at depths beyond the
maximum depth of Nereocystis transects (16 m)
were excluded from analysis, the difference in water
depths between sites became insignificant. Follow-
ing the removal of these deep transects, all species
of fish, both midwater and benthic, were reevalu-
ated. There were no changes in the results presented
above following this treatment.
There was little correlation between densities of
fish and either of the bottom relief indices (r values,
0.025 to 0.482). Throughout the study, bottom relief
typically ranged from 1 to 4 m and relief <1 m was
not encountered. Mean values of the objective relief
index were 44.1 (SE = 2.8) for Macrocystis tran-
sects and 37.2 (SE = 2.2) for Nereocystis transects.
This difference resulted in a P value of 0.061 (two
sample £-test), which I considered significant. How-
ever, when all species of fish which demonstrated
significantly different densities between canopy
types were reevaluated, after excluding the six
Macrocystis transects with relief values more than
one standard deviation above the mean, no change
in results was observed for any species tested.
The total number of species encountered on the
transects was 26 in Macrocystis and 23 in Nereo-
cystis. The two kelp forests had 22 species in com-
mon. Five species were found in only one of the two
canopy types, although none of these were present
in more than 21% of the transects within the canopy
in which it was found. The H' values calculated were
1.76 for Macrocystis transects and 1.58 for the
Nereocystis transects. Although the value of diver-
sity indices has been questioned (Goodman 1975),
such indices are widely used in ecological literature.
Neither measure of diversity used in the present
study indicated differences in the diversity of fish
assemblages between the two kelp forest types
investigated.
DISCUSSION
Several measures of comparison were considered
in the analysis of these two kelp communities:
species composition, species diversity, and abun-
dance of fishes. The data presented here demon-
strate very little difference in either composition or
diversity of fish assemblages (Table 1), while esti-
mates of biomass were markedly higher in giant kelp
compared with bull kelp (Table 4).
The single most obvious difference between the
two kelp communities was in the abundance of the
blue rockfish: mean density of fish (no./lOO m2) was
Table 4.— Estimates of biomass of fish of Macrocystis and Nereocystis kelp forests. Species that were uncommon, (<20%
of transects), or small are not included.
Macrocystis
Nereocystis
Mean
Mean
Density
weight1
Biomass
Density
weight1
Biomass
Species
(#/100 m2)
(kg)
(kg/100 m2)
(#/100 m2)
(kg)
(kg/100 m2)
Midwater transects
Sebastes mystinus
15.0
0.44
6.6
3.92
0.50
1.96
Sebastes serranoides
0.45
0.63
0.28
0.11
0.72
0.08
Sebastes atrovirens
0.18
0.54
0.09
0.006
0.57
0.003
Sebastes melanops
0.02
0.44
0.009
0
0
0
Oxyjulis californica
12.4
0.024
0.30
11.9
0.024
0.29
Benthic transects
Sebastes chrysomelas
1.7
0.36
0.61
1.8
0.36
0.65
Sebastes carnatus
1.0
0.36
0.36
0.43
0.36
0.15
Sebastes atrovirens
0.70
0.38
0.27
0.11
0.38
0.04
Sebastes mystinus
0.15
0.44
0.07
0.15
0.50
0.07
Sebastes melanops
0.21
0.44
0.09
0.03
0.44
0.01
Sebastes miniatus
0.04
2.0
0.08
0.09
2.0
0.18
Hexagrammos decagrammus
0.34
0.5
0.17
0.40
0.5
0.2
Embiotoca lateralis
0.84
0.47
0.39
0.17
0.47
0.08
Embiotoca jacksoni
0.41
0.47
0.19
0.16
0.47
0.08
Scorpaenichthys marmoratus
0.11
0.7
0.08
0.11
0.7
0.08
Ophiodon elongatus
0.13
2.6
0.34
0.09
2.6
0.23
Rhachochilus vacca
0.13
0.47
0.06
0.01
0.47
0.005
Total
9.99 kg/100 m2
= 0.0999 kg/m2
4.11 kg/100 m2
= 0.0411 kg/m2
'Mean weights from collections at Piedras Blancas Field Station, U.S. Fish and Wildlife Service, or estimated from mean total lengths.
805
FISHERY BULLETIN: VOL. 84, NO. 4
15.0 in Macrocystis and 3.9 in Nereocystis. Blue
rockfish probably are the largest contributor to the
total biomass of kelp forest fish communities in Cen-
tral California. Miller and Geibel (1973) estimated
blue rockfish densities at 6.66 fish/100 m2 in 1969
and 8.35 in 1970 in Macrocystis beds at Hopkins
Marine Life Refuge, Monterey County, CA. They
suggested that this represents about 50% of the ac-
tual biomass because their survey method under-
represented midwater species. Considering this ad-
justment, my data for blue rockfish in Macrocystis
forests agree well with theirs. Near Pt. Piedras
Blancas, blue rockfish made up 33% and 18% of the
mean number of fish within the Macrocystis and
Nereocystis forests, respectively. Assuming an aver-
age weight of 440 g (Table 4), blue rockfish con-
tributed about 70% of the total biomass of the
Macrocystis fish assemblage and about 50% of
Nereocystis (species weighing a few ounces or less
were not included in this analysis). The importance
of juvenile blue rockfish as forage for large car-
nivorous kelp forest fishes (primarily Sebastes sp.)
has been well documented (Miller and Geibel 1973;
Burge and Schultz 1973; Hallacher and Roberts
1985). Tagging studies have suggested that the
home range of blue rockfish is relatively small (Miller
and Geibel 1973). The evidence given here illustrates
the important role that blue rockfish play in the kelp
forest communities of central California.
My estimate of the biomass of fish within each of
the two canopy types (Table 4) included only species
that were relatively common and of sufficient size
to contribute significantly to the total. For exam-
ple, although the estimated mean weight of Oxyjulis
californica was only 24 g, its abundance made its
total contribution rather large.
My data showed that in this study area off Cen-
tral California Macrocystis supported a larger stand-
ing crop of fish, primarily midwater species of the
genus Sebastes, than did forests of Nereocystis
(Table 4). The following explanations are offered for
the observed differences. These explanations are not
mutually exclusive; several or all of the proposed ex-
planations may have contributed to the observed
patterns.
1) The amount of algae consumed by blue rock-
fish fluctuates seasonally. Hallacher and Roberts
(1985) showed that blue rockfish may use algae as
a major source of energy during the non-upwelling
period (September through March), which partly
coincides with the period of minimum development
in Nereocystis forests. During this period blue rock-
fish may rely on Macrocystis directly as a food
source, or indirectly as a substrate from which in-
vertebrates are taken. The resulting increased
biomass of blue rockfish in Macrocystis may help
support larger numbers of other carnivorous fish.
Four of the seven species that were densest in
Macrocystis (Table 5) forests are known to rely
heavily on juvenile rockfish for food (Hallacher and
Roberts 1985). Although juvenile rockfish densities
were not statistically greater in the Macrocystis
forest (Table 2) because of large variations in den-
sities (occurring on transects in either very large or
very small schools), they were generally more avail-
able in Macrocystis forests. Subsequent field obser-
vations of juvenile rockfish in central California kelp
forests have indicated that kelp forest rockfish
recruitment may have been poor during the course
of this study.
Table 5. — Summary of species for which densities in the two kelp
types differed significantly.
Species
Canopy type which presented
significantly higher density
Midwater
Sebastes mystinus
Blue rockfish
Sebastes serranoides
Olive rockfish
Sebastes atrovirens
Kelp rockfish
Sebastes melanops
Black rockfish
Benthic
Sebastes carnatus
Gopher rockfish
Embiotoca lateralis
Striped seaperch
Oxylebius pictus
Painted greenling
Sebastes atrovirens
Kelp rockfish
Macrocystis
Macrocystis
Macrocystis
Observed on Macrocystis mid-
water transects only
Macrocystis
Macrocystis
Macrocystis
Macrocystis (considered primarily
as a midwater species)
2) The perennial nature of Macrocystis forests
compared with the annual nature of Nereocystis
forests may contribute to increased fish densities
in Macrocystis forests. Macrocystis forests provide
some structure throughout the year with new
growth providing both vertical and canopy structure
1 to 3 mo earlier than Nereocystis. This temporal
stability may afford necessary habitat structure
within the water column permiting relatively higher
densities of fish.
3) Differences in abiotic factors such as the
physical orientation of the reef systems to oceanic
swells and the resultant surge and scour effects may
play a role in determining habitat suitability for
some species of fish. The effects of sediment trans-
port and scouring, caused by water movement,
806
BODKIN: MACROCYSTIS AND NEREOCYSTIS KELP FORESTS
would be most evident at the sea floor and may in
fact have contributed to the observed differences
in densities in the bottom dwelling surf perch (Table
5). My data indicated that the major differences in
densities of fish were in midwater species, suggest-
ing that exposure to bottom disturbance per se was
not a primary influence on observed patterns.
4) The differing physical characteristics of the
Macrocystis and Nereocystis plants themselves may
play a role in determining their suitability as habitat
for kelp bed fishes. During periods of full develop-
ment, within this study area, Macrocystis typically
has widely spaced, thick bundles of stipes with large
fronds throughout the water column, leading to a
canopy that is frequently closed. Nereocystis, in con-
trast, has single, frondless stipes with large terminal
fronds that generally form a broken surface canopy
(Fig. 1). Due to the distinct physical structure of
these two plants, both within the water column and
at the canopy, the foliage biomass is usually con-
siderably greater within the Macrocystis forest. This
abundance of structure, combined with its persis-
tance over time, may enhance the carrying capacity
of giant kelp forests compared with those of bull kelp
(Leaman 1980).
A comparison of the standing crop estimates pre-
sented in this study is made with those from other
marine reef systems in Table 6. While values for
both Macrocystis and Nereocystis forests are below
those representing fringing coral reefs (Brock 1954;
Randall 1963), my estimates for Macrocystis forests
compare favorably with the upper values obtained
in Monterey, CA (Miller and Geibel 1973) and north-
east New Zealand (Russell 1977), while the Nereo-
cystis estimate corresponds to the estimates from
Southern California Macrocystis forests (Quast
1968; Larson and DeMartini 1984).
In conclusion, Macrocystis forests supported a
biomass of fish about 2.4 times greater than that
supported by Nereocystis forests (Table 4) where
perennial, water column foliage provided a more
persistant, structurally diverse habitat. Larger
numbers of midwater fish, primarily 5. mystinus,
found in the Macrocystis forest can account for this
difference.
ACKNOWLEDGMENTS
This work was supported by the U.S. Fish and
Wildlife Service, Denver Wildlife Research Center,
Marine Mammal Section. I thank R. Brownell, R.
Curnow, J. Estes, R. Jameson, C. Jones, M.
Layman, L. Rathbun, P. Vohs, and S. Wright for
their support. D. Hilger, D. Martin, F. Scott, M.
Shawver, and G. VanBlaricom contributed their
time as dive partners to this work. I would like to
thank the members of my graduate committee— A.
Roest (advisor), F. Clogston, R. Gambs, and R.
Nakamura— and staff— R. Bowker and L. Maksou-
dian, and the Biological Science Department,
California Polytechnic University, San Luis Obispo,
CA. Valuable comments on earlier drafts of this
manuscript were offered by P. Eschmeyer, R.
Table 6.— Comparison of biomass estimates of fish from marine communities (after
Russell 1977).
Location and
Standing crop
reference
Bottom type
(kg.m2)
Hawaii (Brock 1954)
Fringing coral reef: open sand,
broken rock, coral reef, reef
flat
0.001-0.0184
Virgin Islands
Fringing coral reef: boulders,
(Randall 1963)
coral
0.160
Southern California
Kelp bed: broken rocky bottom,
(Quast 1968)
dense algal cover
0.0351
Southern California
Cobble, low relief Macrocystis
(Larson and DeMartini 1984)
forest
Cobble, low relief kelp-
0.039-0.065
depauperate
0.024
Monterey Bay, CA
Kelp bed: broken rocky bottom
(Miller and Geibel (1973)
dense algal cover, rocky reef
0.001 ->0.1 12
N.E. New Zealand
Rocky reef: open low relief,
(Russell 1977)
sparse algal cover.
Rocky reef: high bottom relief,
<0.001
extensive algal cover
0.103
Central California
Rocky reef: high bottom relief;
(Present study)
Macrocystis canopy
0.0999
Nereocystis canopy
0.041 1
'Average estimate.
807
FISHERY BULLETIN: VOL. 84, NO. 4
Jameson, R. Nakamura, G. Rathbun, A. Roest, and
G. VanBlaricom and three exceptional anonymous
reviewers. A special thanks to D. Bodkin and G.
VanBlaricom for their support and encouragement.
LITERATURE CITED
Abbott, I. A., and G. J. Hollenberg.
1976. Marine algae of California. Stanford University Press,
Stanford, CA.
Brock, R. E.
1982. A critique of the visual census method for assessing
coral reef fish populations. Bull. Mar. Sci. 32:269-276.
Brock, V. E.
1954. A preliminary report on a method of estimating reef
fish populations. J. Wildl. Manage. 18:297-308.
BURGE, R. T., AND S. A. SCHULTZ.
1973. The marine environment in the vicinity of Diablo Cove
with special reference to abalones and bony fishes. Calif.
Dep. Fish Game, Mar. Res. Tech. Rep. 19, 433 p.
Cane, M. A.
1983. Oceanographic events during El Nino. Science 222:
1189-1195.
Caughley, G.
1977. Analysis of vertebrate populations. John Wiley and
Sons, Lond.
Dayton, P. K., V. Currie, T. Gerrodette, B. D. Keller, R.
Rosenthal, and D. Ven Tresca.
1984. Patch dynamics and stability of some California kelp
communities. Ecol. Monogr. 54:253-289.
Dayton, P. K., B. D. Keller, and D. A. Ven Tresca.
1980. Studies of a nearshore community inhabited by sea
otters. Final Report MMC-78/14. Mar. Mammal Comm.,
Wash., D.C., 91 p. (Available U.S. Dep. Commer., Natl. Tech.
Inf. Serv., as PB81-109860.)
Goodman, D.
1975. The theory of diversity-stability relationships in
ecology. Q. Rev. Biol. 50:237-266.
Hallacher, L. E., and D. Roberts.
1985. Differential utilization of space and food by the inshore
rockfishes (Scorpaenidae: Sebastes) of Carmel Bay, Califor-
nia. Environ. Biol. Fish. 12(2):91-110.
Larson, R. J.
1980. Competition, habitat selection, and the bathymetric
segregation of two rockfish (Sebastes) species. Ecol.
Monogr. 50:221-239.
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.
Leamon, B. M.
1980. The ecology of fishes in British Columbia kelp beds. I.
Barkley Sound Nereocystis beds. Fish. Dev. Rep. 22.
Ministry of Environment, British Columbia, 100 p.
Miller, D. J., and J. J. Geibel.
1973. Summary of blue rock fish and ling cod life histories;
a reef ecology study and a giant kelp, Macrocystis pyrifera,
experiments in Monterey Bay, California. Calif. Dep. Fish
Game, Fish Bull. 158, 137 p.
Pielou, E. C.
1966. Species-diversity and pattern-diversity in the study of
ecological succession. J. Theoret. Biol. 10:370-383.
Quast, J. C.
1968. Estimates of the population and standing crop of fishes.
In W. J. North and C. L. Hubbs (editors), Utilization of kelp
bed resources in southern California, p. 57-79. Calif. Dep.
Fish Game, Fish Bull. 139.
Randall, J. E.
1963. An analysis of the fish populations of artificial and
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1977. Population and standing crop estimates or rocky reef
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Res. 11:23-36.
808
LIFE HISTORY AND LARVAL DEVELOPMENT OF
THE GIANT KELPFISH, HETEROSTICHUS ROSTRATUS GIRARD, 1854
Carol A. Stepien1
ABSTRACT
Life history data from about 1,200 giant kelpfish, including age, length, and weight relationships, are
described and analyzed. Additionally, differences in habitats and behavior between larvae, juveniles, and
adults are reported. Female giant kelpfish were found to be larger than males at given ages past sexual
maturity. Age data indicate that females live longer and all individuals larger than 28 cm TL collected
in this study were females. Males guard the algal nests until hatching, about 2 weeks after spawning.
Giant kelpfish from nests collected in the field were reared in the laboratory, surviving for up to 9 months.
Feeding and development of laboratory-reared larvae were compared with field-collected specimens. In
situ, they school in the kelp canopy until 2 months old, gradually developing juvenile coloration and becom-
ing increasingly thigmotactic and solitary. Giant kelpfish reach sexual maturity at 1-1.5 years, at which
time they commence to defend territories in given plant habitats.
The cryptically colored giant kelpfish, Heterostichus
7,ostratus, is abundant in southern California kelp
forests and surrounding subtidal plant habitats.
Heterostichus is one of the largest members of the
clinid family, reaching a length of 41.2 cm and an
age of 5 yr (J. E. Fitch in Feder et al. 1974). Al-
though ranging from British Columbia, Canada, to
Cape San Lucas, Baja California, Mexico, it is most
commonly found from Point Conception to central
Baja in depths of 35 m (Roedel 1953). Giant kelpfish
occur in three different colormorphs— red, brown,
and green— which closely match the color of their
surrounding plant habitats (Hubbs 1952; Stepien
1985, 1986). They additionally exhibit four different
dark melanin patterns, which appear superimposed
on the basic color of the fish and, unlike color-
morphs, can change rapidly (Stepien 1985, 1986).
Giant kelpfish spawn year-round, but most fre-
quently during spring months (Limbaugh 1955;
Feder et al. 1974). The eggs are attached to algal
nests with entangling threads that extend from the
egg membranes (Holder 1907; Feder et al. 1974).
The males alone guard the nests from predators
until hatching, averaging 2 wk after spawning
(Coyer 1982). Giant kelpfish are relatively well-
developed at hatching and are planktonic for several
weeks. They school in the kelp canopy until they are
about 6 cm long, then develop juvenile coloration
department of Biological Sciences, University of Southern
California, Los Angeles, CA 9008S; present address: Marine
Biology Research Division A-002, Scripps Institution of Ocean-
ography, University of California at San Diego, La Jolla, CA 92093.
and become solitary, living close to nearshore algae
(Limbaugh 1955).
Although Heterostichus larvae are not uncommon
in the nearshore ichthyoplankton, their development
has not been previously described. Heterostichus egg
morphology was described by Barnhart (1932), and
the egg-laying process was described by Holder
(1907). Matarese et al. (1984) published two draw-
ings of kelpfish larvae. Although diet and some
aspects of general life history have been described
qualitatively by several investigators (Hubbs 1920,
1952; Roedell 1953; Limbaugh 1955; Quast 1968;
Hobson 1971; Feder et al. 1974; Hobson et al. 1981;
Coyer 1982) and one quantitative study was con-
ducted on feeding and distribution of juveniles and
adults in giant kelp (Coyer 1979), specific morpho-
metric data for larval, juvenile, and adult stages
have not previously been reported. This paper
presents life history data, including the following: 1)
Differences in larval, juvenile, and adult habitats and
behavior; 2) size, weight, and age relationships, in-
cluding differences between males and females; and
3) the sequence of larval development and meta-
morphosis.
MATERIALS AND METHODS
Collection and In Situ Observations
In situ observations were made during approx-
imately 280 scuba dives from 1978 to 1983, the
majority in the vicinity of the University of South-
ern California's Catalina Marine Science Center
Manuscript accepted March 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
809
FISHERY BULLETIN: VOL. 84, NO. 4
(CMSC) on Santa Catalina Island (Fig. 1). Most
observations and collections were made in protected
cove areas having well-developed kelpbeds of the
giant kelp, Macrocystis pyrifera, and associated
plant habitats, including surfgrass, Phyllospadix tor-
reyi, and red and brown algae. Approximately 1,200
giant kelpfish were observed during the course of
the study. The aging and sexing study material from
Catalina was also supplemented by 42 specimens col-
lected from subtidal sites off the southern Califor-
nia mainland, including Ventura, Lunada Bay on the
Palos Verdes Peninsula, Huntington Beach, and La
Jolla (Fig. 1).
Kelpfish were collected using a 0.5 x 0.8 m net,
mounted on a 1 m long handle and constructed of
0.25 cm mesh dyed either brown or red to match
the kelpfish algal habitats (it was found that white
netting alarmed the fish, making them difficult to
—i —
119°
— T"
118°
—l —
117°
t
N
, Ventura
34°
-33'
Los
•
Angeles
Santa Monica\
Bay \
*
Long Beach
LUoadaBBV ^
v. Huntington
^\4 Beach
^Q^U
Newport Bay y.
C$
v — J
Catalina Island.
kfOceanside
A COLLECTION SITES
La Jolla
.San
'Diego
u
20
_i_
40 MILES
" — i — i — i — i — i — r-
0 20 40 60 KILOMETERS
Figure 1.— Giant kelpfish collection sites (open triangles) off the southern California coast.
810
STEPIEN: LIFE HISTORY AND DEVELOPMENT OF KELPFISH
catch). Kelpfish were collected by sliding the net for-
ward and downward over the fish. Collection of kelp-
fish was facilitated by their habit of hiding in algae
when pursued rather than escaping by rapid swim-
ming. Those that were actively swimming (usually
through the kelp canopy) were less frequently cap-
tured. They were placed in a collecting bucket
having mesh sides, a snap-on lid, and a funnel entry-
way, preventing escapes when the lid was opened
for other fish. Care was taken to avoid putting the
larger kelpfish in the same bucket as the smaller
ones, because the smaller ones were occasionally
eaten by the larger ones.
Life History Data From Juveniles
and Adults
In the present study, 140 juveniles and adults of
representative sizes (ranging from 10 to 42 cm TL)
were measured live to the nearest 0.1 cm. Total
length (TL) was found to be more quickly measur-
able than standard length (SL). Both SL and TL
were measured, in order to allow comparisons with
other studies. Kelpfish were weighed to the nearest
0.1 g on a triple-beam balance while briefly con-
tained in plastic bags, in which they were quiescent
and unabraded. These data were graphed, and
regression and F-test analyses were performed
(Sokal and Rohlf 1981; Zimmerman and Kremer
1983).
The fish were sexed and aged. Females had clear
or pink, rounded ovaries and most individuals over
14 cm TL had clearly visible developing eggs. Male
gonads were cream-colored and had a characteristic
ventral groove. In cases when sex of juveniles was
questionable, the gonads were examined under a
dissection microscope.
Otoliths (sagitta) were removed and stored dry in
labeled glass. They were briefly submerged in water
and examined against a black background with a
dissecting microscope (25-50 x magnification) for
ring counting (Fig. 2). Ages were determined by
counting alternating white (opaque) and translucent
(hyaline) bands, each representing 6 mo of growth,
KELPFISH OTOLITH
B
NUCLEUS
1 YEAR OLD
2 YEARS OLD
3 YEARS OLD
4 YEARS OLD
O
I
.1
_L-
.2
_l
.7 CM.
Figure 2.— (A) Photograph of otolith (actual length = 6.5 mm) of a 4 yr-old female giant
kelpfish, 33 cm TL. (B) Drawing of otolith (sagitta) showing ring counts.
811
FISHERY BULLETIN: VOL. 84, NO. 4
using standard methods outlined by Fitch (1951),
Jensen (1965), and Collins and Spratt (1969). Each
pair of otoliths was read independently by me and
another reader, neither knowing the identity of the
fish. Our age estimates were in agreement in 80%
of the examinations. When differences in ring count
occurred, a joint reevaluation was made.
Total length versus age comparisons were
graphed, and regression analysis and F-tests were
performed on the log-log transformations. Mean
sizes of male and female kelpfish in age classes
where differences appeared to occur were tested for
significance using i-tests and 2-way ANOVA. Sep-
arate regression equations were also calculated for
males and females, and ANCOVA was performed
to determine whether the distributions were signifi-
cantly different (Sokal and Rohlf 1981).
Seasonal population structure was estimated from
collection data taken from February 1981 through
January 1983. Kelpfish were grouped in six size
classes. Distribution of kelpfish in size classes was
analyzed for significant seasonal variations using
contingency tables and G-tests (Sokal and Rohlf
1981).
Larval Rearing
Nine giant kelpfish nests were collected, four in
spring 1980 and five in spring 1982, off Santa Cata-
lina Island. Both parents of the eggs were collected
in three cases when spawning was observed. In six
cases, only the male parents, which were guarding
the nests, were collected. Eggs were also laid in the
laboratory on five separate occasions, but did not
hatch normally, apparently because of inadequate
dispersion in the nests.
Algal nests containing eggs were suspended from
a glass rod connected to an electric stirring device,
simulating wave motion in shallow subtidal habitats
(Fig. 3A). This method substantially decreased
bacterial and fungal attacks. Parents were not kept
with the eggs, as both males and females were
sometimes found to eat eggs in the laboratory. Nests
were placed in aerated 190 L plastic containers
cooled in 1 m deep aquaria of running seawater.
Filtered seawater in the containers was replaced
every few days. Several eggs were removed daily
for examination of development.
Newly hatched larvae were isolated in lightly
aerated 76 L brown plastic containers bathed in
large aquaria. Kelpfish larvae were fed laboratory-
raised Brachionus plicatilis (marine rotifers) within
24 h after hatching. Brachionus plicatilis were cul-
tured in high densities of the green flagellate,
Tetraselmis tetrahele, which was grown in a
nutrient-rich medium under constant light, follow-
ing methods developed for feeding northern anchovy
larvae (Theilacker and McMaster 1971). Brachionus
plicatilis, ranging from 0.01 x 0.02 mm to 0.07 x
0.20 mm in size, were maintained in the larval kelp-
fish containers at concentrations of 10-40/mL. At
age 1 wk, kelpfish larvae were changed from closed
to open containers of filtered and aerated running
seawater, having two 20 x 30 cm panels of 100 ^m
mesh.
After age 2 wk, kelpfish larvae were also fed wild
plankton, which primarily contained various devel-
opmental stages of the copepod Acartia sp. (92%
wet weight) and some barnacle nauplii and cyprid
larvae (7% wet weight). Wild plankton were col-
lected using a submersible pump attached to a float
off the laboratory pier. A light was suspended over
the pump and the system connected to an electrical
timer. Plankton were filtered through a 335 pm
mesh bag into a 190 L plastic container. The con-
tainer had a removable inner 100 pm mesh lining
and a spillover pipe, retaining only appropriate-sized
plankton between the two filter bags (Fig. 4). Best
copepod catches were obtained from dusk to 2 h
after sunset. Running filtered seawater and an
aerator were used to maintain temperature and
oxygen levels in the collecting container until the
fish larvae were fed the following morning. Den-
sities averaged 1-3/mL, which have been shown to
support high survival rates in laboratory rearing of
other fish larvae (Houde 1973; Hunter 1981).
When plankton catches were low, giant kelpfish
diet was supplemented with cultured Artemia salina
(brine shrimp) nauplii. Brachionus plicatilis were
discontinued after age 3 wk and plankton continued
until age 3 mo. After age 2 mo, diet was supple-
mented with frozen adult brine shrimp, Tetramin2
commercial flake food, and live mysids captured
from net tows in kelpbeds.
Ten larvae were removed every 2 d during the
first 2 wk of development for measurement and
description. After this period, 10 larvae were ex-
amined weekly until 2 mo had elapsed. All measure-
ments were made on fresh material. Drawings of
several stages of larval development were made
using a camera lucida and a dissecting microscope.
Gut contents of three specimens from each weekly
sample through age 4 wk were analyzed. While
viewing with a dissecting microscope, guts were
dissected away from the body and food particles
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service. NOAA.
812
STEPIEN: LIFE HISTORY AND DEVELOPMENT OF KELPFISH
Figure 3.— (A) Giant kelpfish nest in aquarium, attached to an electric stirrer, which simulated wave motion. (B) Photograph
of nest with eggs in brown algae, taken with 70 mm macrolens. (C) Photograph under compound scope of 24-h kelpfish egg show-
ing blastodisc, egg diameter = 1.4 mm. (D-F) Developing kelpfish eggs photographed under dissection microscope (diameters
= 1.4 mm). (D) 72 h after spawning. (E) 10 d after spawning. Note adhesive threads attaching egg to red alga. (F) 12 d after spawning.
813
FISHERY BULLETIN: VOL. 84, NO. 4
PLANKTON COLLECTOR DESIGN
LID WITH HOLE
INNER MESH BAG
OUTER MESH BAG
TIMER
LIGHT
FLOAT
^SUBMERSIBLE PUMP
Y£.s«
Figure 4.— "Automatic" plankton collector design for feeding giant kelpfish larvae. Plankton were attracted
to light on timer after dark. Submersible pump, suspended beneath the float, pumped plankton into large plastic
container on dock. Plankton ranging from 100 to 325 ^m were filtered between two mesh bags. Aeration and
running seawater kept the plankton alive.
teased out using either a single human hair or a
modified paint brush from which only a few long
strands protruded. Gut contents were viewed under
a compound microscope and identified, and average
lengths and widths of prey items were recorded.
At age 2 mo, the kelpfish larvae were moved to
containers having 0.3 cm mesh panels and contain-
ing artificial plant habitats (see Stepien 1985 and
1986). They were subsequently measured bimonth-
ly and their development described. Development
and feeding of laboratory-reared kelpfish larvae
were also compared with 20 field-collected in-
dividuals. Kelpfish larvae of various ages and sizes
were collected in hand nets while night-lighting from
a dock and while scuba diving in kelpbed canopies
using a 1 mm mesh handnet. Other kelpfish larvae
were examined from bongo net collections made in
Santa Monica Bay in 1982. Their development was
compared with similar-sized laboratory-reared lar-
vae. Gut contents of four early-stage larvae (esti-
mated 0-9 d old) were analyzed for food types and
sizes, in comparison with laboratory-reared kelp-
fish.
RESULTS
Spawning
Giant kelpfish nests were guarded by the male
parent, the eggs being interspersed and held by
adhesive threads in either red or brown algae (Fig.
3B). Seven of the nine nests collected were located
in isolated clumps of algae, and all were found be-
tween 6 and 12 m deep. Kelpfish nests were most
common in the red alga Gelidium nudifrons (6 of
9 nests collected) in areas where clumps of taller
brown algae covered patches of red algae. Three of
the nests were located in brown algae, two in Cys-
toseira neglecta, and one in Sargassum muticum.
The male parent hid in the overlying clump of
brown algae, emerging to chase away intruding
fishes. Male kelpfish were observed to defend their
nests against other kelpfish, sheephead, and rock
wrasse. Female kelpfish may spawn several times
a year since a female kept in the laboratory laid eggs
twice within 3 mo. Gonads of all females examined
after spawning were almost entirely spent. Since
814
STEPIEN: LIFE HISTORY AND DEVELOPMENT OF KELPFISH
all eggs in the nests examined were in similar stages
of development, it is likely that each nest contains
the eggs of a single female. After spawning (the
behavior sequence of which is described in Coyer
1982), the male kelpfish chases away the female
parent, as was observed in the laboratory on three
separate occasions. In one case, the male's repeated
pursuits resulted in the female jumping out of the
aquarium.
Eggs occurred in two different colors, red and
brown, which microscopic examination showed was
due to color of the yolk. All eggs in a given nest were
either red or brown and remained that color
throughout development. Nest and egg color did not
always match. Brown eggs were found in four nests
of red algae and two nests of brown algae, while red
eggs were found in two nests of red algae and one
nest of brown algae.
Fertilized eggs laid in the laboratory developed
poorly and few of them hatched, apparently due to
abnormal dispersal in the algal nests by the females.
In all three cases of laboratory spawnings, eggs
were laid in clumps rather than being well-spaced
throughout the algae, as observed in field-collected
nests. Freshly laid nests were collected in the field
on three occasions from pairs that had just com-
pleted spawning. Two of the three spawning females
were brown colormorphs and one was a red morph,
but all three showed the barred melanin pattern. All
nine field-collected male parents were brown color-
morphs exhibiting the characteristic male nuptial
striped melanin pattern (Coyer 1982; Stepien 1985,
1986).
Egg Development and Hatching
Eggs from freshly laid nests hatched in 12-17 d
at 18°C, the largest number hatching in 13 d. Eggs
averaged 1.4 mm in diameter and nests contained
an average of 700 eggs, ranging from 400 to 1,200
eggs. An estimated 800 of the 1,200 eggs hatched
from the most successful laboratory incubation.
Nests that were rotated vigorously and kept well-
aerated produced the most successful hatchings.
The sequence of egg development is summarized
in Table 1 and photographs of the developing eggs
are shown in Figure 3. Hatching occurred from day
14 through day 15. Hatching took about 20 min, the
larvae emerging head-first from the egg membrane.
Early Larval Development
(Prenotochord Flexion)
Giant kelpfish larvae can be distinguished from
other southern California clinid larvae by their large
numbers of myomeres, averaging 55-59. Newly
hatched larvae had large yolk sacs and well-
developed mouths, guts, melanophores, and fin folds
and averaged 6.2 mm TL (Fig. 5A). Larvae floated
upside-down, yolk up, for the first 24-36 h after
hatching. They swam with wriggling movements,
lasting about 30 s, interspersed with longer periods
of inactivity, lasting up to several minutes.
Yolk sacs were present 36-48 h after hatching.
Two- day-old larvae averaged 7.0 mm TL and swam
strongly upright, showing positive attraction to light
and concentrating near the white mesh areas of the
containers. After 4 d, the larvae were less positive-
ly photo tactic, concentrating towards the bottom of
the containers. Mean sizes and a summary of the
sequence of larval development are listed in Table
2. Illustrations of larvae are found in Figure 5.
Later Larval Development
(Postnotochord Flexion)
Flexion of the notochord had begun by 7-9 d and
an average size of 8.5 mm (ranging from 7.6 to 8.9
mm, N = 12). Field-collected giant kelpfish larvae
also showed the beginnings of notochord flexion at
a similar size (7.4-9.3 mm, N = 5). Size at notochord
flexion is smaller than that reported by Matarese
et al. (1984) for other clinid larvae.
Two-week-old giant kelpfish larvae began swim-
ming in organized schools, which also were observed
in situ in giant kelp canopies. Other researchers have
also noted this phenomenon (Feder et al. 1974),
which was not observed in giant kelpfish past the
age of 2 mo in both the laboratory and the field. By
3 wk, the schooling larvae became progressively
more difficult to catch with dip nets, exhibiting well-
Table 1.— Summary of kelpfish egg developmental stages.
Developmental features
well-developed blastodisc, beginnings of epiboly
head fold apparent, neural tube forming
embryo wrapped 180° around egg's circumfer-
ence; notochord, somites, eyes, and lenses
visible
embryo wrapped 240° around egg's circumfer-
ence, myomeres well-developed, lenses of eyes
pigmented, heart beating 95 times per minute
yolk shrunk to 1/2 size of egg; embryo curled 1.5
times around egg; mouth differentiated; gut,
liver, and inner ear developing
otoliths and pectoral and dorsal fin folds visible,
vigorous tail movements, heart beats 90 to 100
times per minute
hatching at 18°C, larva exits head-first, hatching
takes about 20 min
Time after
spawning
24 h
36 h
72 h
6d
10 d
12d
14 d
815
FISHERY BULLETIN: VOL. 84, NO. 4
816
STEPIEN: LIFE HISTORY AND DEVELOPMENT OF KELPFISH
Table 2.— Mean sizes (TL, mm) and developmental stages of laboratory-reared giant kelpfish
larvae 0-60 d.
Age1
(d)
Mean
length
Range
(TL, mm)
No.
Developmental features
0
6.2
6.0-6.5
10
2
7.0
6.7-7.5
10
4
7.7
7.0-8.0
5
7.9
7.4-8.4
10
7
8.3
7.5-9.0
5
9
8.8
7.9-9.4
10
11
9.7
7.9-10.7
10
13
10.3
8.2-11.2
5
15
10.9
9.5-11.7
10
17
11.4
10.0-12.3
10
19
11.5
10.1-12.5
5
21
11.7
10.6-13.6
10
23
12.0
11.4-14.3
10
25
12.2
10.3-16.8
10
30
16.8
13.0-19.0
10
39
23.8
18.0-28.0
5
46
25.6
22.0-27.0
10
53
25.7
18.0-35.0
10
60
30.6
25.0-37.0
10
'Age (d) after hatching.
well-developed mouth, gut, and fin folds; 12 postanal
serial melanophores
12-19 postanal melanophores, first feeding, yolk sac 1/3
original size
20 postanal melanophores, 2 melanophore spots on
liver, melanophores dorsal to anus, yolk sac disap-
peared
some ventral caudal fin rays visible, gill rakers formed,
operculum visible
notochord flexion begun in some
notochord flexion completed, swim bladder formed
caudal fin rays well-developed
schooling behavior is pronounced
fin rays in rear of dorsal and anal fin folds
scattered melanophores on top of head and lower jaw,
melanophores over gut
well-developed schooling and avoidance behavior
pectoral, dorsal, and anal fin rays formed
continuous line of stellate melanophores above the gut
pelvic fins beginning to develop, melanin pigmentation
in pelvic region
orange xanthophore pigmentation on top of the head,
over the gut and at the base of the caudal fin; teeth
visible
pelvic fins formed, 32 postanal ventral melanophores
larvae are pale gold in color
schooling no longer pronounced
most have settled onto algae
developed avoidance patterns and fright responses.
By 5 wk, schooling was no longer as pronounced and
the larvae were observed to stalk their copepod prey
very efficiently.
Larval Feeding
Unless giant kelpfish larvae were given food with-
in the first 48 h, a point of no-return was reached,
after which they starved to death even if given food.
Best results were obtained if larvae were fed within
24 h of hatching. Brachionus (rotifers) and Tetra-
selmis (algae) were found in the guts of 2-d-old lar-
vae in the laboratory. Three-day-old larvae, even
those still having yolk sacs, contained an average
of 5.6 Brachionus and 2.9 Tetraselmis (Table 3).
High mortality (nearly 60% of those hatched) oc-
curred after hatching and through day 5. Dead lar-
vae examined had apparently never eaten, despite
relatively high levels of appropriately sized food
items.
Gut contents of field-collected kelpfish larvae
(estimated to range from 0 to 9 d old) showed that
they fed on a wide variety of food items, including
single-celled algae, rotifers, mollusk larvae, and bar-
nacle and copepod larvae (Table 4). Similar sizes and
quantities of food items were consumed by both the
laboratory-reared and field-collected larvae (Tables
3,4).
Significantly larger food items were consumed by
2-wk-old laboratory- reared larvae, the largest
widths being 52% of the mouth size (Fig. 6). Larger
copepods were eaten more frequently than rotifers,
although both food items were present in guts (Table
3). High mortality (ranging from 20 to 40%) also
occurred at about 2.5 wk of age in both the 1980
and 1982 rearing experiments. At this age, gut ex-
aminations indicated that the larvae were switch-
ing from the smaller prey (rotifers and algae) to the
larger copepods. Older larvae progressively con-
sumed larger copepods whose size reached 70% of
the mouth width by week 3 (Fig. 6, Table 3).
Figure 5.— Drawings of laboratory-reared giant kelpfish larvae,
made with camera lucida and dissection microscope. (A) Day 0
(after hatching), 6.1 mm TL. (B) Day 4 after hatching, 7.0 mm
TL. (C) Day 7 after hatching, 8.4 mm TL. (D) 2 wk, 10.9 mm
TL. (E) 3 wk, 11.6 mm TL. (F) 5 wk, 22.2 mm TL.
Settlement and Metamorphosis
After 8 wk and at a mean length of 30.6 mm, giant
kelpfish larvae had well-developed, pale gold-brown
pigmentation. They became increasingly thigmotac-
817
FISHERY BULLETIN: VOL. 84, NO. 4
Table 3.— Gut contents of laboratory-reared giant kelpfish larvae, 3 d to 5 wk, indicating mean numbers
and sizes of prey items. N = 18 (N = 3/sample). Laboratory diets 0-3 wk consisted of Tetraselmis and
Brachionus. Acartia copepods were added to the diet at 2 wk. Sizes of kelpfish (TL, mm) and mean sizes
of prey items (width x length) given.
larvae
Size
(mm)
6.8
7.1
7.4
Prey items
Kelpfish
Tetraselmis algae
Brachionus rotifers
Acartia copepods
Age
Mean
No.
2.9
Size
(mm)
Mean
No.
Size
(mm)
Mean
No.
Size
(mm)
3d
0.039 x 0.120
5.6
0.10 x 0.149
—
1 wk
8.0
8.2
8.2
3.3
0.050 x 0.120
14.7
0.103 x 0.157
2 wk
9.4
9.7
10.8
10.0
0.078 x 0.130
10.2
0.160 x 0.220
1.2
0.100 x 0.390
3 wk
10.7
11.5
13.6
"
6.8
0.130 x 0.195
2.4
0.221 x 0.520
4 wk
11.9
13.3
16.4
3.3
0.221 x 0.520
5 wk
19.7
22.0
23.0
7.9
0.220 x 0.850
Table 4.— Gut contents of field-collected giant kelpfish larvae 6.24-8.2 mm TL. N = 4. Mean TL
of kelpfish = 6.93 mm (range 6.24-8.82 mm). Mean mouth width = 0.42 mm (0.40-0.44 mm).
Mean no./
Mean width
Mean length
Food iterr
I
larva
and range (mm)
and range (mm)
Diatoms
3.00
0.03 (0.01-0.07)
0.06 (0.04-0.08)
Dinoflagellates
2.00
0.03 (0.01-0.07)
0.04 (0.02-0.20)
Tintinnid protozoans
0.75
0.04 (0.03-0.07)
0.13 (0.10-0.16)
Rotifers
0.75
0.08 (0.03-0.13)
0.19 (0.08-0.35)
Barnacle nauplii and
cyprids
0.75
0.10 (0.07-0.13)
0.16 (0.12-0.23)
Copepod nauplii and
copepodites
3.50
0.12 (0.07-0.21)
0.40 (0.14-0.46)
Mollusk larvae
1.00
0.11 (0.09-0.12)
0.25 (0.22-0.29)
Nemertean worms
0.25
0.10
0.34
Siphonophores
0.25
0.29
0.30
tic during the next few weeks, darting amongst the
artificial plants placed in their containers. Similar-
ly, kelpfish individuals observed in situ had "settled"
onto juvenile habitats by 30-50 mm TL. Juvenile
habitats included the fronds of giant kelp; the brown
alga, Sargassum muticum; and green surfgrass.
Juveniles were usually in loose aggregations of three
to seven similar-sized individuals until reaching a
size of 7-9 cm TL.
At 5-7 cm (between 2 and 4 mo), laboratory-reared
and field-collected giant kelpfish lost their trans-
parent light gold-colored appearance, developing
either green, gold, or brown pigmentation depend-
ing on their juvenile habitat, whether surfgrass,
kelp, or Sargassum. The majority of juveniles found
in surfgrass were green with striped or mottled
melanin patterns and had silvery horizontal patches.
Those in kelp were usually plain or mottled gold-
brown with gold bellies while those in Sargassum
developed brown pigmentation and barred or mot-
tled melanin patterns (see Stepien 1985 and 1986
for detailed descriptions of color patterns).
Morphometries of Larvae,
Juveniles, and Adults
The SL and TL of giant kelpfish larvae were
linearly related (Fig. 7). Early growth (to 40 d) of
laboratory-reared larvae was logarithmic (Fig. 8A)
while length and age were linearly related between
1 and 9 mo of age (Fig. 8B). Otoliths of laboratory-
reared kelpfish showed abnormal ring patterns,
818
STEPIEN: LIFE HISTORY AND DEVELOPMENT OF KELPFISH
MEAN MOUTH WIDTH AND MAXIMUM PREY WIDTH
10 r
E
E
5
N* 15
N (ea. sample) ■ 3
0 12 3 4
Age (Weeks)
Figure 6.— Mean mouth width and maximum prey width
consumed by laboratory-reared giant kelpfish larvae 0-4
wk old. N = 15 (N each sample = 3).
having several "checks" (false rings). Maximum age
reached by laboratory-reared kelpfish in these ex-
periments was 9 mo, at which time they succumbed
to a bacterial infection.
Weight versus length of juvenile and adult kelp-
fish was exponentially related (Fig. 9), and SL and
TL were directly linearly related (Fig. 10). Length
versus age determinations also followed an exponen-
tial curve (Fig. 11). Sexual maturity occurred at a
mean size of 18.6 cm TL and an age of 1-1.5 yr.
Regressions of sizes of adult males and adult
females on age class were found to be significantly
different using ANCOVA (see Fig. 11 legend). When
sizes at given ages were compared using £-tests,
females were found to be significantly larger than
males at given ages past 2 yr (Fig. 12). The largest
males sampled in this study were not older than 3
yr or larger than 28 cm TL. In contrast, large
females, reaching ages of 4.5 yr and sizes of 42 cm
(TL) were collected. Larger individuals collected
throughout the 5-yr sampling regime were consis-
tently females.
Population Structure
Seasonal size class structure of the giant kelpfish
population was consistent over 2 yr of regular sam-
STANDARD LENGTH (SL) VS. TOTAL LENGTH (TL)
OF KELPFISH LARVAE
30r-
10
14
18 22
Total Length (mm)
26
34
Figure 7.— SL (mm) versus TL (mm) of laboratory-reared giant kelpfish larvae 0-30 d old. * =
one fish. N = 108. Regression equation: SL = 0.598 + 0.819 (TL). F = 11,588.62, P < 0.00001.
819
FISHERY BULLETIN: VOL. 84, NO. 4
LOG LARVAL LENGTH VS. AGE (0 - 40 DAYS)
E
c
TO
o
2 4 6 7 9 T1 13 15 17 21 23 25
Age (days)
30
B
LENGTH VS AGE (0 - 9 MONTHS)
3 4 5
Age (months)
Figure 8.— (A) Log length (TL, mm) versus age (0-40 d) of laboratory-reared giant kelpfish
larvae. * = one fish. N = 130. Regression equation: Log TL = 0.814 + 0.013 (days).
F = 1,211.9, P < 0.0001. (B) Growth of laboratory-reared giant kelpfish (0-9 mo), length
(cm) versus age (months). * = one fish. N = 100. Regression equation: TL = 0.379 +
1.482 (months). F = 2,230.8, P < 0.0001.
pling (Fig. 13). Contingency tests of independence
showed that numbers of individuals in various size
classes differed significantly with season in 1981-82
and 1982-83. Juveniles appeared in significant num-
bers during the spring and summer months. These
data agreed with observations on spawning and
appearance of larvae in the water column, indicating
that most Catalina Island kelpfish in these years
spawned from January through May. During spring
and summer, a large portion of the population was
estimated to be 1 and 2 yr old, composed of in-
dividuals of reproductive age. During the fall
820
STEPIEN: LIFE HISTORY AND DEVELOPMENT OF KELPFISH
LOG WEIGHT VS. LOG LENGTH OF JUVENILES AND ADULTS
2.6
1.0 1.1 1.2 1.3
Log Total Length (cm)
1.4
1.5
1.6
Figure 9.— Log weight (g) versus log TL (cm) of juvenile and adult giant kelpfish. * = one
fish. N = 140. Regression equation: Log weight = -2.508 + 3.243 flog TL). F = 3,622.7, P
< 0.0001.
45 r-
STANDARD LENGTH (SL) VS. TOTAL LENGTH (TL)
OF JUVENILES AND ADULTS
Total Length (cm)
Figure 10.— SL (cm) versus TL (cm) of juvenile and adult giant kelpfish. * = one fish. A = 11 fish.
N = 140. Regression equation: SL = -0.580 + 0.906 (TL). F = 15,993.0, P < 0.0001.
821
FISHERY BULLETIN: VOL. 84, NO. 4
LOG LENGTH VS. LOG AGE
.7 -.6
.5 -.4 -.3 .2 -.1 0 .1 .2 .3 .4
LOG AGE CYEARS)
8 .9 1.0
Figure 11.— Log TL (cm) versus log age class (years) of juvenile and adult giant kelpfish
(males and females). * = one fish. N = 137. Regression equation: Log TL = 1.234 +
G.528 (log age). F = 1,589.28, P < 0.0001. Regression equation for females only (N =
77): Log TL = 1.234 + 0.561 Gog age); F = 1,460.7, P < 0.0001. Regression equation
for males only (N = 60): Log TL = 1.235 + 0.453 (log age); F = 535.0, P < 0.001. ANCOVA
regression analysis of log TL for males and females (two different groups versus log age
class (years): F = 5.82 (P < 0.05).
MEAN LENGTH VS. AGE OF FEMALES AND MALES
Figure 12.— Mean TL (cm) versus age class (years) of
female and male giant kelpfish. Significant differences
between male and female mean sizes indicated.
* = Significant difference in t-test results (0.05 level).
Standard error bars shown. N = 137. Two-way ANOVA
with replication for mean lengths of male and female
kelpfish at three ages (2.0, 2.5, and 3.0 yr) showed signifi-
cant differences between the sexes (F = 38.52, P < 0.001)
and the age classes (F = 78.01, P < 0.001), but no inter-
action (sex x ages; F = 3.37).
1.0
1.5 2.0 2.5
Age (.5 years)
3.5
822
STEPIEN: LIFE HISTORY AND DEVELOPMENT OF KELPFISH
SIZE FREQUENCIES OF KELPFISH
50
40
30 -
>20
o
a» 10
3
a>
£ 0
0>
re
§ 50
S. 40
30 H
20
10
Feb- Apr 81
N=63
May-Jul 81
N =111
Aug -Oct 81
N = 128
Nov 81 -Jan 82
N = 61
■F3*-
5 15 25 35 5 15 25 35 5 15 25 35 5 15 25 35
Feb- Apr 82
N = 74
May-Jul 82
N = 153
AugOct82 Nov82-Jan83
N--130 N--24
15 25 35
5 15 25 35 5 15 25 35
Total Length (cm)
15 25 35
Figure 13.— Percentage frequencies of giant kelpfish size classes collected seasonally from February 1981
to January 1983. N = 744. Contingency table R x C G tests of independence showed significant seasonal
variations in frequencies of kelpfish size classes in 1981-82 (N = 363; *2 = 167.73, 15 df, P < 0.001) and
1982-83 (N = 381; x2 = 86.07, 15 df; P < 0.001). (Sokal and Rohlf 1981.)
months, the most abundant size classes were esti-
mated as 0.5 and 1.5 yr of age. These size frequen-
cies also indicate that a relatively low percentage
of the population is composed of individuals 3 yr and
older.
DISCUSSION
Reproduction and Development
Unlike Heterostichus, whose nests contain eggs
in similar stages of development, those of the fringe-
head Neoclinus bryope (family Clinidae; subfamily
Chaenopsidae) contain various developmental
stages, apparently from several spawnings (Shiogaki
and Dotsu 1972). Heterostichus eggs have a single
large oil globule (see Barnhart 1932 and Figure 3C),
while other described clinid eggs have several (Spar-
ta 1948; Shiogaki and Dotsu 1972; Matarese et al.
1984). Unfertilized eggs of Gibbonsia elegans con-
tain a mass of 6-16 small oil globules (Stepien3). Like
Heterostichus (see Figure 3D), Clinus argentatus
eggs develop large black melanophores over the sur-
face (Sparta 1948).
Early larval development in other clinids resem-
bles that of Heterostichus, although few species have
been studied and none have been reared past the
yolk-sac stage. Other clinids are reported to hatch
at similar sizes and at comparable development
(Sparta 1948; Shiogaki and Dotsu 1972; Matarese
et al. 1984). As in Heterostichus, the yolk-sac stage
persists for 2-3 d (Shiogaki and Dotsu 1972), caudal
fin rays develop first (Matarese et al. 1984), and dor-
sal and anal fin rays form posteriorly to anteriorly
(Risso 1948; Shiogaki and Dotsu 1972; Matarese et
al. 1984). Flexion of the notochord appears to occur
at a smaller size in Heterostichus (mean 8.5 mm TL)
than in some other clinids (by 11.1 mm TL in Neo-
clinus and 11.52 mm TL in Clinus argentatus) (Spar-
ta 1948; Shiogaki and Dotsu 1972).
3Stepien, C. A. 1986b. Life history of the spotted kelpfish, Gib-
bonsia elegans Cooper. Unpubl. manuscr. Marine Biology
Research Division A-002, Scripps Institution of Oceanography,
University of California at San Diego, La Jolla, CA 92093.
823
FISHERY BULLETIN: VOL. 84, NO. 4
Swimming behavior of newly hatched kelpfish lar-
vae, characterized by short periods of swimming
interspersed with longer periods of inactivity, is
common in many small marine yolk-sac larvae
(Hunter 1972; Ellertsen et al. 1980; Weihs 1980).
Like kelpfish, some other newly hatched larvae in-
cluding cod, Gadus morhua, (Ellertsen et al. 1980)
and white seabass, Atractoscion (Cynoscion) nobilis,
(Orhun4) swim upside-down for the first 24 h after
hatching. This behavior is due to positive buoyancy
of the yolk (Hunter5). Kelpfish larvae, in situ as well
as in the laboratory, schooled between 2 wk and 2
mo of age. Larval schooling is common in species
of nearshore fishes which also school as adults
(Smith 1981; Hunter 1981) and may serve to in-
crease the probability of locating patches of food
and/or may help them avoid predation. No reference
to larval schooling in fishes that do not school as
adults was found in the literature.
Larval Feeding
A point of no-return at which starvation occurs
even if larvae are fed appears to occur earlier in
giant kelpfish (after 36 h) than in fish larvae hatch-
ing from pelagic eggs (Hunter 1981) and is probably
due to their greater degree of development at hatch-
ing (i.e., smaller yolks and well-developed mouths
and digestive tracts). Only a small number of species
are sufficiently developed to consume exogenous
food shortly after hatching (Balon 1984a, b). Early
feeding during the yolk-sac stage may be critical for
the larvae to develop a "search" image and capture
skills (Hunter 1981).
In this study, high mortality following the yolk-
sac stage was apparently due to starvation, despite
relatively high levels of appropriate-sized food items.
In many marine fishes, relatively low feeding suc-
cess is apparently common in field-collected, as well
as laboratory-reared, larvae (Hunter 1981). During
the first week, field-collected, as well as the labora-
tory-reared, larvae consume a wide variety of food
items, primarily smaller ones such as unicellular
algae. Like Heterostichus, most species of larval
fishes have been found to eat many more small prey
items than larger ones (Hunter and Kimbrell 1980;
Hunter 1981).
"Orhun, R. M. 1986. Culture and growth of larval and early
juvenile white seabass, Atractoscion (Cynoscion) nobilis. M.S.
Thesis in preparation, Center for Marine Studies, Department of
Biology, San Diego State University, San Diego, CA 92182.
6 John Hunter, Southwest Fisheries Center La Jolla Laboratory,
National Marine Fisheries Service, NOAA, 8604 La Jolla Shores
Drive, La Jolla, CA 92038, pers. commun. January 1986.
High mortality also occurred in the laboratory at
about 2.5 wk, when larvae were apparently switch-
ing from smaller to larger prey. This may be a
critical period when the larvae have to learn to cap-
ture larger, faster swimming crustaceans as the
primary dietary component in order to obtain suffi-
cient caloric intake. Studies on other fish larvae have
demonstrated the necessity of increasing prey size
with growth (Hunter 1977; Hunter and Kimbrell
1980).
Juvenile and Adult Life History
Ages of juveniles and adults calculated in the pres-
ent study agree with estimates for giant kelpfish
determined by J. E. Fitch (in Feder et al. 1974) and
by R. Collins6. Ages by Coyer (1982), based on 42
kelpfish samples, do not agree with those in the pres-
ent study. Coyer appeared to have overestimated
the oldest kelpfish by 3 yr. This may have been due
to the prevalence of "checks" or partially completed
false rings on the otoliths which are commonly
formed during spawning (Collins and Spratt 1969)
and were frequently observed in the present study.
Estimated size at sexual maturity (mean 18.6 cm
TL) agrees with that reported by Coyer (1982).
Past the age of sexual maturity, female giant kelp-
fish are significantly larger than males and also live
several years longer. Size discrepancy between adult
males and females may have evolved from the
females' behavior of venturing away from their ter-
ritories during the spring spawning season into
those occupied by males (Stepien 1985, 1986). They
are often readily visible at this time while away from
plants of matching colors. Large size may help
females to avoid predation or, alternatively, may be
the result of selection for increased fecundity.
ACKNOWLEDGMENTS
Grants and funds supporting this research
included Sigma Xi, the Lerner Fund for Marine Re-
search, the Theodore Roosevelt Memorial Scholar-
ship Fund of the American Museum of Natural
History, the University of Southern California
Department of Biological Sciences and Graduate
School, and a Sea Grant Traineeship. Laboratory
facilities were provided by the Catalina Marine
Science Center, U.S.C.'s Fish Harbor Research
Laboratory, and Southern California Edison (Redon-
do Beach).
6Robson Collins, California State Department of Fish and Game,
Long Beach, CA 90813, pers. commun. March 1982.
824
STEPIEN: LIFE HISTORY AND DEVELOPMENT OF KELPFISH
I thank the following people for giving technical
assistance and information: Robson Collins, John
Hunter, Kenneth Rich, C. Robert Bostick, Charles
Winkler, Peter McGroddy, Steve Edwards, Eric
Lynn, Robert Lavenberg, Gerald McGowen, Gary
Brewer, and Laura Alderson. Steven Naffziger,
Donald Wilkie, Robert Moore, Neale Jones, Mark
Carr, Brandon Kulik, Richard Wright, John Sudick,
Neale Jones, and Larry Allen assisted in collecting
kelpfish. Robert Provin helped draw the figures and
Stanley Azen provided statistical advice. This manu-
script benefited substantially from critical reviews
by Basil Nafpaktitis, Richard Brusca, Gerald Bakus,
Gerald McGowen, and Bernard Abbott.
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Balon, E. K.
1984a. Reflections on some decisive events in early life of
fishes. Trans. Am. Fish. Soc. 113:178-185.
1984b. Patterns in the evolution of reproductive styles in
fishes. In G. W. Potts and R. J. Wooton (editors), Fish
reproduction: strategies and tactics, p. 35-53. Acad. Press,
Lond.
Barnhart, P. S.
1932. Notes on the habits, eggs, and young of some fishes
of southern California. Bull. Scripps Inst. Oceanogr., Univ.
Calif. 3:87-99.
Collins, R. A., and J. D. Spratt.
1969. Age determination of northern anchovies, Engraulis
mordax, from otoliths. Calif. Fish Bull. 147:39-55.
Coyer, J. A.
1979. The invertebrate assemblage associated with Macro-
cystis pyrifera and its utilization as a food resource by kelp-
forest fishes. Unpubl. Ph.D. Thesis, Univ. Southern Califor-
nia, Los Angeles, 314 p.
1982. Observations on the reproductive behavior of the giant
kelpfish, Heterostichus rostratus (Pisces: Clinidae). Copeia.
1982:344-350.
Ellertsen, B., P. Solemdal, T. Stromme, S. Tilseth, T.
Westgard, E. Moksness, and V. Oiestad.
1980. Some biological aspects of cod larvae (Gadus morhua
L.). Fiskeridir. Skr. Ser. Havunders. 17:29-47.
Feder, H. M., C. H. Turner, and C. Limbaugh.
1974. Observations on fishes associated with kelp beds in
southern California. Calif. Fish Bull. 160:1-144.
FlTCH, J. E.
1951. Age composition of the southern California catch of
Pacific mackerel 1939-40 through 1950-51. Calif. Fish Bull.
83:1-75.
Hobson, E. S.
1971. Cleaning symbiosis among California inshore fishes.
Fish. Bull., U.S. 69:491-523.
Hobson, E. S., W. N. McFarlane, and J. R. Chess.
1981. Crepuscular and nocturnal activities of Californian
nearshore fishes, with consideration of their scotopic visual
pigments and the photic environment. Fish. Bull., U.S.
79:1-30.
Holder, C. F.
1907. The nest of the kelpfish. Am. Nat. 41:587-588.
Houde, E. D.
1972. Some recent advances and unsolved problems in the
culture of marine fish larvae. Proc. World Maricult. Soc.
3:83-112.
Hubbs, C.
1952. A contribution to the classification of the Blennioid
fishes of the family Clinidae, with a partial revision of the
eastern Pacific forms. Stanford Ichthyol. Bull. 4:41-165.
Hubbs, C. L.
1920. Protective coloration and habits in the kelpfish, Hetero-
stichus rostratus. Copeia 1920:19-20.
Hunter, J. R.
1972. Swimming and feeding behavior of larval anchovy
Engraulis mordax. Fish. Bull., U.S. 70:821-838.
1977. Behavior and survival of northern anchovy Engraulis
mordax larvae. Calif. Coop. Oceanic Fish. Invest. Rep. 19:
138-146.
1981. Feeding ecology and predation of marine fish larvae.
In R. Lasker (editor), Marine fish larvae: morphology,
ecology, and relation to fisheries, p. 33-77. Wash. Sea Grant
Program, Seattle.
Hunter, J. R., and C. A. Kimbrell.
1980. E arly life history of Pacific mackerel , Scomber japoni-
cus. Fish. Bull., U.S. 78:89-101.
Jensen, A. C.
1965. A standard terminology and notation of otolith readers.
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Limbaugh, C.
1955. Fish life in the kelp beds and the effects of kelp har-
vesting. Inst. Mar. Res. Ref. 55-9, 158 p.
Matarese, A. C, W. Watson, and E. G. Stevens.
1984. Blennioidea: Development and relationships. In H. G.
Moser et al. (editors), Ontogeny and systematics of fishes,
p. 565-577. Am. Soc. Ichthyol. Herpetol. Spec. Pub. 1.
Quast, J. C.
1968. Observations on 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. Bull. Calif.
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Roedel, P. M.
1953. Common ocean fishes of the California coast. Calif.
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1972. The life history of the blenniid fish, Neoclinus bryope.
[In Jpn., Engl, abstr.] Bull. Fac. Fish. Nagasaki Univ. 34,
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Smith, P. E.
1981. Fisheries on coastal pelagic schooling fish. In R.
Lasker (editor), Marine fish larvae: morphology, ecology, and
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1981. Biometry: The principle and practice of statistics in
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1948. Uova ovariche, uova fecondate tenute in colture larva
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1986. Regulation of the colormorphic patterns in the giant Weihs, D.
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826
A SIMPLE METHOD FOR ESTIMATING THE FOOD CONSUMPTION
OF FISH POPULATIONS FROM GROWTH DATA AND
FOOD CONVERSION EXPERIMENTS1
Daniel Pauly2
ABSTRACT
Experimental data on the gross food conversion efficiency of fishes (Kl = growth increment/food in-
gested) are usually reduced to a model of the form Kx = aWb ; it is shown that the model K-, = 1 -
(WIWao)1' has a number of advantages over the traditional model.
The new model can be used to compute the food consumption per unit biomass of an age-structured
fish population, by relying on the first derivative of the von Bertalanffy growth formula (VBGF) to ex-
press growth increments, and the identity of W^, in the VBGF and in the model expressing Kx as a func-
tion of weight.
Computed examples, using published growth and mortality parameters, and the results of food con-
version experiments were used to obtain consumption estimates in a carnivorous grouper (Epinephelus
guttatus) and an herbivorous angelfish (Holacanthus bermudensis). Results were shown to be most sen-
sitive to the parameter /J. Various applications of this simple model are discussed, particularly as a method
to estimate key inputs in J. J. Polovina's ECOPATH model.
A multiple-regression extension of the basic model is presented which accounts for the impact of
factors other than body weight on values of Kl and /?. This method is illustrated with an analysis of data
on dab (Limanda limanda).
Estimating the quantity of food eaten during a cer-
tain period by a fish population from field data is
usually a difficult task and various sophisticated
methods developed for this purpose have data re-
quirements which can make their routine applica-
tion impossible (Beverton and Holt 1957; Ursin
1967; Daan 1973, 1983; Andersen 1982; Armstrong
et al. 1983; Rice et al. 1983; Stewart et al. 1983;
Pennington 1984; Majkowski and Hearns 1984).
Polovina (1984) recently presented a technique
for construction of ecosystem models which is
structured around a well-documented computer
program called ECOPATH (Polovina and Ow3). In
situations where classical fishery data are sparse this
technique has the potential of becoming a standard
method for consolidating and examining the data
available on aquatic ecosystems. ECOPATH esti-
mates equilibrium biomass (B), annual production
'Based on Chapter 3 of a "Habilitationschrift" presented in
December 1984 to the Dean of the Mathematics and Science Facul-
ty, Kiel University (Federal Republic of Germany) and titled "Zur
Biologie tropischer Nutztiere: eine Bestandsaufnahme von
Konzepten und Methoden." ICLARM Contribution No. 281.
international Center for Living Aquatic Resources Manage-
ment, MCC P.O. Box 1501, Makati, Metro Manila, Philippines.
3Polovina, J. J., and M. D. Ow. 1983. ECOPATH: a user's
manual and program listings. Southwest Fish. Cent. Admin. Rep.
H 82-83. Southwest Fisheries Center Honolulu Laboratory, Na-
tional Marine Fisheries Service, NOAA, 2570 Dole Street, Hono-
lulu, HI 96822-2396.
(P), and annual consumption (Q) for each group in
the model. ECOPATH requires a number of data
inputs for each group treated in the model and usual-
ly the most difficult to obtain is the average food
consumption per unit biomass (Q/B) of each group.
The present study derives a method to estimate Q/B
through a combination of experimental and field
data that are easily obtained. In the process, a model
is derived which will allow for more information to
be extracted from feeding experiments than has
hitherto been the case.
MODEL FOR REDUCING
EXPERIMENTAL DATA ON
THE CONVERSION EFFICIENCY
OF FISHES
Usually laboratory or pond feeding experiments
lead to estimates of Kx, the gross conversion ef-
ficiency, which are obtained, for short intervals,
from
Kx = growth increment/food ingested (1)
(Ivlev 1939, 1966).
Usually, Kx declines with body size (other factors
affecting Kx are discussed below) and it has become
Manuscript accepted April 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
827
FISHERY BULLETIN: VOL. 84, NO. 4
a standard procedure to plot empirical values of Kx
obtained against the corresponding body weights,
i.e., the mean weights (W) corresponding to each
growth increment, or
logio Ki = log10 a + b log10 W
which leads to the model
Kx = aWb.
(2)
(3)
(See Sprugel 1983 for a method to correct the bias
due to log transformation in this and the other
models below.) A discussion of this model may be
found in Jones (1976) (see Figure la for an example).
This model has three liabilities, the first of which
is the most serious:
1) The parameters "a" and "6" have no biological
meaning, i.e., cannot be predicted from one's
knowledge of the biology of a given fish. Converse-
0.4
o
o
0.5
0.6
0.7
0.8
0.9
0.25
*r
0.20
0.15
o
1
0.10
0.05
0.00
Traditional model
(r2 = 0.821)
New model
(r2 = 0.888)
,oqiow°>
2 3
Body weight (g,log|0units)
ooi
o
.s> i.o
<u
c
o
w
a)
>
c
o
o
0.6
0.4
0.2
Traditional
model
Upper limit
for new model
(K=l,when W=0)
— Traditional model
— New model
Lower limit
for new model Traditional
(KpO when W» Woo) model
\
50
100
_i ty\/\ s---ii- ,
150 1,500
00
Body weight (g)
Figure 1.— Relationship of gross food conversion efficiency (K{) and body weight (W) in Channa striata, a)
Plot of \ogwK1 on log10W^, as needed to estimate parameters "a" and "b" of traditional model for prediction
of Kx from body weight, b) Plot of -log10(l -Kx) on log10W, as needed to estimate parameters Wm and p of
new model, c) Comparison of the two models. Note that both fit the data well over the range for which data
points are available, but that the traditional model provides nonsensical results beyond this range (see text).
Based on the data in Pandian (1967).
828
PAULY: ESTIMATING FOOD CONSUMPTION OF FISH POPULATIONS
ly, these parameters do not provide information
which can be interpreted via another model.
2) The model implies values of K1 > 1 when a~llb
> W > 0, which is nonsensical.
3) The model implies that, except when W = 0,
Kx is always > 0, even in very large fish, although
it is known that fish cannot grow beyond certain
species-specific and environment-specific sizes,
whatever their food intake.
The new model proposed here has the form
Kx = 1 - (W/Wy (4)
with ft as a constant and Wm as the weight at which
Kx = 0. The model implies that Kx = 1 when W =
0, whatever the values of p and W^ (see Discussion
for comments on using values other than 1 as up-
per bound for Kx in Equation (4)). The new model
can, as the traditional model, be fitted by means of
a double logarithmic plot:
C = p log10 W„- p log10 W
(5)
where C = -log10 (1 - Kx), the sign being changed
here to allow the values of C to have the same posi-
tive sign as the original values of Kx. Interesting-
ly, it also appears that negative values of Kx (based
on fish which lost weight), which must be ignored
in the traditional model, can also be used in this
model (as long as they do not drag the mean of all
available Kx values below zero, see Table 1),
although their interpretation seems difficult.
The new model requires no more data, nor
markedly more computations than the old one. It
produces "possible" values of Kx over the whole
range of weights which a given fish can take. The
values of W^, which represent the upper bound of
this range can be estimated from
W^ = antilog10 (C intercept/ 1 slope |). (6)
Thus, while p has no obvious biological meaning,
the values of Wx obtained by this model do have a
biological interpretation, which is, moreover, anal-
ogous to the definition of Wx in the von Bertalanffy
growth function (VBGF) of the form
Table 1 .—Data on the food conversion efficiency of Channa striata (= Ophiocephalus
striatus) (after Pandian 1967), Epinephelus striatus (after Menzel 1960), and Hola-
canthus bermudensis (after Menzel 1958).
Body
weight
Food
conv.
Transformed data
C =
Species
and
(g)1
(KiP
iog10 w
log^K,
-log10(1-K
,) remarks
1.86
0.391
0.270
-0.408
0.215 v
9.92
0.274
0.998
-0.562
0.139 '
13.09
0.320
1.117
-0.495
0.167
19.65
0.284
1.293
-0.547
0.147
24.63
0.278
1.391
-0.556
0.141
35.09
0.234
1.545
-0.631
0.116 |
45.15
0.199
1.655
-0.701
0.096 '
Channa striata
50.70
0.227
1.705
-0.644
0.112
(see Figure 1)
51.30
0.235
1.710
-0.629
0.116
57.00
0.208
1.756
-0.682
0.101
79.80
0.177
1.897
- 0.752
0.085
93.80
0.232
1.972
-0.635
0.115
107.50
0.157
2.031
- 0.804
0.074 ,
0.079 /
123.80
0.166
2.093
- 0.780
216
0.247
2.334
-0.607
0.123 \
285
0.219
2.455
- 0.600
0.107
Epinephelus
319
0.160
2.504
-0.796
0.076
guttatus;
392
0.153
2.593
-0.815
0.072 (
log10 W = 2.617;
C = 0.0894
424
0.179
2.627
-0.747
0.086 [
628
0.161
2.798
-0.793
0.076 I
(see Figure 2)
647
0.177
2.811
- 0.752
0.085
649
0.187
2.812
-0.728
0.090 '
66
0.222
1.820
- 0.654
0.109 )
Holacanthus
139
0.178
2.143
-0.750
0.085 >
bermudensis
256
-0.258
2.408
not de-
fined
-0.100 J
(28°C only)3
log10 W = 2.124
C = 0.031
'Mean of starting and end weights.
2Growth increment/food intake.
3Note that the experiment considered here was conducted with a food which led to deposition
of fat, but not of protein (see also Table 2), a consideration that is ignored for the sake of this example.
829
FISHERY BULLETIN: VOL. 84, NO. 4
Wt = Wm (1 - e-^-fo))3
(7)
(von Bertalanffy 1938; Beverton and Holt 1957), and
where Wt, the weight at time t, is predicted via the
constants K, t0, and W^, all three of which are
usually estimated from size-at-age data obtained in
the field (see Gulland 1983 or Pauly 1984a).
That Wx values obtained via Equations (2) and (6)
are realistic can be illustrated by means of that part
of the data in Table 1 pertaining to Channa striata
(= Ophiocephalus striatus), the "snakehead" or
"mudfish" of south and southeast Asia. These data
give, when fitted to the traditional model
KY = 0.482 If"0-205.
(8)
The same data, when fitted to the new model give
Kx = 1 - (Ml,580)0073. (9)
(See Figure 1 for both models.) The value oiW00 =
1,580 g is low for a fish which can reach up to 90
cm in the field (Bardach et al. 1972). However, its
growth may have been reduced in laboratory growth
experiments conducted by Pandian (1967).
Equation (6) used here to predict W^ is extreme-
ly sensitive to variability in the data set investigated,
and two approaches are discussed to deal with this
problem.
The first approach is the appropriate choice of the
regression model used. In the example above (Equa-
tion (9)), the model used was a Type I (predictive)
regression, which is actually inappropriate, given
that
1) the log10 W values are not controlled by the
experimentator and
2) regression parameters are required, rather
than prediction of C values (see Ricker 1973).
The use of a Type II ("functional", or "Geometric
Mean") regression appears more appropriate; con-
version of a Type I to Type II regression (with
parameters a, b') can be performed straight-
forwardly through
b' = bl\r\
and
a = C - b' log10 W
(10)
(11)
where r is the correlation coefficient between the
C and the log10 W values (Ricker 1973). In the case
of the example here, one obtains with r = 0.942 a
new model:
Kx = 1 - (W71,290)0077
(12)
close to that obtained using a Type I regression, due
to the high value of r of this example. However, in
cases where the fit to the model is poor, the use of
a Type II regression can make all the difference
between realistic and improbable values of W^.
Another approach toward optimal utilization of
the properties of the new model (4) is the use of "ex-
ternal" values of asymptotic weight, which will here
be coded W^ to differentiate them from values of
Wx estimated through the model. In such case, (i
can be estimated from
P = C/(log10 WM - log10 W)
(13)
in which W{ao) is an asymptotic size estimated from
other than food conversion and weight data, e.g.,
from growth data or via the often observed close-
ness between estimates of asymptotic size and the
maximum sizes observed in a given stock (see Pauly
1984a, chapter 4).
These two approaches are illustrated in the exam-
ple below, which is based on the data in Table 1 per-
taining to the grouper Epinephelus guttatus. When
Equation (6) is interpreted as a Type I regression,
these data yield a value of W^ > 12 kg, which is far
too high for a fish known to reach 55 cm at most
(Randall 1968). Interpreting Equation (5) as a Type
II regression leads to a value of Wx = 3.5 kg which
is realistic, although still not close to the asymptotic
weight of 1,880 g estimated by Thompson and
Munro (1977). Finally, using the latter figure as an
estimate of W{oo) yields the model
Kx = 1 - (W/1,880)0136
(14)
as a description of the relationship between Kx and
weight in Epinephelus guttatus (Fig. 2). The value
of p in Equation (14) lies within the 95% confidence
interval of the value of p = 0.060 which generated
the first unrealistically high estimate of Wm.
MODEL FOR ESTIMATING
THE FOOD CONSUMPTION
OF FISH POPULATIONS
When feeding experiments have been or can be
conducted under conditions similar to those prevail-
ing in the sea (food type, temperature, etc.), the
830
PAULY: ESTIMATING FOOD CONSUMPTION OF FISH POPULATIONS
0.14
Wo, estimated through
Type I regression
Wm estimated through
Type H regression
■)£ Mean of y,x values
W(a,) input
from outside
loginAB(TypeI)\. logotype I)
10
0.00
K/
i X
7
2.0
2.5
3.0
3.5
4.0
Body weight (g, log units)
Figure 2.— Relationship between gross food conversion efficiency (KJ and body weight in
Epinephelus guttatus. Note that a Type I "predictive" regression leads to an overestimation
of W„ while a Type II "functional" regression leads to a value of W^ close to an estimate
of W^ based on growth data (see text). Based on data in Menzel (1960).
model presented above can be made a part of a
model for estimation of food consumption per unit
biomass (Q/B), provided a set of growth parameters
is also used in which the value of Wm or W{oo) is iden-
tical to that estimated from or used to interpret the
feeding experiments.
In this case, inserting Equation (8) into Equation
(5) leads to
Km = 1 - (1 - e-*«-<o))3P
(15)
where Kl(t) is the food conversion efficiency of the
investigated fish as a function of their age t, and
K, t0, and /? are as defined above.
Equation (1) is then rewritten as
dq/dt = (dw/dt) IK
i(«)
(16)
where rx = t - t0. Equations (17) and (15) may be
substituted into Equation (16), which is a separable
differential equation and may be solved by direct in-
tegration. The cumulative food consumption of an
individual fish between the age at recruitment (tr)
and the age at which it dies (tmax) is thus
Qc = W„ 2,K
'max
/
(1 - exp(-Kr1))2 ■ exp(-Kr1)
1 - (1 - exp(-Kr1))
3/3
dt.
(18)
The food consumption of a population should de-
pend, on the other hand, on the age structure of that
population. The simplest way to impose an age struc-
ture on a population is to assume exponential decay
with instantaneous mortality Z, or
Nt = R e-W-U
(19)
where the "growth increment" is replaced by a
growth rate (dw/dt) and the "food ingested" is also
expressed as a rate (dq/dt ). The growth rate of the
fish is then expressd by the first derivative of the
VBGF (Equation (7)) or
Q
dw/dt = W^ 3K(1 - expi-KrJ)2 ■ exp(-ifr1) (17) R
where tr is the age at recruitment (i.e., the starting
age at which Z applies, assuming, if there is any
fishery, that tr = tc, the mean age at first capture),
R the number of recruits, and Nt is the number of
fish in the population. As the model below assumes
a stationary population, the food consumption of the
population per unit time can be expressed on a per-
recruit basis or
= W„3K
fmax
/
(1 - exp(-Kr1))2 • exp(-(i!Lr1 + Zr2))
1 - (1 - exp(-iTr1))3/?
dt
(20)
831
FISHERY BULLETIN: VOL. 84, NO. 4
where r2 = t - tr.
The biomass per recruit in fish whose growth can
be described by Equation (7) is, according to the
model of Beverton and Holt (1957; see also Ricker
1975, p. 253):
| = Wm (A, + A2+ A3+ AA)
(21)
where Al =
A9 =
A9 =
and
AA =
1 - e~Zr3
-3 e~Kr* (1 - e^z+K^)
Z + K
3 e-2gr4 (! _ e-(Z+2K)r^
Z + 2K
_ e-3KrA fa _ e-(Z+3K)r3}
Z + 3K
where r3 = £max - tr
rA = t, - U.
This model assumes, as does Equation (20), a stable
age distribution.
Combining Equations (21) and (20) leads to the
model for estimating Q/B, which has the form:
APPLICATION EXAMPLE AND
SENSITIVITY ANALYSIS OF
THE MODEL
In the following application examples, the newly-
derived model (Equation (22)) is used to compare the
food consumption of a tropical carnivore (Epine-
phelus guttatus) with that of a tropical herbivore
(Holacanthus bermudensis). A list of the parameter
values used is given on Table 2.
The solutions of Equation (22), inclusive of the in-
tegration of its numerator, were obtained by means
of a short BASIC microcomputer program available
from me. Note that the integration, which according
to Equation (22) should be performed for the inter-
val between two ages (tr and £max), can be per-
formed for the intervals between two sizes (Wr,
Wmax), the age corresponding to these sizes being
estimated from the inverse of Equation (7); i.e.,
t = t0 - ((UK) (log, (1 - WIWJ™)). (23)
The results, i.e., the values of Q/B, expressed as
a percentage on a daily basis are 0.76 for E. gut-
tatus and 2.50 for H. bermudensis.
A sensitivity analysis of Equation (22) was per-
formed, following the outline in Majkowski (1982).
The results are given in Figure 3, which shows that
of the six parameters of Equation (22), (3 is the one
which has the strongest impact on the estimates of
Q
B
-max
Qir fq - exp(-/Cr1))2 • exy(-(Kr1+Zr2))
6KJ 1 - (1 - exv(-Kr{))W " at
(Ax + A2 + A3 + A4)
Equation (22) has only 6 parameters (K, t0, tr,
tmax, Z, and P); of these, K and t0 are estimated
from growth data, while tr and tmax can be set more
or less arbitrarily (see text below and Figure 3).
Total mortality (Z), which is here the equivalent of
a production/biomass ratio (see Allen 1971) can be
estimated easily, e.g., from length-frequency data
and growth parameters (see Pauly 1982, 1984a:
chapter 5) and is an input required anyway by the
ECOPATH program (Polovina 1984). Thus only p
and a "hidden" value of W^ applicable to both food
experiment and growth data are needed in addition
to the easily obtainable parameters required by this
model.
(22)
Q/B, while tr has the least, the relationships be-
tween the importance of these parameters being
best summarized by
p > K> Z » tmax > to > tr
(24)
These results suggest that, when using this model,
most attention should be given to an accurate esti-
mation of p (see below). It should be also noted that
P and K have opposite effects on the estimation of
Q/B (see Figure 3). Thus, a biased (e.g., high)
estimate of Wx will be associated with too low
values of p and K which partially compensate each
other.
832
PAULY: ESTIMATING FOOD CONSUMPTION OF FISH POPULATIONS
90
t w w
'o ' r » i
max
-50
-10 o 10
Input change (%)
50
Figure 3.— Sensitivity analysis of Equation (22), based on parameter estimates in Table 4 for
Epinephelus guttatus. Note strong effects of changes in /?, intermediate effects of K and Z, and
negligible effects of Wmax, Wr , and t0 .
Table 2.— Properties and parameter values of Epinephelus gut-
tatus and Holacanthus bermudensis relevant to the computation
of their food consumption (based on data in Menzel 1958, 1960;
See Table 1 and text).
Property/
Epinephelus
Holacanthus
parameter
guttatus
bermudensis
Asymptotic
weight (g)
1 1,880
2800
K(1/yr)
10.24
30.25
to (yo
4 -0.2
-0.2
t, (yr)
50.35
50.45
(3
60.136
20.040
Z (1/yr)
10.64
70.72
'max (y)
812
812
food (in
fish (Anchoa,
Algae (Monostroma
experiments)
Sardinella
oxysperma
and Haren-
and Enteromorpha
gula)
satina)
1From Thompson and Munro (1977); Z = 0.64 refers to an unfished stock
and is thus an estimate of M.
2From data in Table 1 and Equation (13).
3Based on method in Pauly and Munro (1984) and on growth parameter
estimates pertaining to members of the related family Acanthuridae, in Pauly
(1978).
4Assumed; has little influence on results (see text and Figure 3).
Corresponding to a fish of 1 g with growth parameters W^, K, and f0 as
given.
6See text and Figure 2.
7Based on equation (11) in Pauly (1980), with T = 28°, L„ = 30 cm, K =
0.25, and M = Z.
eAssumed; has little influence on results (see text and Figure 3).
QUANTITIES OTHER THAN QIB
ALSO ESTIMATED BY THE MODEL
In addition to estimating QIB, the model presented
above can be used to obtain other useful quantities;
namely, 1) maintenance ration and related informa-
tion, and 2) trophic efficiency.
Although there are differences between authors,
maintenance ration is usually defined as the food
used by fish to just maintain their weight at some
"routine" level of activity. Usually, maintenance ra-
tion is estimated by feeding fish over a wide range
of rations and determining by interpolation the ra-
tion generating neither weight gains nor losses
(Jones 1976).
The model presented here allows the estimation
of maintenance ration (even if fish have been fed
constant rations) through extrapolation of weight-
specific estimates of QIB, such as presented in
Figure 4 to the size W^, i.e., to the size at which,
by definition, all food consumed by a fish is used for
maintenance. In the case of the feeding data on E.
guttatus analyzed here, an estimate of daily main-
833
FISHERY BULLETIN: VOL. 84, NO. 4
(/>
</l
O
e
g
"E
k.
CD
Q.
C
o
V-
Q.
£
Z3
in
c
o
o
o
Q
1.2
1.0
0.8
0.6
,^_
0.4
^^
M
0.2
j
• maintenance ration = 0.5 % per day
i i i i
1
1
i
<
)
250 500 750 1,000
1,250
1,500
1,750 A
Wa
Body weight (g)
Figure 4.— Size-specific estimates of food consumption per unit biomass in Epinephelus guttatus,
as obtained by integrating Equation (22) over narrow ranges of weight, then plotting the resulting
Q/B estimates against the midranges of the weights. Note definition of maintenance ration as
"Q/B at Wm".
tenance ration of 0.5% body weight per day is ob-
tained (Fig. 4), while the corresponding value for
H. bermudensis is 1.73%.
Using the computed output of Equation (22) one
can also obtain an estimate of population trophic ef-
ficiency (ET) from
ET = Z ■ (B/Q)
(25)
which expresses production per unit food consumed,
production being expressed here as total mortality
(i.e., production/biomass ratio) times biomass (Allen
1971).
For E. guttatus, the estimated value of trophic
efficiency is ET = 0.23, i.e., slightly less than one
quarter of the fish food eaten by a population of
E. guttatus is turned into production. The cor-
responding value for H. bermudensis is ET =
0.08, which is low, as should be expected in an
herbivore.
ACCOUNTING FOR
MULTIFACTOR EFFECTS ON Kx
Experimental data allowing for the estimation of
values of Wm and p corresponding exactly to those
to be expected in nature cannot be obtained, since
no experimental design can account for all the en-
vironmental factors likely to affect the food conver-
sion of fishes in nature. Among the factors which
can be experimentally accounted for are
1) ration size (Paloheimo and Dickie 1966; but see
Condrey 1982),
2) type of food (see below),
3) temperature (Menzel 1958, Taylor 1958, Kinne
1960, and see below),
4) salinity (Kinne 1960).
Also, "internal states" affecting food conversion
efficiency, such as the sex of the fish, previous ther-
mal history, and stress undergone during an experi-
ment, can be accounted for given a suitable
experimental design.
One method of incorporating some of these fac-
tors into a linear form of the basic model (Equation
(5)) is to extend the model into a multiple regres-
sion of the form
C = a- H log10 W + b,V, + b2V2 . . . bnVn (26)
in which Vlt V2, and Vn are factors which affect C
(= -log10 (1 - K{)) after the effect of weight on C
has been accounted for.
For example,
C = 0.363 - 0.0419W - 0.0116T
+ 0.0156S + 0.0488M
(27)
834
PAULY: ESTIMATING FOOD CONSUMPTION OF FISH POPULATIONS
is derived from the results of experiments conducted
with dab (Limanda limanda) by Pandian (1970, figs.
5, 6)4 in which the type of food, M (0 = herring meat,
1 = cod meat), and sex, S (0 = o% 1 = 9), and the
temperature, T(in °C) were reported in addition to
the weight, W (in g and log10 units).
This model permits exact tests on the effects of
each factor (Table 3), and permits adjusting param-
eter values (W^, (1) so that they relate to conditions
resembling those occurring in nature.
Then, Wm is estimated— at least in principle—
from
4A table listing all values extracted from figures 5 and 6 in Pan-
dian (1970) is included in the document mentioned in footnote 1,
and will be supplied on request by me.
Table 3. — Details of a Type I multiple regression to quan-
tify the effects of some factors on the food conversion
efficiency of dab (Limanda limanda) (see text footnote 3).
Source of
variation
Degrees
of freedom
Sum of
squares
Mean
squares
Regression
Residual
Total
4
57
61
0.0813
0.0516
0.1329
0.0203
0.0009
F(4.57)
22.465 P < 0.001
multiple correlation = 0.7822
R2 = 0.6119
Corrected R2 = 0.5846
Standard error = 0.0301
Variable
Coefficient
t SE
P
Weight
Temp
Sex
Meat
Constant
-0.041869
-0.011584
0.015635
0.048840
0.363416
-3.926 0.0107
-7.362 0.0016
1 .982 0.0079
5.301 0.0092
<0.001
<0.001
0.049
<0.001
W„ = antilog10 (1/0) (a + bxVx + b2V2 . . . bnVn).
(28)
This equation implies that there is, for every com-
bination of Vx, V2, ... Vn values, a corresponding
value of W^. This is reasonable, as it confirms that
WM is environmentally controlled (Taylor 1958;
Pauly 1981, 1984b). W^- values obtained through
Equation (31) will generally be reliable— as was the
case with the one-factor model (4)— only when a wide
range of weights are included, variability is low, and
the correct statistical model is used.
As a first approach toward an improved statistical
model, one could conceive of a geometric mean
multiple regression which, in analogy to a simple
geometric mean regression, would be derived from
the geometric mean of the parameters of a series
of multiple regressions. This approach would in-
volve, in the case of n + 1 variables (= Y, Ylt Y2,
... Yn) in the following steps:
1) Compute the parameters of n + 1 Type I multi-
ple regressions, where each regression (j) has
another variable as dependent variable (i.e., Y, then
Ylt Y2, ... to Yn; see j = 1 to 5 in Table 4).
2) Solve each of the j equations for the "real"
dependent variable (Y = C, see j = 6 to 10 in Table
4).
3) Compute the geometric mean of each partial
regression coefficient from
b- = (V 62i -...&„/*. (29)
4) Compute the intercept of the new Type II
Table 4. Estimation of parameters in a "mixed" multiple regression (see also text).
Depen-
dent
/ variable
Constant
("a")
Independent variables and partial
regression coefficients1
Remarks
and R2
1 C
s
0.363
-0.0419
W
-0.016 T
+ 0.0156 S
+ 0.0488 M
0.585
2 W
=
3.52
-5.08
C
-0.0820 T
+ 0.0693 S
+ 0.300 M
0.199
3 T
=
23.1
-2.45
W
-42.1 C
+ 1.07 S
+ 1.94 M
0.490
4 S
=
-1.30
+ 0.151
W
+ 0.0780 T
+ 4.13 C
-0.285 M
0.035
5 M
=
-2.32
+ 0.341
w
+ 0.0739 T
-0.149 S
+ 6.76 C
0.295
6 C
=
0.363
-0.419
w
-0.0116 T
+ 0.0156 S
+ 0.0488 M
—
7 C
=
0.693
-0.197
w
-0.0161 T
+ 0.0136 S
+ 0.0591 M
—
8 C
=
0.549
-0.0582
w
-0.0238 T
+ 0.0254 S
+ 0.0461 M
—
9 C
=
-0.315
-0.0366
w
-0.0189 T
+ 0.242 S
+ 0.0690 M
not used,
10 C
=
-0.345
-0.0504
w
-0.0109 7"
+ 0.0220 S
+ 0.148 M
see text
mean partial regression
coefficients: to,
= -0.0783
-0.0164
+ 0.0175
+ 0.0510
(for y = 6-8)
11 0.1564 =
12 C
a' -
(0.0.83
0.4892
1.738) -
-0.0783
(0.164
W
• 13.32) + i
-0.0164 T
[0.0175 • 0.581)
+ 0.0175 S
+ (0.051 • 0.226)
+ 0.051 M final result
1Note that body weight (IV) is here expressed in log10 units.
835
FISHERY BULLETIN: VOL. 84, NO. 4
multiple regression from
a = Y - (Vfi + 62^2 • • • + &.T.) (30)
where the 3^ are the means of the Fr values and
6/ the geometric mean partial regression coeffi-
cients.
This method cannot be used here without modi-
fication because in most cases the multiple regres-
sion is "mixed" (Raasch 1983), consisting of vari-
ables which can be expected to generate normally
distributed residuals when used as dependent vari-
ables (here: C, W, T) as well as "dummy" or binary
variables (S, M) which cannot generate normally
distributed residuals when they are used as depen-
dent variables.
As might be seen in Table 4, the use of dummy
variables as "dependent" variables generates un-
stable interrelationships between the remaining
variables, making the computation of meaningful
mean partial regression coefficients impossible.
The best solution here seems to omit for the com-
putation of the mean regression coefficient those
multiple regressions which have binary variables as
"dependent" variables; Table 4 illustrates this
approach.
The mixed model so obtained is
C = 0.489 - 0.0738W - 0.01647/ + 0.0175S
+ 0.0151M
(31)
which corresponds to the standard model
C = 0.62W - 0.90T' + 0.195' + 0.46AT (32)
in which the original variables C, W, T, S, and M
are expressed in standard deviation units and in
which the slopes (= path coefficients, see Li 1975)
allow for comparing the effects of W, T, S, and M
on C. These variables suggest that with regards to
their impact on C,
T > W > M » S.
(33)
See Li (1975) for further inferences based on path
coefficients.
In the southern North Sea in late summer-early
autumn, Limanda limanda experiences tempera-
tures usually ranging between 10° and 20°C (Lee
1972). Solving Equation (31) for T = 18°C, the
highest temperature in Pandian's experiments (i.e.,
assuming the higher late summer-early autumn
temperatures limit WJ leads to estimates of W =
500 g for the females and 298 g for the males, com-
pared with the values of 756 and 149 g obtained by
Lee (1972) on the basis of growth studies.
Estimating values of /? that are wholly compatible
with the latter estimates of W^ is straightforward,
however, since it consists of solving Equation (31)
forT=18°C,M=0, and the appropriate value of
S, based on the equation
P = 1/log WM (a + VVi + b2'V2 . . . bn'Vn) (34)
In the present case, this leads to /3 values of 0.073
and 0.089 for females and male dab, respectively.
The "average" relationship (if such exists) between
food conversion efficiency and body weight in female
dab fed herring meat is thus
Kx = 1 - (H7756)0073
while for males it is
Kx = \ - (IF/149)0089
(35)
(36)
with both values of fi within the 95% confidence
interval of the first estimate of /3 (in Equation (27),
see Table 3).
DISCUSSION
The model presented here for the computation of
Q/B is not meant to compete against the more
sophisticated models whose authors were cited
above. Rather, it was presented as a mean of link-
ing up the results of feeding experiments with
elements of the theory of fishing such that infer-
ences can be made on the food consumption of fish
populations which 1) do not invoke untenable
assumptions, 2) make maximum use of available
data, and 3) do not require extensive field sampling.
A distinct feature of the method is that it does not
require sequential slaughtering of fish for the esti-
mation of their stomach evacuation rate, nor field
sampling of fish stomachs, which may be of rele-
vance when certain valuable fishes are considered
(e.g., coral reef fishes in underwater natural parks).
Several colleagues who reviewed a draft version
of this paper suggested that Equation (4) should in-
corporate an upper limit for Kx smaller than unity.
This model would have the form
Kx = Klmax - (W/WJP™
(37)
with parameters W^ and (im identical and analogous
respectively to those in Equation (4) and a value of
836
PAULY: ESTIMATING FOOD CONSUMPTION OF FISH POPULATIONS
Klmax to be estimated independently prior to fitting
Equation (37) to data.
Data do exist which justify setting the upper limit
of Kx at or near unity. They pertain to fish em-
bryos, whose gross conversion efficiency can be
defined by
Kx =
Wh
we - wy
(38)
where Wh is the larval weight at hatching, We the
egg weight, and Wy is the weight of the yolk sac at
hatching. Values of Kx as high as 0.93 have been
reported using this approach (From and Rasmussen
1984), extending further toward unity the range of
Kx values reported by earlier authors, e.g., 0.85 in
Solea solea (Fliichter and Pandian 1968), 0.79 in Sar-
dinops caerulea (Lasker 1962), and 0.74 in Clupea
harengus (Blaxter and Hempel 1966).
Thus, for a wet weight of 0.5 mg corresponding
to a spherical egg of 1 mm diameter, one obtains,
using Equation (14) for E. guttatus, a value of K1
= 0.87 which is within the range of Kx values given
above. This example is not meant to suggest that
Kx values pertaining to large fish should be used in
combination with the model presented here to
"estimate" K1 in eggs or larvae. Rather, it is
meant to illustrate the contention that, of the possi-
ble choices of an upper bound for Kx in Equation
(4), the one selected here has the feature of making
the model robust, particularly with respect to high
values of Kx and extrapolations toward low values
of W.
Apart from (1, the key elements of the model
(isometric von Bertalanffy growth, constant ex-
ponential decay, steady-state population) are all
parts of other, widely used models. Thus, whether
estimates of QIB obtained by this model are con-
sidered "realistic" or not will depend almost entirely
on the value of (i used for the computation.
There are several ways of reducing the uncertain-
ty associated with p. The following may need special
consideration:
1) Feeding experiments used to estimate p could
be run so as to mimic as closely as possible the
crucial properties of the habitat in which the popula-
tion occurs whose QIB value is estimated, inclusive
of seasonally oscillating factors.
2) Further research and study should lead to the
identification of anatomical, physiological, and
ecological properties of fish correlating with their
most common value of ft.
3) An additional parameter could be added to
account for fish reproduction, which is not explicit-
ly considered in Equation (22).
Little needs to be said about item 1 which should
be obvious since (except in the context of aquacul-
ture) feeding and growth experiments are conducted
in order to draw inferences on wild populations.
With regards to item 2, it suffices to mention that
relative gill area ( = gill surface area/body weight),
which appears to a large extent to control food con-
version efficiency (Pauly 1981, 1984b), should be a
prime candidate for correlational studies. Item 3
could cause QIB values obtained by the model pre-
sented here to substantially underestimate actual
food consumption, were it not for three circum-
stances which produce opposite tendencies:
a) The assumption that the energy needed by fish
to develop gonads is taken from the energy other-
wise available for growth may not apply (lies 1974;
Pauly 1984b). Rather, the reduction of activity
occurring in some maturing fish may more than
compensate for the energy cost of gonad develop-
ment (Koch and Wieser 1983).
b) Growth parameters are usually computed using
size data from fish whose gonads have not been
removed, thus accounting for at least a fraction of
the food converted into gonad tissue. When the
value of Z used in the model is high, this fraction
will be large because the contribution of the older
fish to the overall estimate of QIB will be small.
c) Experimental fish are usually stressed and
therefore have lower conversion efficiencies than
fish in nature, even though they may spend little
energy on food capture (see Edwards et al. 1971).
This effect leads to low values of ft and hence high
estimates of QIB.
Because of these factors, the values of QIB obtained
by the method proposed here may lack a downward
bias.
ACKNOWLEDGMENTS
I wish to thank R. Jones (Aberdeen), as well as
E. Ursin (Charlottenlund), A. McCall (La Jolla), J.
J. Polovina (Honolulu), P. Muck (Lima), and the two
anonymous reviewers for their helpful comments on
the draft of this paper.
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FISHERY BULLETIN: VOL. 84, NO. 4
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839
FISHERY BULLETIN: VOL. 84, NO. 4
APPENDIX
List of symbols used in model development and illustration
b'
B
AX-AA terms used in computation of biomass per
recruit (Equation (21))
a - multiplicative term in equation linking Kx
and body weight (Equation (3))
- intercept of a Type I (multiple) linear re-
gression
a - intercept of a Type II (multiple) linear re-
gression
b - slope of a Type I linear regression
- exponent in equation linking Kx and body
weight
bc - slope of a Type I multiple linear regression
- slope of a Type II linear regression
- slope of a Type II multiple linear
regression
- biomass (under equilibrium condition)
- exponent in model linking Kx and body
weight (Equation (4))
- similar to ft, but estimated jointly with
#imax (Equation (37))
- (-log10(l - KJ)
- same as C, but expressed in standard
deviation units
- rate of food consumption
- rate of growth in weight
- trophic efficiency, i.e., production by popu-
lation/food consumption by population
i - counter for number of variables in a multi-
ple regression
j - counter for number of multiple regres-
sions
K - constant in VBGF
Kx - gross conversion efficienty (Equation (1))
■^lmax ■ hypothetical upper limit for Kx (with
#lmax < 1) (Equation (37))
M - instantaneous rate of natural mortality
- a dummy variable expressing food type
(Equation (27))
M' - a dummy variable expressing food type in
standard deviation units
n - number of partial regression coefficient
used in computing a given value of 6/
N - number of fish in population (Equation
(19))
840
C
C
dq/dt
dwldt
Q - food consumption of a population (per unit
time)
Q/B - food consumption per unit biomass of an
age-structured animal population
Qc - cumulative food consumed by a single fish
between ages tr and tmax (Equation (22))
R - number of recruits (Equation (19))
r - product moment correlation coefficient
5 - a dummy variable expressing sex
S' - a dummy variable expressing sex in stan-
dard deviation units
t - age
tc - mean age at first capture (in an exploited
stock)
£0 - a parameter of the VBGF expressing the
theoretical age at size zero
^max ■ maximum age considered (= longevity)
tr - mean age at recruitment to the part of the
population considered when computing
Q/B
temperature in °C
temperature in °C, expressed in standard
deviation units (Equation (32))
any variable beyond W which affects Kx
the von Bertalanffy growth function
body weight (in log units in some cases)
body weight (in log10 units), expressed in
standard deviation units
weight of a fish egg
weight of a fish at hatching (yolk sac ex-
cluded)
body weight corresponding to tmax
body weight corresponding to tr
mean weight at age t
yolk sac weight in a newly hatched fish
asymptotic weight in the VBGF or in new
model (Equation (4))
an estimate of asymptotic weight obtained
indirectly (i.e., from data of a type differ-
ent than those in model using value of
W
Y{ - any variable included in a multiple regres-
sion
Z - instantaneous rate of mortality (= PIB
ratio)
T
T
Vi
VBGF
W
w
wc
wh
w
" max
wr
wt
wy
w,
(oo)
REPRODUCTIVE BIOLOGY OF KING MACKEREL, SCOMBEROMORUS
CAVALLA, FROM THE SOUTHEASTERN UNITED STATES
John H. Finucane, L. Alan Collins, Harold A. Brusher,
and Carl H. Saloman1
ABSTRACT
The reproductive biology of king mackerel, Scomberomorus cavalla, was studied from specimens collected
off Texas, Louisiana, and northwest Florida in the Gulf of Mexico and off North and South Carolina
in the Atlantic Ocean. Gonads were examined from 1,163 females and 595 males obtained in 1977-78.
Spawning was prolonged. Most king mackerel were reproductively active from May through September.
A few fish were in spawning condition as early as April and as late as October. All females were mature
at 850-899 mm fork length (FL). Estimates of fecundity ranged from about 69,000 to 12,207,000 eggs
for fish from 446 to 1,489 mm FL, 618 to 25,610 g total weight (TW), and 1 to 13 years of age. Fecundity
(F) was usually significantly correlated with FL, TW, and age in each area but TW was the best predic-
tor of fecundity in all areas combined (F = 1.854 x 101 (TW)1'361) with r2 = 0.856.
King mackerel, Scomberomorus cavalla, is one of the
most valuable commercial and recreational fish in
the Gulf of Mexico and south Atlantic. It is an
epipelagic, neritic species that occurs in the western
Atlantic Ocean from Massachusetts to Rio de
Janeiro, Brazil (Collette and Russo 1979, 1984). Most
of the king mackerel caught off the southeastern
United States are landed in Florida (Manooch 1979)
where it is an important component of charter boat
catches (Moe 1963; Brusher et al. 1978). Commer-
cial landings in Florida during 1983 totaled 2,017
t and the estimated recreational catch from the Gulf
of Mexico was 1,090,000 fish in 1984 (U.S. Depart-
ment of Commerce 1985a, b).
Although much has been written on king mack-
erel, little is known of its reproductive biology
(Manooch et al. 1978). Ovarian histology and size-
at-maturity has been described by Alves and Tome
(1967) for fish from Brazil and by Beaumariage
(1973) for fish from Florida. Maturation based on
blood hormone levels from fish off northwest Florida
was reported by MacGregor et al. (1981). Spawn-
ing times and areas have been inferred from ichthyo-
plankton collections of king mackerel larvae (Dwinell
and Futch 1973; Finucane and Collins 1977; Houde
et al. 19782; McEachran et al. 1980). The only fecun-
'Southeast Fisheries Center Panama City Laboratory, National
Marine Fisheries Service, NOAA, 3500 Delwood Beach Rd.,
Panama City, FL 32407-7499.
2Houde, E. D., J. C. Leak, C. E. Dowd, S. A. Berkely, and W.
J. Richards. 1979. Ichthyoplankton abundance and diversity in
the eastern Gulf of Mexico. Part I: Executive summary, abstract,
text reference. Unpubl. manuscr., 119 p. Draft Final Report to
dity estimates in the literature were made by Ivo
(1974) for fish from Brazil.
The purpose of our study was to provide additional
information on king mackerel reproductive biology
by determining spawning season, length-at-
maturity, and fecundity from four areas off the
southeastern coast of the United States. This infor-
mation will be useful in the management of king
mackerel since the measure of reproductive poten-
tial is a basic element of productivity and stock
dynamics (Baglin 1982).
METHODS
King mackerel were sampled from commercial
and recreational catches in four separate areas along
the coast of the southeastern United States during
1977 and 1978 (Fig. 1). These areas were I, the
northwestern Gulf of Mexico off the central and
south coasts of Texas; II, the northcentral Gulf off
Louisiana and Mississippi; III, the northeastern Gulf
off northwest Florida; and IV, the western Atlan-
tic Ocean off South and North Carolina.
Procedures for processing gonads, weighing, and
measuring fish followed the methods of Finucane
and Collins (1984). If no total weight had been
recorded for a fish, we estimated TW by using the
formula TW = 1.4959 x 10 "5 (FL)2-89284 (TW =
total weight in grams; FL = fork length in milli-
meters). This formula (Ricker 1975) was derived
Manuscript accepted April 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
Bureau of Land Management, Contract AA550-CT7-28. Rosen-
stiel School of Marine and Atmospheric Science, University of
Miami, Miami, FL 33149.
841
FISHERY BULLETIN: VOL. 84, NO. 4
GULF OF MEXICO
Figure 1.— Sampling areas for king mackerel, Scomberomorus cavalla, in the Gulf of Mexico and Atlantic Ocean during 1977-78.
from a length-weight regression (r = 0.996; n =
186) of king mackerel data from all areas.
Egg size distributions within the ovary were sta-
tistically compared to ensure that subsamples taken
for studies of maturation and fecundity were repre-
sentative (Yuen 1955; Otsu and Uchida 1959). Both
ovarian lobes were divided into three sections
(anterior, middle, and posterior) of about equal
length. At a selected point along each of these sec-
tions, a 2-4 mm thick cross section was cut and
removed. A wedged-shaped portion was then taken
from each of the three cross sections and divided
into three zones: inner, middle, and outer. A sam-
ple of 150 yolked eggs from each of the zones was
examined with a microscope and all eggs were mea-
sured to the nearest 0.02 mm at 500 x on whatever
axis the egg happened to be located in respect to
an ocular micrometer scale (Clark 1934). A chi-
square test of independence (Steel and Torrie 1960)
was used to test for significant differences in mean
egg diameters (EDs) among the sections, zones, and
zones within a section in each lobe.
Each wedge-shaped sample of eggs was placed in
a dish with 10% Formalin3 and the eggs were then
teased apart. Samples containing only unyolked
eggs (<0.20 mm ED) were considered to be from
immature fish and only 100 eggs from these samples
were measured. Samples with yolked eggs (^0.20
mm ED) were considered to be from mature fish and
300 eggs were measured.
Seasonal maturation was determined by plotting
monthly mean EDs of the most advanced eggs found
in each ovary and by gonadosomatic indices (GSI =
the percentage of TW represented by gonad
weight). The range and 95% confidence interval of
the monthly mean GSIs were also plotted. To com-
pare the variation of GSIs, we calculated the coef-
ficient of variation for each month. We estimated
the length at which the fish first matured by com-
puting mean GSIs for fish in each 50 mm interval
and used the length at which the greatest increase
in mean GSIs between consecutive FL intervals oc-
curred. For this analysis we only used data that were
collected during the fish's most sexually active
months as indicated by the highest values of mean
EDs and GSIs. An additional estimate was made for
females by assigning immature or mature status to
each fish according to egg stage and then calculating
the percentage of mature fish by FL intervals.
3Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
842
FINUCANE ET AL.: REPRODUCTIVE BIOLOGY OF KING MACKEREL
Fecundity estimates were based on the number
of yolked eggs ^0.20 mm in diameter in the most
mature ovaries. Similar methods were discussed by
Hunter and Goldberg (1980) and used by Morse
(1980). A diameter of 0.20 mm was used to separate
immature and mature eggs, because it was at this
size that yolk first appeared. A gravimetric method
was used for fecundity and followed the procedures
of Finucane and Collins (1984). Ages of fish were
determined from otoliths (Johnson et al. 1983).
Analysis of covariance was used to test for differ-
ences in fecundity by year and area. Regression and
correlation were used to examine the linear and
curvilinear relationships between fecundity and fork
length, total weight, and age.
RESULTS
Gonads from 1,165 female and 593 male king
mackerel were examined. Fish ranged in FL from
351 to 1,554 mm, in TW from 658 to 31,780 g, and
in age from 1 to 13 yr. Temporal coverage varied
from 3 mo in area I to 12 mo in area II. Number
and percentage composition of fish by area were
area I, 85 and 4.8%; area II, 646 and 36.7%;
area III, 768 and 43.7%; and area IV, 259 and
14.7%.
Analysis of the egg size distribution indicated that
there were significant differences (a = 0.05) in ED
between the inner, middle, and outer zones within
ovarian sections; there were no differences between
sections. Therefore, we took a wedge-shaped sam-
ple (representing the three cross-sectional zones)
from the middle of the right or left ovary as repre-
sentative of the entire ovary for ED analysis. King
mackerel ovaries were grouped into five reproduc-
tive stages based on ED. Stage I (immature ovaries)
contained eggs <0.06 mm. Eggs in stage II (resting
ovaries) ranged from 0.07 to 0.20 mm. Stage III
(maturing) and stage IV (mature) ovaries contained
eggs 0.21-0.50 mm and 0.51-0.71 mm, respective-
ly. Stage V eggs measured 0.71-1.20 mm and in-
dicated ripe ovaries.
The seasonal progression of mean GSIs and EDs
indicated that king mackerel have a prolonged
spawning season that varied between areas (Figs.
2-5). Peak spawning months occurred from May
through September as observed in 14 ripe females
from areas I, II, and IV. A few fish were in spawn-
ing condition as early as April and as late as Octo-
ber. In area I, GSIs and EDs peaked in July and
August for both sexes. Area II fish had the highest
GSIs and EDs for both sexes during May. In area
III, GSIs for both sexes were greatest during June
O 1
O 2
fir t
VI
-im-
MALES
NO. FISH
2 23 36
IX
0.50
0.40
0.30
0.20
0.10
0
FEMALES
NO. FISH 3 11 12
J J A
MONTHS
Figure 2.— Seasonal maturation cycle of male and female king
mackerel from area I (Texas) shown by monthly gonadosomatic
index (GSI) and mean egg diameters (EDs) in mm.
while EDs peaked in August. Area IV fish had the
highest female GSIs and EDs during July.
Serial spawning was suggested by several lines
of evidence. Distribution of EDs was multimodal
during spawning months. The highest coefficient of
variation for GSIs occurred during the spawning
months, suggesting that eggs were maturing and
released serially throughout the spawning season
(Table 1).
The size at maturation of king mackerel also
varied between areas. Maturity was based on the
number and percentage of fish with stage Ill-stage
V ova for each 50 mm FL interval. Length inter-
vals in which at least 50% of the females were
mature for areas I-IV, respectively, were 450-499
mm, 600-649 mm, 600-649 mm, and 650-699 mm
843
FISHERY BULLETIN: VOL. 84, NO. 4
5
4
to
O 2
MALES
1
0
NO. FISH
-B-
2 3
■§• T-'-fx
1 8 10 6 8 14
0
7
6
5
4
3
2
1
■FEMALES
95%C.I.-)
RANGE JJj.MEAN
MO. FISH 19 31 49 39 4 58 A
-*HHi-
■£*-*-
J FMAMJ JASOND
MONTHS
Figure 3.— Seasonal maturation cycle of male and female king
mackerel from area II (Louisiana and Mississippi) shown by month-
ly gonadosomatic index (GSI) and mean egg diameters (EDs) in
mm.
O 2
6
5
_ 4
O 3
MALES
NO. FISH 1 5 59 78 74 163
r^GEj
95%C.l.n
11-
MEAN
2 -
1 -
0
0.3
£0.2
IX
0.1
FEMALES
NO. FISH 7 41 107 76 85 72
i i I
J-
M J J A S O
MONTHS
Figure 4.— Seasonal maturation cycle of male and female king
mackerel from area III (northwest Florida) shown by monthly
gonadosomatic index (GSI) and mean egg diameters (EDs) in mm.
Table 1 .—Coefficient of variation for monthly GSIs of female (F) and male (M) king
mackerel in each area.
Area I
Area II
Area III
Area IV
Month
F
M
F
M
F
M
F
M
January
—
—
12.7
—
—
—
—
February
—
—
12.5
—
—
—
—
—
March
—
—
18.0
7.1
—
—
—
—
April
—
—
43.6
15.3
—
—
—
—
May
—
—
20.4
i
28.2
—
56.3
52.9
June
51.7
16.0
55.0
57.1
96.9
56.4
39.1
—
July
33.6
35.4
77.3
58.2
95.5
104.8
36.2
1
August
54.2
38.9
66.2
43.4
95.5
75.7
44.4
2.5
September
—
—
56.7
38.7
85.9
51.9
64.9
61.5
October
—
—
36.8
48.4
62.7
51.6
41.7
54.5
November
—
—
32.8
—
—
—
—
—
December
—
—
20.0
—
—
—
—
—
'n = 1
844
FINUCANE ET AL.: REPRODUCTIVE BIOLOGY OF KING MACKEREL
5 2
O
1
0
■RANGE
IX
_ 3
«/»
° 2
1
0
0.50
0.40
0.30
0.20
0.10
0
MALES
k
NO.FISH 2 1 2 8 89
NO FISH 3 12 10 8 20 104
MJ J A S O
MONTHS
FIGURE 5.— Seasonal maturation cycle of male and female king
mackerel from area IV (North and South Carolina) shown by
monthly gonadosomatic index (GSI) and mean egg diameters (EDs)
in mm.
(Table 2). All females were mature at 850-899 mm.
Another maturation pattern was noted when the
midpoints of fork length intervals were plotted
against mean GSIs for each area (Fig. 6). The size
interval where greatest increases in GSIs occurred
were 650-699 mm (area I), 700-749 mm (area II),
450-499 mm (area III), and 650-699 (area IV).
Fecundity ranged from 69,000 to 12,207,000 eggs
in 65 king mackerel from all areas. Fish ranged
in FL from 446 to 1,489 mm, in TW from 681 to
25,610 g, and in age from 1 to 13 yr (Table 3).
Analysis of covariance with TW as the covariate
showed no significant differences (a = 0.05) in
fecundity between years or among areas. The best
predictor of fecundity based on regression and cor-
relation analysis was TW for areas II, IV, and all
areas combined and FL for areas I and III (Table
4). Log transformed linear models were better pre-
dictors of fecundity than nontransformed models in
all areas but area IV.
DISCUSSION
Our results on the seasonal maturation and pro-
tracted spawning season of king mackerel agree
closely with other studies. In waters off Florida,
Beaumariage (1973) found late-maturing (stages III
and IV) eggs in king mackerel from May through
October. In the northeastern Gulf of Mexico (area
III), Dwinell and Futch (1973) caught king mackerel
larvae during the same time interval and MacGregor
et al. (1981) reported early- or late-maturing ovaries
from August through October. In the northwestern
Gulf of Mexico off Texas (area I), Finucane and Col-
lins (1977) and McEachran et al. (1980) noted
catches of larvae from May through August, and
April through October, respectively. In the area off
Cape Fear, NC, to Cape Canaveral, FL, Powles4 col-
lected king mackerel larvae from May through
September.
Length at maturation was difficult to determine
because the sample size of small fish (<600 mm) was
limited in all areas except area III (northwest
Florida). Using only fish from this area, maturity
first occurred about 450-499 mm and 50% of the fish
were mature at about 550-599 mm. These estimates
of maturity agreed with some of the other studies.
Female king mackerel first reached sexual matur-
ity at 630 mm and 4 yr of age (Gesteira and Mes-
quita 1976) or at 586 mm (Alves and Tome 1967)
off Brazil. Another study on Brazilian fish, however,
noted that females were first mature at 770 mm and
5-6 yr of age (Ivo 1972). In Florida waters, Beau-
mariage (1973) estimated that females 3 yr or
younger were immature and probably had not
spawned. He believed that the first major spawn-
ing by females and males occurred at 880 and 770
mm SL, respectively. Some of his 1-yr-old females
contained stage IV eggs that had been aborted or
reabsorbed since he did not find ripe (stage V) eggs
until the fish were 4 yr old. His standard length for
king mackerel from Florida at age 1 was 610 mm
(651 mm FL), which was higher than our estimate
of length at first maturity.
4Powles, H. W. Abundance and distribution of king mackerel,
(Scomberomorus cavalla) and Spanish mackerel (S. maculatus) lar-
vae of the southeast United States. Unpubl. manuscr. Gouvern-
ement du Canada, Peches et Oceans, Division des Sciences halieu-
tiques, C. P. 15500, Quebec, Canada GlK 7Y7.
845
FISHERY BULLETIN: VOL. 84, NO. 4
Table 2.— Total sample number and percentage of mature (Stages lll-V) king mackerel females
collected during the peak maturation season in each area.1
Area I
Area II
Area III
Area IV
(Louisiana,
(Northwest
(North and South
I
Texas)
Mississippi)
Mature
Florida)
Carolina)
Mature
Mature
Mature
Fork length
No.
(0/0)
No. (%)
No. (%)
No. (%)
300-349
0
0 —
0 —
0 —
350-399
1
0.0
0 —
1 0.0
0 —
400-449
0
—
0 —
2 0.0
0 —
450-499
1
100.0
0 —
3 33.3
0 —
500-549
0
—
0 —
16 6.3
0 —
550-599
0
—
0 —
28 46.4
0 —
600-649
2
100.0
2 100.0
31 71.0
1 0.0
650-699
0
—
0 —
31 71.0
4 75.0
700-749
4
100.0
1 100.0
35 80.0
2 100.0
750-799
8
100.0
0 —
29 62.1
5 100.0
800-849
6
100.0
0 —
41 75.6
4 100.0
850-899
2
100.0
5 100.0
29 100.0
11 100.0
900-949
2
100.0
6 100.0
21 100.0
8 100.0
950-999
0
—
22 100.0
19 100.0
7 100.0
1,000-1,049
0
—
19 100.0
13 100.0
3 100.0
1,050-1,099
0
—
18 100.0
4 100.0
3 100.0
1,100-1,149
0
—
18 100.0
6 100.0
1 100.0
1,150-1,199
0
—
13 100.0
4 100.0
1 100.0
1 ,200-1 ,249
0
—
18 100.0
2 100.0
0 —
1,250-1,299
0
—
14 100.0
1 100.0
0 —
1 ,300-1 ,349
0
—
17 100.0
0 —
0 —
1,350-1,399
0
—
11 100.0
0 —
0 —
1,400-1,449
0
—
3 100.0
0 —
0 —
1,450-1,499
0
—
2 100.0
0 —
0 —
Total
26
169
316
50
'Area I, June-August; Area II, May-August; Area III, May-September; and Area IV, June-September.
Factors influencing the maturation cycle of king
mackerel are not well known. Presumably, photo-
period and water temperature are important for
spawning, egg, and larval development. Beau-
mariage (1973) indicated that seasonal changes
in photoperiod influenced the spawning of king
mackerel while McEachran et al. (1980) noted that
larvae were more abundant at temperatures
from 20.2° to 29.8°C and salinities from 28.2 to
34.47oo. A study by MacGregor et al. (1981) also
showed that the levels of serum androgens and
estrogens may be indicators of maturation in king
mackerel.
Our inferences on spawning peaks and activity of
king mackerel, as determined by largest mean EDs,
usually coincided with those of other studies. Our
largest mean ED of 0.61 mm agrees with the 0.60
mm reported by Alves and Tome (1967). In contrast,
the largest mean ED of 0.33 mm shown by Beau-
mariage (1973) suggests that most of his fish were
not ready to spawn. Our largest mean egg sizes from
northwest Florida fish were similar to those re-
ported by Beaumariage (1973) and probably in-
dicates that spawning activity off the west coast of
Florida is not extensive. Peak spawning months by
area in this study were area I, August; area II, May;
area III, August; and area IV, July. In the north-
western and northeastern gulf, (our areas I and III)
the highest catches of larval king mackerel occurred
during September (Dwinell and Futch 1973;
McEachran et al. 1980). Houde et al. (fn. 2) stated
that because of their rare catches of larvae, king
mackerel does not appear to spawn frequently in the
eastern gulf.
The reproductive cycle of king mackerel off the
coast of Brazil is probably similar to that of this
species from American waters. Ivo (1972) noted that
spawning occurred throughout the year off the state
of Ceara which is south of the Equator. Other
studies indicate that they begin to spawn from Octo-
ber through December (Menezes 1969) with peaks
in November and March (Gesteria and Mesquita
1976). Since the seasons are reversed in this area,
they would correspond to our spring and late sum-
mer spawning peaks for king mackerel.
We were unable to determine the number of times
individual king mackerel spawn during the year
from the data. Beaumariage (1973) concluded that
king mackerel were multiple spawners, based on
their extended spawning season and presence of
several modal groups of yolked eggs. Morse (1980)
reported that individual Atlantic mackerel, Scomber
846
FINUCANE ET AL.: REPRODUCTIVE BIOLOGY OF KING MACKEREL
3.0 1-
2.5
2.0
1.5
1.0
0.5
0
2.5
2.0
1.5
1.0
0.5
0
NORTH CAROLINA
SOUTH CAROLINA
AREA IV
N = 50
-J I L
J I L
J I I I ' '
NORTHWEST FLORIDA
woo
O
1.5
z 1.0
2 0.5
* 0
2.5
2.0
1.5
1.0
0.5
0
_l L
AREA III
N=316
j i_j i
LOUISIANA,
MISSISSIPPI
. TEXAS
AREA I
N=26
3
2
5
4
2
5
5
2
5
l i ' '
6
2
5
7
2
5
8
2
5
_
9
2
5
1
0
2
5
I I I l
1
1
2
5
1
2
2
5
■ ' ' i
1
3
2
5
1
4
2
5
I L
MIDPOINTS OF FORK LENGTH INTERVALS (mm)
Figure 6.— Mean GSI plotted by midpoint of fork length interval for female king
mackerel in each area.
scombrus, are capable of spawning six batches of
eggs during the spawning season. Documentation
of spawning frequency and numbers of eggs pro-
duced will require that king mackerel be held in
captivity.
Major spawning areas for king mackerel could not
be determined during this study because of the scar-
city of ripe fish. Gonad maturation data suggest that
spawning occurs throughout the sampling areas but
the magnitude of spawning and extent of spawning
areas are unknown. Ichthyoplankton surveys con-
ducted by Wollam (1970), Houde et al. (fn. 2), and
McEachran et al. (1980) have revealed general
spawning locations of king mackerel by the occur-
rence of small larvae (<3 mm SL). These studies in-
dicate that spawning probably occurs over the con-
tinental shelf of the northwestern and northeastern
Gulf of Mexico. Most small larvae collected by
McEachran et al. (1980) were captured over the mid-
dle and outer continental shelf in water depths of
35-130 m off the Texas coast.
No comparative fecundity data were available
from the southeastern U.S.; however, Ivo (1974)
determined fecundity for 39 fish from Brazilian
waters. He found great variation in fecundity for
fish with the same fork length.
The fact that disjunct spawning appears to occur
off the Carolinas and in the northcentral and west-
ern Gulf of Mexico from spring through fall may sug-
gest separate stocks of king mackerel in these areas.
847
FISHERY BULLETIN: VOL. 84, NO. 4
Table 3.— Summary of data on king mackerel for which fecundity was estimated, 1977-78.
Fork
Gonad
Total
Gonad
Fork
Gonad
Total
Gonad
length
weight
weight
index
Fecundity
length
weight
weight
index
Fecundity
Date
(mm)
(g)
(g)
(x100)
Age
(estimated)
Date
(mm)
(g)
(g)
(x100)
Age
(estimated)
Area I (Texas)
Area III (Northwest Florida)
8/26/78
500
18.16
900
2.02
2
185,608
8/8/77
508
9.24
944
0.98
1
196,938
7/8/78
650
55.66
2,270
2,45
—
985,340
8/8/77
568
11.95
1,318
0.91
1
160,722
7/26/78
750
76.09
3,042
2.50
4
1,082,301
8/7/77
608
24.70
1,950
1.27
1
404,982
8/26/78
760
35.23
3,166
1.11
—
466,252
7/2/78
652
39.53
2,497
1.58
1
688,354
7/8/78
770
92.87
3,405
2.73
2
1,194,283
8/14/77
727
105.96
3,180
3.33
2
1 ,640,497
7/8/78
800
142.53
4,086
3.49
4
2,009,870
7/14/77
780
139.64
3,424
4.08
—
2,102,579
7/8/78
810
135.50
4,313
3.14
—
1,435,752
6/27/78
816
301.26
4,450
6.64
—
5,049,856
7/8/78
835
82.96
4,540
1.83
4
1 ,380,342
8/7/78
826
167.31
4,903
3.41
2
2,912,649
7/8/78
860
176.00
4,994
3.52
5
2,753,638
6/19/77
862
186.02
4,680
3.98
4
2,509,948
7/8/78
870
130.19
4,994
2.61
5
2,236,664
7/4/78
906
210.33
5,630
3.74
6
3,005,716
8/7/78
895
212.86
5,448
3.91
6
2,309,622
6/27/78
929
96.05
6,492
1.48
—
1,891,588
—
—
239.41
4,183
—
3
4,183,921
7/13/77
980
205.49
8,170
2.52
—
3,346,332
Area II (Louisiana)
7/20/77
6/19/77
1,018
1,087
268.22
602.45
12,700
1 1 ,350
2.11
5.31
7
4,960,702
5,744,230
6/24/78
446
8.43
681
1.24
—
69,264
8/24/77
1,108
476.06
9,768
4.87
—
5,836,910
6/23/77
635
13.45
1,930
0.70
1
182,863
9/5/78
1,142
538.60
12,031
4.48
8
8,070,585
6/20/77
710
26.92
2,500
1.08
2
2,570,133
8/14/78
1,220
575.39
14,437
3.99
7
7,489,089
9/13/77
852
96.36
4,380
2.20
4
1,179,625
7/13/78
895
158.51
5,130
3.09
4
2,079,204
Area IV (North Carolina)
8/15/77
951
239.09
6,221
3.84
—
4,448,492
7/13/77
617
171.17
5,765
2.97
—
2,625,338
5/20/78
972
451.68
7,310
6.18
6
6,319,134
9/9/78
780
131.11
3,632
3.61
3
1,667,418
5/20/78
994
577.18
11,120
5.19
6
5,890,631
7/28/78
841
207.22
5,766
3.59
4
2,330,248
7/7/78
1,025
325.56
9,000
3.62
6
4,686,248
9/21/78
844
100.07
4,722
2.12
4
969,206
8/7/78
1,037
417.00
8,325
5.01
6
6,437,542
7/26/78
865
150.50
4,631
3.25
—
1,639,189
6/23/78
1,055
314.33
8,626
3.64
11
4,686,598
7/15/78
869
227.67
4,767
4.78
—
2,795,451
9/3/77
1,086
303.52
9,750
3.11
—
5,401,961
9/9/78
880
119.88
4,858
2.47
5
1 ,236,055
6/25/78
1,109
247.66
9,534
2.60
—
2,771,744
7/1/78
900
170.57
6,628
2.57
4
3,321,377
6/25/78
1,149
401.59
10,896
3.69
9
4,268,537
8/27/78
972
214.00
7,173
2.98
6
3,204,055
6/16/78
1,178
478.74
13,286
3.60
6
8,899,756
8/27/78
996
282.01
7,718
3.65
6
2,652,453
7/10/78
1,194
447.88
9,045
4.95
10
6,010,133
9/9/78
1,000
267.35
6,992
3.82
8
2,797,301
4/29/78
1,220
498.52
15,150
3.29
9
7,315,781
8/30/78
1,050
416.04
9,988
4.17
8
6,102,347
5/20/78
1,229
698.36
14,070
4.96
6
10,116,890
6/17/78
1,265
611.04
15,095
4.05
9
9,209,082
6/17/78
1,291
468.64
15,890
2.95
10
7,487,826
8/10/77
1,312
583.79
17,120
3.41
—
6,689,189
5/20/78
1,316
840.08
17,800
4.72
10
10,711,026
6/17/78
1,370
570.66
19,885
2.87
11
7,650,064
8/15/78
1,489
815.00
25,610
3.18
13
12,206,888
Table 4.— Regressions of fecundity (F) on total weight (TW), fork length (FL),
and age (A) of king mackerel by areas.
Area
Predictor
Equation
r2
I
TW
F
=
8.554
X
101(TW)1465
0.745
(TX)
FL
F
=
8.816
X
10-7(FL)4 206
0.781
A
F
=
2.487
X
105(A)1.390
0.373
II
TW
F
=
1.475
X
101(TW)1381
0.847
(LA-MS)
FL
F
=
9.973
X
10_7(FL)4175
0.840
A
F
=
4.207
X
105(A)1313
0.721
III
TW
F
=
1.327
X
101(TW)1408
0.877
(NWF)
FL
F
=
1.918
X
10_7(FL)4455
0.884
A
F
=
4.684
X
105 + 9.494 x
105(A)
0.870
IV
TW
F
=
1.419
X
106 + (6.658 x
102)TW
0.760
(NC-SC)
FL
F
=
-2.554
x 106 + (5.840
x 103)FL
0.257
A
F
=
-2.778
x 105 + (5.579
x 105)A
0.436
l-IV
TW
F
=
1.854
X
101(TW)1361
0.856
(All areas)
FL
F
=
4.391
X
10-6(FL)3 974
0.820
A
F
=
3.399
X
105(A)1356
0.730
848
FINUCANE ET AL.: REPRODUCTIVE BIOLOGY OF KING MACKEREL
Williams and Godcharles5 have postulated on the
basis of mark-recapture data that two migratory
groups occur: one in the South Atlantic and the
other in the Gulf of Mexico. Both of their ranges
overlap in south Florida.
ACKNOWLEDGMENTS
We thank Dale S. Beaumariage, Churchill B.
Grimes, and Steven A. Bortone for their critical
review of this manuscript.
LITERATURE CITED
Alves, M. I. M., and G. S. Tome.
1967. Alguns aspectos do desenvolvimento maturativo das
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1982. Reproductive biology of western Atlantic bluefin tuna.
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1973. Age, growth, and reproduction of king mackerel, Scom-
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Brusher, H. A., L. Trent, and M. L. Williams.
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1934. Maturity of the California sardine (Sardina caerulea),
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1984. Morphology, systematics, and biology of the Spanish
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DWINELL, S. E., AND C. R. FUTCH.
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1977. Environmental assessment of an active oil field in the
northwestern Gulf of Mexico, 1976-1977. Ichthyoplankton,
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1984. Reproductive biology of cero, Scomberomorus regalis,
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1976. Epoca de reproducao tamanho e idade na primeira
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burg, FL 33701.
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Hunter, J. R., and S. R. Goldberg.
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1972. Epoca de desova e idade na primeira maturacao sex-
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1974. Sobre a fecundidade da cavala, Scomberomorus cavalla
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Johnson, A. G., W. A. Fable, Jr., M. L. Williams, and L. E.
Barger.
1983. Age, growth, and mortality of king mackerel, Scom-
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MACGREGOR, R. M., Ill, J. J. DlNDO, AND J. H. FINUCANE.
1981. Changes in serum androgens and estrogens during
spawning in bluefish, Pomatomus saltator, and king macker-
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Manooch, C. S., III.
1979. Recreational and commercial fisheries for king mack-
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Gulf of Mexico, U.S.A. In E. L. Nakamura and H. R. Bullis,
Jr. (editors), Proceedings of Colloquium on the Spanish and
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33-41. Gulf States Marine Fisheries Commission No. 4.
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1978. Annotated bibliography of four Atlantic scombrids:
Scomberomorus brasiliensis, S. cavalla, S. maculatus, and
S. regalis. U.S. Dep. Commer., NOAA Tech. Rep. NMFS
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1980. Distribution, seasonality and abundance of king and
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1969. Alimenta?ao da cavala, Scomberomorus cavalla
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Mar. 9(l):15-20.
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1963. A survey of offshore fishing in Florida. Fla. State
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Morse, W. W.
1980. Spawning and fecundity of Atlantic mackerel, Scomber
scombrus, in the Middle Atlantic Bight. Fish. Bull., U.S.
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1959. Sexual maturity and spawning of albacore in the Pacific
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Ricker, W. E.
1975. Computation and interpretation of biological statistics
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1960. Principles and procedures of statistics (with special
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1985a. Fisheries of the United States, 1984. Current Fish-
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849
FISHERY BULLETIN: VOL. 84, NO. 4
Wollam, M. B. Dep. Nat. Resourc. Mar. Res. Lab. Tech. Ser. 61, 35 p.
1970. Description and distribution of larvae and early juven- Yuen, H. S. H.
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Spanish mackerel, Scomberomorus maculatus (Mitchill), Spec. Sci. Rep. Fish. 150, 30 p.
(Pisces: Scombridae) in the western north Atlantic. Fla.
850
NEW OCCURRENCE OF EPIZOOTIC SARCOMA IN
CHESAPEAKE BAY SOFT SHELL CLAMS, MYA ARENARIA
C. A Farley,1 S. V. Otto,2 and C. L. Reinisch3
ABSTRACT
Maryland soft shell clams, My a arenaria, from Chesapeake Bay were sampled from 1969 through January
1983. Four cases of sarcomatous neoplasia were diagnosed histologically [1979 (1), 1982 (2), January
1983 (1)] in 3,584 animals. Hemocytologic sampling between December 1983 and May 1984 revealed
peak prevalences of 42-65% in clams from five sites. Sarcomas in laboratory-held clams progressed from
early to advanced stages and death. This is the first time epizootic neoplastic disease has been observed
in a wild molluscan population which was previously documented to be sarcoma-free. An infectious etiology
is implied and data indicate the potential for mass mortality of bay clams.
Neoplastic diseases in soft shell clams, Mya arenar-
ia, have been reported from New England popu-
lations in both polluted and nonpolluted areas (Barry
and Yevich 1975; Farley 1976a; Yevich and Barszcz
1977; Brown et al. 1977, 1979; Brown 1980; Cooper
et al. 1982a; Reinisch et al. 1984). Generally, the
types of neoplasia noted have been considered as
having hemocyte (blood cell) (Yevich and Barszcz
1977; Brown et al. 1977, 1979; Brown 1980; Cooper
et al. 1982a; Reinisch et al. 1984) and gonadal (Barry
and Yevich 1975; Yevich and Barszcz 1977; Brown
et al. 1977, 1979; Brown 1980) origins or have been
designated as sarcomatous (Farley 1976a). A single
neoplastic clam was reported from Chesapeake Bay
with an apparent teratoma composed of nerve and
muscle tissue and digestive epithelium (Harshbarger
et al. 1977). Chesapeake Bay soft clams collected
and examined by several authors between 1971 and
1978 were free of the neoplastic disease (Barry and
Yevich 1975; Brown 1980) with the exception of 1
case found in a collection of 3,000 clams used as ex-
perimental controls (Brown 1980). Evidence for a
viral etiology for hematopoietic neoplasia in clams
was reported in a Rhode Island study (Oprandy et
al. 1981). Improved techniques such as examination
of hemolymph using a combination of histologic and
cytologic procedures (Cooper et al. 1982b) and the
development of a monoclonal antibody test specific
for neoplastic clam cells (Reinisch et al. 1983) have
facilitated the identification and diagnosis of the
disease. High prevalences of sarcomas have been
■Northeast Fisheries Center Oxford Laboratory, National Mar-
ine Fisheries Service, NOAA, Oxford, MD 21654.
2Aspen Cove, Bozman, MD 21612.
3Tufts University School of Veterinary Medicine, Boston, MA
02111.
found repeatedly in populations of Chesapeake Bay
clams.
This paper documents the first occurrence of epi-
zootic sarcoma in soft shell clams in Chesapeake
Bay, and the first time neoplastic disease has ap-
peared in a wild molluscan population that was
previously shown to be free of the disease. Epizootic
prevalences of this condition may have a potential-
ly devastating impact on the clam industry of the
region.
MATERIALS AND METHODS
Sixty samples of 25 or more soft shell clams (total-
ing over 3,500 clams) have been collected periodi-
cally by the Maryland Department of Natural
Resources (DNR) or purchased from seafood outlets
from 51 sites in Chesapeake Bay since 1969. Each
animal was necropsied and tissues were fixed, pro-
cessed, and diagnosed histologically via standard
methods (Howard and Smith 1983) for diseases and
parasites. Recent samples (Table 1) were examined
by cytologic methods to determine the percent
prevalence and number of abnormal cells. Late
spring samples (YCLP, YSWP, YAGH, and YPIS,
Table 1) were diagnosed by both histology and histo-
cytology (technique described below).
Hemolymph was drawn via hypodermic syringe
into sterile, ambient (15%o), artificial seawater to
produce a 1:9 dilution of cells to seawater. One milli-
liter of this sample was placed on a 25 mm, cham-
bered, poly-L-lysine coated microscope slide and
cells were allowed to settle for 1 h (the poly-L-lysine
coating improves the adhesiveness of neoplastic cells
which in vitro are rounded and do not usually stick
to glass [Cooper 1982a]). Fluid and chambers were
Manuscript accepted May 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
851
FISHERY BULLETIN: VOL. 84, NO. 4
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852
FARLEY ET AL.: EPIZOOTIC SARCOMA IN SOFT SHELL CLAMS
removed, while slides were wet-fixed in an aldehyde
fixative (1% glutaraldehyde/4% formaldehyde)
(McDowell and Trump 1976) in half ambient sea-
water and stained with Feulgen picromethyl blue
(Farley 1969), dehydrated, and mounted with a
coverslip using a synthetic mounting medium. We
are designating the term "histocytology" to describe
this technique. The significance of this method is
that the monolayer preparations, which result from
treating living cells with histologic procedures, are
permanent. Cytologic artifacts are minimal and
cases can be accurately staged using cell counting
procedures. Since histocytologic preparations con-
tain between 100,000 and 500,000 cells in a mono-
layer, very early stages of the proliferative process
can be diagnosed. Staging is arbitrarily determined
by estimating the number and determining the ratio
of both normal and neoplastic cells (Table 2). A
similar diagnostic and staging method using cyto-
logic techniques was reported by Cooper et al.
(1982b); however, our method appears to have bet-
ter accuracy and increased sensitivity to light cases.
Diagnosis of histologic sections is reliable for stages
3-5 (Fig. 1A). As an example, comparison of late
spring samples shows that histocytology is the more
sensitive method while histology alone clearly
demonstrates a massive increase in prevalence from
zero in 1969-78 to 29.5% in 1984 (Table 1).
Monoclonal antibody was developed against neo-
plastic clam cells from Massachusetts clams by tech-
niques described elsewhere (Reinisch et al. 1983).
Periodic histocytologic diagnosis and mortality ob-
servations were made on clams held in 55 L aquaria
with 15°/oo, 10 °C artificial seawater, circulated
through floss and charcoal filtering systems.
RESULTS
Sarcomas in clams were diagnosed histologically
in 1/25 in November 1979 from Eastern Bay; 1/25
in May 1981 from West River; 1/50 in November
1981 from Little Choptank River; and 1/75 in Janu-
ary 1983 from Chester River. In December 1983,
histocytologic diagnoses of clams obtained from a
local seafood restaurant showed 8/18 with sarcomas.
An intensive survey and study of local populations
was initiated in December 1983 to evaluate the ex-
tent of this apparently new epizootic in Chesapeake
Bay soft shell clams. Table 1 presents epizootiology
of field collections while Table 2 shows comparable
information on laboratory-held clams. Field preva-
lences were found to be high in most samples from
December 1983 through April 1985. At the same
time, disease intensities which were light in Decem-
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FISHERY BULLETIN: VOL. 84, NO. 4
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Figure 1.— Cytology of clam sarcoma, 1 unit =10 ^m. (A) Histologic section: Note large, hyperchromatic nuclei, abundant mitotic
figures and metaphase with laggard chromosomes. (B-G) Histocytologic preparations: (B) Stage 5 (all cells neoplastic); rounded cells
show mitosis and large, reniform, hyperchromatic nuclei. (C) Stage 3 sarcoma; about 10% of the cells are neoplastic. Compare sizes
of normal (small) and neoplastic (large) nuclei. (D) Mitotic figure in anaphase. (E) Binucleate neoplastic cell with prominent, multiple
nucleoli (normal hemocyte, arrow). (F) Neoplastic cell with intranuclear inclusion (arrow). (G) Very large neoplastic cell with nucleus
and prominent Golgi zone.
ber progressed to advanced and terminal stages by
April in laboratory -held animals. This situation was
reflected in the field by an increase in the prevalence
of advanced cases as the season progressed. The
higher histologic prevalence in the YAGH sample
was due to four positive cases from sections of dead
animals which were not diagnosable by histocyto-
logy. This information provides additional evidence
of mortality in feral populations. Cooper et al.
(1982a) demonstrated in laboratory experiments the
lethal nature of this disease in animals with ad-
vanced cases and noted similar implications in field
monitored populations. A chronic phase with remis-
sion was reported by Cooper, but these features
were not evident in the Chesapeake Bay epizootic.
It is conceivable that some resistance has developed
in the long-term occurrence of this disease over
generations of clams in New England. Selection has
not, as yet, had a chance to develop resistant animals
in Chesapeake Bay. The mortality which began in
laboratory -held animals in April was 100% by the
end of June (Table 2). Field prevalences also dropped
to zero in June. Sarcomas reappeared in the popula-
tion in October.
Neoplastic clam cells from OXC 1 and EBC 6
(Table 2) were incubated with the murine mono-
clonal antibody IE 7 which is specifically reactive
with Massachusetts Mya neoplastic cells (Reinisch
et al. 1983). Upon fluorescence activated cell
sorter analyses, neoplastic cells from OXC 1
(Fig. 2) and EBC 6 were positive when stained with
IE7.
854
FARLEY ET AL.: EPIZOOTIC SARCOMA IN SOFT SHELL CLAMS
FLUORESCENCE INTENSITY
Figure 2.— OXC 1 cells were fixed in 0.1% neutral formaldehyde. Following three washes in sterile seawater, the cells were then in-
cubated with: (A) a 1:50 dilution of fluoresceinated (FITC) goat and antimouse IgG antibody (---), (B) a 1:100 dilution of heat-inactivated
normal mouse serum, and subsequently with a 1:50 dilution of FITC-goat antimouse IgG antibody ( ), or (C) monoclonal antibody
IE7, and subsequently with a 1:50 dilution of FITC-goat antimouse IgG antibody ( ). All the antisera were diluted in sterile sea-
water immediately prior to use. The samples were then evaluated by a Becton-Dickinson Fluorescence Activated Cell Sorter IV (Reference
to trade names does not imply endorsement by the National Marine Fisheries Service, NOAA).
DISCUSSION
Epizootiology
Laboratory and field observations complement
each other and confirm the suspicion that affected
animals die from the disease. Individual diseased
clams monitored in aquaria from early December
1983 to May 1984 had progressed from early stages
1 and 2 to advanced stages 4 and 5 with 100% mor-
tality. The high prevalences and advancing stages
seen in natural populations may signal significant,
impending mortalities. Samples collected from Swan
Point (YSWP) in July and August 1984 (Table 1)
showed 1/15 and 0/25 sarcomas, respectively. Sam-
ples from Poplar Island in July and August were
0/25 and 0/25. High sarcoma prevalences reappeared
in the fall in smaller clams at Swan Point (25%) and
Poplar Island (32%) in October. The decrease in
prevalence to zero corresponds with observations
of laboratory-held animals, suggesting that the
disease was also 100% fatal in field populations. The
experiments of Brown (1980) and others (Oprandy
et al. 1981) indicate an infectious etiology for the
disease. The nature of the new situation in Chesa-
peake Bay suggests that an infectious agent may
have been established in clams by introduction from
New England, since previous information indicated
that the disease was confined to sites north of New
Jersey (Barry and Yevich 1975; Yevich and Barszcz
1977; Brown etal. 1977, 1979; Brown 1980; Koepp
1984). Introductions of clams from New England to
855
FISHERY BULLETIN: VOL. 84, NO. 4
Maryland have been documented in the past (post-
tropical storm Agnes in 1972) (S. V. Otto unpubl.
data). Antigenic similarity between neoplastic clams
in New England and Maryland suggests that target
cells in the disease are the same in both areas. Addi-
tionally, the sudden appearance of isolated occur-
rences of the disease in widespread areas of the Bay
and the apparent tenfold increase in frequencies
since its appearance in 1978 in populations occur-
ring over most of the geographic range of soft clams
in the Bay suggest an infectious etiology rather than
point source chemical oncogen activity or pollution
(Barry and Yevich 1975; Yevich and Barszcz 1977;
Cooper et al. 1982a; Reinisch et al. 1984) as has been
implied in some New England studies.
hyperchromatic nuclei); and 5) clinical features such
as progression and malignancy.
ACKNOWLEDGMENTS
This study was supported in part by the U.S.
Department of Commerce, National Marine Fish-
eries Service (contract no. NA-82-FA-C-00048). We
thank Keith R. Cooper for the critical review of the
manuscript. We also thank the technical staffs of
the Oxford Biological Laboratory, NMFS— G. Roe,
C. Roney, D. Howard, M. Prettyman; DNR-R.
Scott; James B. Engle Scholarship at Washington
College, Chestertown, MD— E. D. Grogan; and
Tufts University— H. Sakamoto, P. Cronin.
Classification
Histologically, the clam sarcomas (Fig. 1A) con-
sist of diffusely disseminated round cells with a
large, 6-10 ^m, hyperchromatic, often lobed nucleus
containing one or more prominent nucleoli. Cyto-
plasm is sparse, mitosis is common, and nuclei are
more than twice as large as normal hemocyte nuclei.
Histocytologic preparations (Fig. 1B-G) reveal sar-
coma cells with identical characteristics and which
can be definitively recognized on the basis of their
morphology.
Other authors (Yevich and Barszcz 1977; Brown
et al. 1977; Reinisch et al. 1983) have called this
disease a "hematopoietic neoplasm" because of the
general similarity of neoplastic cells and hemocytes,
and because of its occurrence in vascular spaces.
While this is the most probable origin for these cells,
previous studies in other species have shown that
these criteria can be misleading. The neoplasm in
Macoma balthica (Christensen et al. 1974), which
was characterized by anaplastic cells inhabiting the
vascular spaces, was shown ultrastructurally to be
of epithelial origin and, therefore, diagnosable as a
carcinoma (Farley 1976b). Since no specific identi-
fying organelles have been seen in the soft clam
neoplasm (Brown et al. 1977) and since some mono-
clonal antibodies developed against neoplastic cells
do not cross react with normal hemocytes, we prefer
the more conservative term "sarcoma" which iden-
tifies the disease by behavior and cytology but does
not imply a particular cell origin. These data indicate
disease irreversibility and satisfy most of the other
criteria for sarcoma or carcinoma, namely: 1) loss
of cell specialization (anaplasia); 2) cell proliferation;
3) invasiveness (diffuse infiltration of connective
tissue and muscle); 4) clonal alteration of genetic
material (probable polyploidy evidenced by enlarged,
LITERATURE CITED
Barry, M. M., and P. P. Yevich.
1975. The ecological, chemical and histopathological evalua-
tion of an oil spill site: Part III. Histopathological studies.
Mar. Pollut. Bull. 6:171-173.
Brown, R. S.
1980. The value of the multidisciplinary approach to research
on marine pollution effects as evidenced in a three-year study
to determine the etiology and pathogenesis of neoplasia in
the soft-shell clam, Mya arenaria. Rapp. P. -v. Reun. Cons.
int. Explor. Mer 179:125-128.
Brown, R. S., R. E. Wolke, S. B. Saila, and C. W. Brown.
1977. Prevalence of neoplasia in 10 New England populations
of the soft-shell clam (Mya arenaria). Ann. N. Y. Acad. Sci.
298:522-534.
Brown, R. S., R. E. Wolke, C. W. Brown, and S. B. Saila.
1979. Hydrocarbon pollution and the prevalence of neoplasia
in New England soft-shell clams (Mya arenaria). In
Animals as monitors of environmental pollutants, p. 41-51.
National Academy of Sciences, Washington, D.C.
Christensen, D. J., C. A. Farley, and F. G. Kern.
1974. Epizootic neoplasms in the clam Macoma balthica (L.)
from Chesapeake Bay. J. Natl. Cancer Inst. 52:1739-1749.
Cooper, K. R., R. S. Brown, and P. W. Chang.
1982a. Accuracy of blood cytological screening techniques for
the diagnosis of a possible hematopoietic neoplasm in the
bivalve mollusc, Mya arenaria. J. Invertebr. Pathol. 39:
281-289.
1982b. The course and mortality of a hematopoietic neoplasm
in the soft-shell clam, Mya arenaria. J. Invertebr. Pathol.
39:149-157.
Farley, C. A.
1969. Probable neoplastic disease of the hematopoietic
system in oysters, Crassostrea virginica and Crassostrea
gigas. Natl. Cancer Inst. Monogr. 31:541-555.
1976a. Proliferative disorders in bivalve mollusks. Mar.
Fish. Rev. 38(10):30-33.
1976b. Ultrastructural observations on epizootic neoplasia
and lytic virus infection in bivalve mollusks. Prog. Exp.
Tumor Res. 20:283-294.
Harshbarger, J. C, S. V. Otto, and S. C. Chang.
1977. Proliferative disorders in Crassostrea virginica and
Mya arenaria from the Chesapeake Bay and intranuclear
virus-like inclusions in Mya arenaria with germinomas from
a Maine oil spill site. Haliotis 8:243-248.
856
FARLEY ET AL.: EPIZOOTIC SARCOMA IN SOFT SHELL CLAMS
Howard, D. W., and C. S. Smith.
1983. Histological techniques for marine bivalve mollusks.
U.S. Dep. Commer., NOAA Tech. Memo. NMFS F/NEC 25,
97 p.
Koepp, S. J.
1984. Detection of a DNA virus within an upper New York
Bay soft-shell clam population. Coastal Ocean Pollut.
Assess. News 3:26-28.
McDowell, E. M., and B. F. Trump.
1976. Histologic fixatives suitable for diagnostic light and
electron microscopy. Arch. Pathol. Lab. Med. 100:405-414.
Oprandy, J. J., P. W. Chang, A. D. Pronovost, K. R. Cooper,
R. S. Brown, and V. J. Yates.
1981. Isolation of a viral agent causing hematopoietic neo-
plasia in the soft-shell clam, Mya arenaria. J. Invertebr.
Pathol. 38:45-51.
Reinisch, C. L., A. M. Charles, and J. Troutner.
1983. Unique antigens on neoplastic cells of the soft shell clam
Mya arenaria. Dev. Comp. Immunol. 7:33-39.
Reinisch, C. L., A. M. Charles, and A. M. Stone.
1984. Epizootic neoplasia in soft shell clams collected from
New Bedford Harbor. Hazardous Waste 1:73-81.
Yevich, P. P., and C. A. Barszcz.
1977. Neoplasia in soft-shell clams (Mya arenaria) collected
from oil-impacted sites. Ann. N.Y. Acad. Sci. 298:409-
426.
857
SIZE-SPECIFIC VULNERABILITY OF
NORTHERN ANCHOVY, ENGRAULIS MORDAX, LARVAE TO
PREDATION BY FISHES
Arild Folkvord1 and John R. Hunter2
ABSTRACT
Vulnerability of larval northern anchovy (6-33 mm SL) to predation by adult northern anchovy and juvenile
chub mackerel, Scomber japonicus, was estimated by measuring the response and escape probabilities
of larvae. The proportion of larvae responding to the attacks of either predator increased with larval
length and differed little between predator species. About 20% of 6 mm larvae responded to attacks
of predators while 85-100% of 33 mm larvae responded. The proportion of larvae escaping attacks also
increased with larval length, but more larvae of all sizes escaped the attacks of adult northern anchovy
than those of juvenile chub mackerel. The rate of consumption of northern anchovy larvae by adult north-
ern anchovy was highest when the larvae were 8.5-15 mm long, indicating that greater avoidance suc-
cess of larvae in this size range relative to smaller ones may not completely compensate for their greater
visibility to predators.
The events that cause variation in year-class
strength in marine fish stocks occur during the first
year of life, but no single life stage or period has
been identified as being uniquely influential in the
establishment of year classes. Mortality rates are
size specific over this period with rates being the
highest during the egg and yolk-sac stages and
declining thereafter (Hunter 1984; Smith 1985).
Variation in the relatively low mortality rates of
older larval and juvenile stages may be more influ-
ential in year-class formation than the variation of
the high mortality rates of eggs and first feeding
larvae (Smith 1985). Thus all early life stages from
egg through juvenile must be considered and knowl-
edge of the size- or age-specific vulnerability of lar-
vae to predation and starvation is central in any
attempt at modeling the recruitment process.
Starvation is probably a direct source of larval
mortality for only a few weeks after the onset of
feeding, and most losses in the first year of life may
be attributed to predation. Predation is believed to
be the major cause of mortality during the egg and
yolk-sac stages (Hunter 1984), and incidence of
starving jack mackerel, Trachurus symmetricus,
and northern anchovy, Engraulis mordax, in the sea
indicate that significant starvation mortality is
^cripps Institution of Oceanography, University of California
at San Diego, La Jolla, CA 92093; present address: Austevoll
Aquaculture Station, 5392 Storebtf, Norway.
2Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, 8604 La Jolla Shores Drive, La
Jolla, CA 92038.
Manuscript accepted June 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
restricted to the first 1-2 wk of feeding or about
10-20% of the larval period (O'Connell 1980; Hewitt
et al. 1985; Theilacker 1986). The vulnerability of
larvae to predation has been studied over limited
size ranges; laboratory data indicate that yolk-sac
larvae seem to be vulnerable to small invertebrate
predators (copepods, amphipods, and euphausiids
[Hunter 1984]). In addition, some egg and larval
predators have been identified in field studies and
in several cases loss rates due to predation have been
estimated (Moller 1984; Frank and Leggett 1984;
Van der Veer 1985; Purcell 1985; older literature
summarized by Hunter 1984).
The objective of this paper was to determine the
size-specific vulnerability of northern anchovy lar-
vae to predation by pelagic fishes. The size-specific
vulnerability of larval Cape anchovy, E. capensis,
to cannibalism has been investigated by Brownell
(1985) and vulnerability of larval E. mordax to
predation by the aquarium fish Amphiprion percula
was studied by Webb (1981). The results of the cur-
rent study will be compared to these papers in the
discussion.
Our approach was to observe the avoidance
behavior of northern anchovy larvae in response to
predatory attacks by adult northern anchovy and
juvenile chub mackerel, Scomber japonicus. Adult
northern anchovy were selected as a predator
because it is the most abundant fish stock in the
California Current region and because it has a plank-
tivorous diet which includes fish eggs and larvae
(Baxter 1967; Hunter and Kimbrell 1980). Chub
859
FISHERY BULLETIN: VOL. 84, NO. 4
mackerel is also a major fish stock in the region and
is both planktivorous and piscivorous, with juvenile
and adult northern anchovy being a dominant item
in the diet of larger individuals (Schaefer 1980;
Hunter and Lynn, unpubl. data, Southwest Fisheries
Center, La Jolla, CA).
MATERIALS AND METHODS
Experimental Fishes
The northern anchovy larvae used in the experi-
ments were reared from the egg; 2,000-7,000 eggs,
from a laboratory brood stock (Leong 1971), were
stocked in 400 L black circular fiberglass tanks con-
taining about 150 L of filtered sea water. The culture
methods of Hunter (1976) were used to rear the lar-
vae, with extra additions of wild zooplankton when
the larvae were 10-25 mm SL. Temperature in the
rearing tanks was maintained at about 18 °C (range,
17.2°-19.2°C).
Three groups of 5 adult northern anchovy (range
of mean standard length [SL] = 8.3-8.9 cm) and a
single group of 3 juvenile chub mackerel (mean SL
= 19.1 cm) were used as predators. They were fed
mainly adult brine shrimp and occasionally north-
ern anchovy larvae. The predators were not fed for
10 h before an experiment.
Apparatus
Predators were kept in two rectangular fiberglass
tanks (0.75 m x 2.15 m x 0.83 m = 1.35 m3) with
a clear glass window on one side for observation.
Two 100 W tungsten household lamps produced
2,000-3,000 mc at the surface of each tank and a
black plastic tent enclosed the window, providing
a darkened compartment for an observer. Larvae
were released into the tank by gently submerging
a beaker at the water surface. Horizontal and ver-
tical metric scales on the tank window aided esti-
mation of predator attack distances. The tanks were
continuously supplied with ambient seawater rang-
ing from 20.5° to 23.8°C, except during an experi-
ment when the water was static.
Experimental Procedure
It was necessary to measure the feeding perfor-
mance of predators fed a standard prey because 1)
adult northern anchovy are easily frightened and
fright behavior reduces feeding motivation; 2) feed-
ing could be affected by satiation during an experi-
ment; and 3) feeding could be affected by the fish
860
learning and responding to cues associated with the
introduction of food. We used live adult brine shrimp
(Artemia sp., 6.4 mm mean total length, standard
deviation [SD] 1.2 mm, n = 25) as a standard prey.
Variation in feeding performance of the predators
could be more easily detected when Artemia were
used because unlike the larvae the Artemia did not
vary in size among experiments nor did they avoid
attack by the predators.
Northern anchovy larvae and the adult Artemia
were added to the tank in groups of three. An addi-
tion of three of either prey constituted a trial. A trial
ended after 5 min or when all prey were taken. Dur-
ing a trial we used a computer compatible event
recorder to record observations of the interactions
between predator and prey. All the experiments
using northern anchovy as predators started with
5 consecutive trials in which 3 Artemia were offered
per trial. This was done to insure that northern an-
chovy predator groups had a similar level of feeding
motivation. Preliminary experiments indicated that
it normally took a few feeding trials before adult
northern anchovy fed consistently. After the 5 ini-
tial trials, predators were offered fish larvae and
adult Artemia alternately for 4-10 trials. Adult
Artemia were always used in the last trial to deter-
mine if satiation had occurred. A less rigorous
schedule was used for the chub mackerel predators
because their feeding behavior was less variable
than that of the northern anchovy. After 3 initial
Artemia trials, the chub mackerel were given 5 lar-
val trials followed by an Artemia trial. In most cases,
a second set of 5 larval trials were also given and
these were followed by a final Artemia trial to check
if satiation had occurred.
The number of observations for each larval size
class was the total number of predator-prey inter-
actions observed among larvae in that size class.
This number exceeded the number of larvae tested
in many cases because, if a larva escaped the first
encounter with a predator, the subsequent en-
counter was also recorded as an event. The total
number of observations (predatory events) per lar-
val size class (mean SL), when northern anchovy
were the predators, was 5.9 mm, 24; 8.5 mm, 55;
11 mm, 48; 15 mm, 53; 21 mm, 82; and 33 mm, 62.
Those for the chub mackerel experiments were 6.7
mm, 19; 10 mm, 75; 16 mm, 54; 21 mm, 27; 31 mm,
47; and 50 mm, 39.
Classification of Behavior
Prey behavior was recorded only when the
predator attacked a prey. An attack was defined as
FOLKVORD and HUNTER: VULNERABILITY OF NORTHERN ANCHOVY LARVAE
a movement directed toward the prey with the
mouth open. During an attack the northern anchovy-
predator usually increased its swimming speed, but
the chub mackerel increased speed only when
attacking larvae larger than 10 mm SL.
Four measures of predator-prey interactions were
calculated: mean and maximum attack distance; fre-
quency of avoidance responses; frequency of
escapes; and predation rate (percentage of larvae
captured during the 5-min trials). The attack
distance was the distance in decimeters (dm) from
the prey to the point where the predator started the
attack. An avoidance response was a change in
speed or direction of a larva occurring before the
predator had completed the attack by closing its
mouth.
An escape was defined as a larval response in
which the predator failed to capture the larva dur-
ing a single attack. Repeated attacks were scored
as separate events. By definition, adult Artemia
could not be credited with an escape since they did
not respond to an attack. Cases where attacked
Artemia were not captured were considered
predator errors. Predator error could only be
assessed for Artemia. All interactions between
predators and larvae in which the larvae were not
captured were recorded as an escape.
Predator Performance
The feeding success and variation in feeding rates
of predator groups fed live adult Artemia were
analyzed to estimate predator error and to deter-
mine if differences existed in feeding performance
among predator groups, or among or within ex-
periments. An experiment was 2-5 larval trials con-
ducted on a single size class of larvae on one day
using a single predator group.
Predator errors were obvious when Artemia were
the prey because Artemia did not avoid the attack.
In such cases the trajectory of the attack was inac-
curate and the predator simply missed the prey.
Such errors occurred in 3.4% of the attacks on
Artemia; this estimate is similar to error rates esti-
mated for other predators (Curio 1976). We could
not measure the predator error when larvae were
the prey because we attributed any failure to cap-
ture a larva to larval avoidance success. Presumably
our estimates of larval escape probabilities include
an unknown number of cases where failure to cap-
ture a larva was the direct result of inaccuracies in
the predator's attack rather than being the result
of larval avoidance.
Considering all northern anchovy predator
groups, predator error in capturing Artemia was
higher in the first 5 trials than in the subsequent
trials of the experiments where Artemia trials were
alternated with larval trials (Fig. 1A). Predator er-
ror averaged 3.4% for all Artemia trials, whereas
it was 2.1% during the period of alternating larval
and Artemia trials. Similarly, adult northern an-
chovy took more time to capture all the Artemia in
the first trial than in subsequent ones (Fig. IB). No
decline in feeding performance on Artemia existed
at the end of the experiments, indicating that satia-
tion did not constitute a bias in the experiments. The
initial decline in the time required for northern an-
chovy predators to capture Artemia may have been
caused by an increase in feeding motivation, learn-
ing, or a decrease in fright behavior. As the decline
occurred during only the initial 5 Artemia trials, the
larval data were probably unaffected.
Minor differences in feeding performance also ex-
isted among predator groups. In two experiments
northern anchovy predatory groups fed markedly
less on both Artemia and larvae (30% fewer prey
taken in 5 min; £-test, P < 0.05). The effect of omit-
ting these two experiments is indicated in the
results. Overall, comparisons of feeding perfor-
mance among groups, within trials, and among
experiments indicated that variation in predator per-
formance as measured by predation rates on
Artemia was not significantly biased (additional
details are given by Folkvord 1985) (see also Figure
1).
RESULTS
Probability of a Response to Predators
The most striking feature of the vulnerability of
the youngest larval stages of northern anchovy to
predators was the low frequency of escape attempts.
Only 16% of the 6 mm larvae responded to the at-
tacks of northern anchovy predators (Fig. 2B) and
only 26% of 6.7 mm larvae responded to chub
mackerel predators (Fig. 3B). The probability of
smaller larvae (SL <20 mm) responding to either
chub mackerel or northern anchovy predators was
about the same (Fig. 4), although size, feeding
behavior, and body form of these two fishes were
distinctly different. The tendency to respond to at-
tacking predators steadily increased with larval size
until by the time northern anchovy larvae were 30
mm all attempted to avoid attacking northern
anchovy and over 80% responded to chub mackerel
attacks.
861
FISHERY BULLETIN: VOL. 84, NO. 4
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Artemia AND LARVAL TRIALS
0 12345678 9 10 1112 13 14 15
TRIAL NUMBER
Figure 1.— Variation in feeding performance of northern anchovy predators fed live
Artemia as a function of trial number (equivalent to elapsed time of experiment);
shaded area indicates trials in which northern anchovy were fed only Artemia; un-
shaded areas, Artemia trials alternated with larval trials. A, percent predator error
in capturing adult Artemia (percentage of attacks in which a northern anchovy missed
the prey); dashed line indicates mean. B, mean time required for predator group
to capture 3 adult Artemia; bars are 2 x SE of the mean. (N = 21.)
Success of Avoidance Movements
Larval vulnerability depended not only on the
responsiveness but also on the success of avoidance
movements. The proportion of larvae escaping
northern anchovy predators increased from 8% for
6 mm larvae to 92% for 33 mm larvae with an esti-
mated 50% of the 17 mm larvae escaping. The
percentage of larvae escaping the attacks of chub
mackerel was lower than for adult northern an-
chovy, but the curves given in Figures 2 and 3 had
a similar form. Weibull curves were fit to the data
to provide trend lines (equations and parameters
given in Figure legends). The fraction of larvae that
escaped increased from 6% of 6.7 mm larvae to an
estimated 50% of the 30 mm larvae. Of the 50 mm
juvenile northern anchovy used as prey only 64%
escaped the attacks of the chub mackerel.
The ability to successfully avoid predator attacks
was strongly affected by species-specific differences
in predator behavior since the fraction of larvae
escaping the attacks of northern anchovy increased
much more rapidly with larval length than did the
fraction escaping the attacks of chub mackerel. In
contrast, the fraction of smaller larvae (SL <20 mm)
responding to the attacks of these two predators
was similar (Fig. 4). This indicates that probability
of a larva responding to an attack is less affected
862
FOLKVORD and HUNTER: VULNERABILITY OF NORTHERN ANCHOVY LARVAE
PREDATOR - Engraulis mordax
Escaping attack
Taken in 5 min.
i i i i
B
/ Responding to attack
i i i i i i i
2 6 10 14 18 22 26 30 34 38 42 46 50
LARVAL STANDARD LENGTH (mm)
Figure 2.— Vulnerability of northern anchovy larvae to adult northern anchovy
predators as a function of larval length. A, Percentage of northern anchovy
larvae escaping attack; bars are 2 x SE; line is Weibull curve fit to six points
using Marquardt's least squares method (Pielou 1981); equation is N = K(\ -
exp (1 - (Lib) -A)) where K = 0.93, 6 = 17.85, A = 2.85, N is the percentage
of larvae and L = larval length; and predation rate of the northern anchovy
predators (percentage eaten in 5 min) where dashed line is data when ex-
periments with biased predator feeding motivation are omitted. B, Percentage
of northern anchovy larvae that responded to the attack of an adult northern
anchovy; bars are 2 x SE; and Weibull parameters for curve are K = 1.00,
b = 13.58, and A = 1.94.
by differences in predator behavior than is its suc-
cess in avoiding the attack.
The success of avoidance movements can be
separated from larval responsiveness by calculating
the avoidance success of responding larvae (numbers
escaping/numbers responding). Webb (1981) found
no change in this fraction over the larval size range
he examined (3-12 mm SL), indicating that changes
in responsiveness alone were responsible for the
decline in the vulnerability of northern anchovy lar-
vae to Amphiprion with increasing larval length. In
the present study, no significant trend existed in the
success of avoidance movements over the size range
of larvae studied by Webb (1981) but success of
avoidance movements greatly increased in larger
larvae (Fig. 5). The figure also indicates that north-
ern anchovy larvae were much more successful in
avoiding Amphiprion than in avoiding adult north-
ern anchovy and that the larvae had the least suc-
cess in avoiding chub mackerel.
863
FISHERY BULLETIN: VOL. 84, NO. 4
PREDATOR - Scomber Japonicus
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2 6 10 14 18 22 26 30 34 38 42 46 50
LARVAL STANDARD LENGTH (mm)
Figure 3.— Vulnerability of northern anchovy larvae and juveniles to juvenile chub
mackerel predators as a function of anchovy length. A, percentage of northern
anchovy larvae escaping attack; bars are 2 x SE; line is Weibull curve fit to six
points using Marquardt's least squares method (Pielou 1981); equation is N = K(\
- exp (1 - (Lib) - A)) where K = 0.66, b = 27.41, N = percentage of larvae, L
= larval length, and A = 2.12; and predation rate of chub mackerel predators
(percentage eaten in 5 min) where dashed line is data when experiments with biased
predator feeding motivation are omitted. B, percentage of northern anchovy lar-
vae that responded to the attack of a chub mackerel, bars are 2 x SE; and Weibull
parameters for curve are K = 0.93, 6 = 12.61, and A = 1.24.
Predation Rates
The predation rate of northern anchovy (propor-
tion of larvae consumed by northern anchovy
predators in 5 min) reached a maximum somewhere
between larval lengths of 8.5 and 15 mm when all
data were used, but it occurred between larval
lengths of 8.5 and 11 mm when we deleted the ex-
periment where northern anchovy predator perfor-
mance was lower than average (dashed line in
Figure 2A). Statistical comparisons of the fraction
of larvae consumed in the various size classes in-
dicated that 6.8 mm larvae were taken less often
than larvae in 8.5, 11, and 15 mm size classes despite
the fact that these larvae had a low escape ability
(P < 0.05; normal approximation to the binomial
mean; n = 35, 48, 40, and 60, for 5.9, 8.5, 11, and
15 mm size classes). Owing to their small size and
864
FOLKVORD and HUNTER: VULNERABILITY OF NORTHERN ANCHOVY LARVAE
St
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-Gr-3 -L«7/aDon*icus
Scomber »aP
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6 10 14 18
22 26
30
34 38
42
46 50
STANDARD LENGTH (mm)
Figure 4.— Percentage of northern anchovy larvae that responded to attacks by adult northern anchovy (lines for the
three different predator groups shown separately), chub mackerel and the aquarium fish Amphiprion percula (from
Webb 1981).
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LARVAL STANDARD LENGTH (mm)
42
46 50
Figure 5.— The percentage of responding northern anchovy larvae in various length classes that escaped the predator.
Species names identify the predator species.
lack of pigmentation, 6 mm larvae may have been
less visible to the predators than larger larvae and
consequently were detected less frequently. The
decline in predation rates in larvae longer than 15
mm was the result of their greater escape ability.
The number of larvae consumed in 5 min was an
insensitive measure of predation rates of chub
mackerel, because they usually ate all larvae in the
tank within 5 min regardless of their size. Only in
the two smallest larval size groups (6-10 mm SL)
were some larvae left after a 5-min elapsed time;
the deletion of one experiment because of low chub
mackerel predator performance changed the preda-
tion rate on 10 mm larvae from 87 to 95% (dashed
line in Figure 3A). These adjusted data indicate that
the feeding rate of chub mackerel was lowest when
865
FISHERY BULLETIN: VOL. 84, NO. 4
the smallest larval size group (6.7 mm) were the
prey.
Predator Behavior
Sighting distances, persistence of the attack, at-
tack speed, and other characteristics of predator
behavior were not well documented in our experi-
ments because our focus was on the larvae. Such
information could be quite useful if one were to
develop a predation model for northern anchovy lar-
vae, using northern anchovy or chub mackerel
predators. We provide some general observations
on the behavior of the predators.
Chub mackerel attacked 6.7 mm larvae from a
shorter distance than larger larvae (£-test, P = 0.05),
but no statistically significant trend was evident
when northern anchovy were predators. Mean at-
tack distances were a poor measure of sighting
range as they included repeated, short-range attacks
on the larger larvae. We observed both predator
species swimming within 2-3 dm of the smallest lar-
vae without attacking them, whereas larger larvae
were always attacked from this distance indicating
that sighting distances may be shorter for small
larvae.
Adult northern anchovy usually attacked a larva
only once during a feeding sequence, and if the larva
escaped, it was rarely attacked again or pursued.
On the other hand, if the chub mackerel did not cap-
ture the larva on the first attack, it usually turned
and attacked again. Chub mackerel usually chased
an escaping larva until it was captured. The attack
speeds of adult northern anchovy, although not
measured, seemed to be similar over a wide range
of larval prey sizes, whereas the attack speeds of
chub mackerel clearly were faster when attacking
larvae greater than about 10 mm SL than when at-
tacking smaller larvae.
DISCUSSION
Factors Affecting Larval Vulnerability
A low level of responsiveness seems to be the
dominant feature of the vulnerability of northern
anchovy larvae to fish predators over the smallest
larval size classes we tested (6-10 mm SL). Presum-
ably northern anchovy larvae <6 mm would respond
even less frequently, as Webb (1981) found that only
9% of 2.9 mm northern anchovy larvae responded
to the aquarium fish Amphiprion percula, whereas
about 30% of 6 mm larvae did so. During this period
vulnerability of northern anchovy larvae to fish
predators seems to be primarily a function of visual
detection by the predator, because when the larvae
are detected they have a low probability of escap-
ing. Our data on predation rates and maximum at-
tack distances indicate that predation in the sea on
the small, young larval stages might be lower than
expected because of the short range at which such
larvae may be detected. Thus, factors that affect the
distance at which larvae are detected by predators,
such as larval size, visual contrast, and water clar-
ity (Vinyard and O'Brien 1976), may be the most im-
portant variables during the first 3 wk of life. As
larvae grow they more often respond to the attacks
of predators and escape them more frequently.
Maturation of visual and lateral line systems (O'Con-
nell 1981) may be the principal cause of this general
increase in responsiveness with larval length. Al-
though older larvae are more responsive, they are
also more readily detected by predators because
they are larger and have more pigmentation. Im-
proved avoidance behavior may not completely com-
pensate for the greater visibility of larvae in the 8-12
mm range, as our data on predation rates by north-
ern anchovy indicated that the rates of consump-
tion were highest for larvae in this range.
Larvae longer than 20 mm responded more fre-
quently to northern anchovy than to chub mackerel
predators, possibly because chub mackerel attacked
such large larvae at much higher speeds. At higher
attack speeds, less time is available for the larvae
to respond; consequently, predators with the most
rapid attack speeds evoke the lowest proportion of
prey responses (Webb 1982). Thus one might expect
a larva to respond to small fish predators more fre-
quently than to larger ones, since attack speed
would be expected to increase with predator size.
This may explain why northern anchovy larvae
(2.9-12 mm SL) responded more frequently to the
small Amphiprion (44 mm) (Webb 1981) than they
did to either northern anchovy or chub mackerel
predators (Fig. 4). The pectoral swimming of
Amphiprion might also provide more cues of an im-
pending attack than did the swimming movements
of either northern anchovy or chub mackerel.
In addition to size-specific avoidance capabilities
and visibility, many other larval characteristics
affect their vulnerability to predators. We briefly
consider here three of these: effects of starvation,
effects of the onset of schooling, and effects of varia-
tions in larval growth rates. Clupeoid larvae undergo
degradation of muscle and other tissues during star-
vation, and a reduced predator avoidance behavior
might be anticipated (Ehrlich 1974; O'Connell 1980).
In a preliminary experiment Folkvord (1985)
866
FOLKVORD and HUNTER: VULNERABILITY OF NORTHERN ANCHOVY LARVAE
reported that only 50% of starved, 33 mm northern
anchovy larvae responded to the attacks of adult
northern anchovy as compared with 100% for fed
larvae. No starved 10 mm larvae escaped attack
whereas 15-20% of the fed 10 mm larvae did so. The
numbers of observations were insufficient for a
statistical comparison, but recent work by Booman
(unpubl. data, Southwest Fisheries Center, La Jolla,
CA) indicates starvation can have a statistically
significant effect on responsiveness of 10 mm north-
ern anchovy larvae to adult northern anchovy
predators.
The effect of the onset of larval schooling was not
considered in these experiments; however, escape
and response probabilities of individual larvae may
not be altered greatly by the onset of schooling. The
work of Major (1978) indicates that the most impor-
tant effect of schooling may be to reduce the rate
of attack by predators. He also found that the ma-
jority of Hawaiian anchovy captured by predators
were isolated individuals that had moved away from
the school, and predator success on schooled prey
was similar to that on isolated prey. The onset of
schooling in larval northern anchovy occurs between
11 and 15 mm SL, but the time spent in organized,
cohesive schools increases throughout the northern
anchovy's larval and juvenile periods (Hunter and
Coyne 1982). Thus attack rates of predators might
be expected to decline throughout later larval and
juvenile life as the northern anchovy spends more
time in cohesive schools. The onset of schooling oc-
curs over the size range in which we observed the
maximum predation rate (numbers consumed in 5
min) on individual northern anchovy larvae by north-
ern anchovy predators. Thus predation pressure
may be an important evolutionary factor in the tim-
ing of the onset of schooling during the larval stage.
The interaction between larval growth rate and
size-specific vulnerability to predation may be an im-
portant source of interannual variation in larval
mortality (Shepherd and Cushing 1980; Smith 1985).
A simple calculation illustrates this point using the
size-specific vulnerability of northern anchovy lar-
vae (10-20 mm SL) to adult northern anchovy
predators. We assumed larval escape ability to be
an inverse measure of predator vulnerability and
normalized it to the average mortality rate over this
size interval (Table 1). Thus in our calculation, the
rate larval mortality decreased with increasing lar-
val size was inversely proportional to the rate escape
ability increased with size (larval escape ability in-
creased linearly with larval length over the 10-20
mm length range). Our calculation indicated that a
50% increase in growth rate from the average rate
of growth in the sea resulted in a 58% increase in
survival in 30 d compared with average conditions.
Decreasing the growth rate by 50% gave a 37%
decrease in survival over the same interval. A longer
period of reduced or enhanced growth rates will, of
course, give a larger deviation from average survival
values.
Table 1 .—Calculation of the effect of growth rate on survival of
10-20 mm northern anchovy larvae when mortality is inversely pro-
portional to length specific escape probabilities.
Terms
Parameter values
z =
mortality rate
Z = 0.05 at 16 mma
s =
larval length (mm)
10 mm < S< 20 mm
G =
growth rate
G = 0.325 mm/db
T =
time
T = 30 d
N =
relative numbers of larvae
A/(0) = 1
Initial equations
Z = 0.15 - (0.00625 x S) a
S = 10 + (G x 7")
dNIdt = - (Z x N)
Final equations after substitution and integration
N = 0.0724 x exp (2.808 x G)
Estimates of survival after 30 days
Growing
conditions
Growth rate
(mm/d)
Relative numbers
of larvae
Relative
survival
(%)
Average
50% increase
50% decrease
0.325
0.488
0.162
0.1803
0.2850
0.1141
+ 58
-37
aMortality function generated from larval anchovy escape data with adult
northern anchovy as predators. Values are normalized to Z 0.05 at 16 mm
(Smith 1985).
"From Smith (1985), 0.325 ± 50% also used in calculation.
Effect of Predator Size
We examined the existing literature on predators
of larval northern anchovies to determine how the
ability to escape a predator varied among different
predator species. Regardless of the predator species,
larval escape ability always increases with larval
size, but the rates vary greatly with predator size.
In general the smaller the predator, the faster lar-
val escape abilities improve with increasing larval
length (Fig. 6). The results of our work on E. mor-
dax were similar to those of Brownell (1985) on E.
capensis. However, capture success of the 85 mm
E. mordax predators used in our study was about
20% higher than the 34 mm E. capensis predators
used by Brownell.
The extent of the predator field for a given size
and species of predator can be defined as the larval
size range in which larval escape success is <100%.
For adult northern anchovy predators (85 mm and
867
FISHERY BULLETIN: VOL. 84, NO. 4
100 -
juv. Euphausia
(6- 10mm)
Engraulis
capensis
(15mm)
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Scomber japonicus
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60
70
80
90
STANDARD LENGTH (mm)
Figure 6.— Percentage of larval and juvenile anchovies escaping attacks of various predators as a function of length.
Data for Engraulis capensis feeding on larval E. capensis are from Brownell (1984); juvenile Euphausia fed E. mordax
from Theilacker and Lasker (1974); Amphiprion percula fed E. mordax from Webb (1981); and others are from this study.
Numbers indicate length (mm) of the various predators.
larger), the field extends from the egg (Hunter and
Kimbrell 1980) to about 40 mm. The field for juvenile
chub mackerel is much wider than that for northern
anchovy extending from northern anchovy eggs to
adults (120 mm), whereas the predation field for
Euphausia is restricted to the yolk-sac period
(Theilacker and Lasker 1974). The limited data
available (Table 2) provide a crude index for the up-
per limit of the predator field for northern anchovy
larvae. When the larval length exceeds about 50%
of the predator length little or no predation occurs.
CONCLUSIONS
Much of the past research on recruitment has
focused on early larval stages where mortality rates
are the highest (May 1974). Our work supports a
growing contention that later larval stages and early
juvenile stages may be as important in determining
year-class strength (Smith 1985) and that such ef-
fects might be mediated through an interaction
between larval growth and size-specific vulnerability
to predators. Our results and those of others indicate
that the ability of northern anchovy larvae to escape
pelagic predators increases throughout the larval
stage. On the other hand, the susceptibility of lar-
vae to predation may not decrease strictly accord-
ing to size because large larvae may be more easily
Table 2.— Upper limit of some predator fields for larval anchovies,
Engraulis mordax and E. capensis.
Upper limit of predator
Predator
field
Predator
length
Larval
length
Larval length
Species
(mm)
(mm)
Predator length
Euphausia juveniles
8
4.5
0.6
(Theilacker and Lasker
1974)
Engraulis capensis
15
8.2
0.6
(Brownell 1984)
Engraulis capensis
34
20
0.6
(Brownell 1984)
Amphiprion percula
44
18
0.4
(Webb 1981)
Engraulis mordax
85
2~40
0.5
(this study)
Scomber japonicus
190
2~120
0.6
(this study)
'Upper limit = larval size at which all larvae escape predator.
2Extrapolated values.
detected by visual feeding planktivorous fishes than
smaller ones.
ACKNOWLEDGMENTS
We wish to thank Roderick Leong for providing
the northern anchovy eggs on demand, Carol Kim-
brell for editorial assistance, and Clelia Booman and
868
FOLKVORD and HUNTER: VULNERABILITY OF NORTHERN ANCHOVY LARVAE
Paul Smith for reviewing the manuscript and offer-
ing helpful suggestions.
LITERATURE CITED
Baxter, J. L.
1967. Summary of biological information on the northern an-
chovy Engraulis mordax Girard. CalCOFI Rep. 11:110-
116.
Brownell, C. L.
1985. Laboratory analysis of cannibalism by larvae of the
Cape anchovy Engraulis capensis. Trans. Am. Fish. Soc.
114:512-518.
Curio, E.
1976. The ethology of predation. Springer- Verlag, N.Y., 249
P-
Ehrlich, K. F.
1974. Chemical changes during growth and starvation of
herring larvae. In J. H. S. Blaxter (editor), The early life
history of fish, p. 310-323. Springer- Verlag, N.Y.
Frank, K. T., and W. C. Leggett.
1984. Selective exploitation of capelin (Mallotus villosus) eggs
by winter flounder (Pseudopleuronectes americanus): capelin
egg mortality rates, and contribution of egg energy to the
annual growth of flounder. Can. J. Fish. Aquat. Sci.
41:1294-1302.
FOLKVORD, A.
1985. Size specific vulnerability of northern anchovy
Engraulis mordax larvae to predation by fishes. MS Thesis,
University of California at San Diego, 96 p.
Hewitt, R. P., G. H. Theilacker, and N. C. H. Lo.
1985. Causes of mortality in young jack mackerel. Mar.
Ecol. Ser. 26:1-10.
Hunter, J. R.
1976. Culture and growth of northern anchovy, Engraulis
mordax, larvae. Fish. Bull., U.S. 74:81-88.
1984. Inferences regarding predation on the early life stages
of cod and other fishes. F10devigen rapportser., 1. ISSN
0333-2594 The propagation of cod Gadus morhua L, p.
533-562.
Hunter, J. R., and K. M. Coyne.
1982. The onset of schooling in northern anchovy larvae,
Engraulis mordax. CalCOFI Rep. 23:246-251.
Hunter, J. R., and C. A. Kimbrell.
1980. Egg cannibalism in the northern anchovy, Engraulis
mordax. Fish. Bull., U.S. 78:811-816.
Leong, R.
1971. Induced spawning of the northern anchovy, Engraulis
mordax Girard. Fish. Bull., U.S. 69:357-360.
Major, P. F.
1978. Predator-prey interactions in two schooling fishes,
Caranx ignobilis and Stolephorus purpureus. Anim. Behav.
26:760-777.
May, R. C.
1974. Larval mortality in marine fishes and the critical period
concept. In J. H. S. Blaxter (editor), The early life history
of fish, p. 3-19. Springer- Verlag, N.Y.
Moller, H.
1984. The reduction of a larval herring population by jellyfish
predator. Science 224:621-622.
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. 78:475-484.
1981. Development of organ systems in the northern an-
chovy, Engraulis mordax, and other teleosts. Am. Zool.
21:429-446.
Pielou, E. C.
1981. The usefulness of ecological models: a stock-taking. Q.
Rev. Biol. 56:17-31.
Purcell, J. E.
1985. Predation on fish eggs and larvae by pelagic cnidarians
and ctenophores. Bull. Mar. Sci. 37:739-755.
Schaefer, K. M.
1980. Synopsis of data on the chub mackerel, Scomber
japonicus, 1782, in the Pacific Ocean. In W. H. Bayliff
(editor), Synopses of biological data on eight species of scom-
brids. Inter-Am. Trop. Tuna Comm., Spec. Rep. 2, p.
395-445.
Shepherd, J., and D. H. Cushing.
1980. A mechanism for density dependent survival of larval
fish as the basis of stock recruitment relationship. J. Cons,
int. Mer 39:160-167.
Smith, P. E.
1985. Year-class strength and survival of 0-group clupeoids.
Can. J. Fish. Aquat. Sci. 42 (Suppl. l):69-82.
Theilacker, G. H.
1986. Starvation-induced mortality of young sea-caught jack
mackerel, Trachurus symmetricus, determined with histo-
logical and morphological methods. Fish. Bull., U.S. 84:
1-15.
Theilacker, G. H., and R. Lasker.
1974. Laboratory studies of predation by euphausiid shrimps
on fish larvae. In J. H. S. Blaxter (editor), The early life
history of fish, p. 287-299. Springer Verlag, N.Y.
Van Der Veer, H. W.
1985. Impact of coelenterate predation on larval plaice
Pleuronectes platessa and flounder Platichthys flesus in
the western Wadden Sea. Mar. Ecol. Prog. Ser. 25:229-
238.
Vinyand, G. L., and W. J. O'Brian.
1976. Effects of light and turbidity on the reactive distance
of bluegill (Lepomis macrochirus). J. Fish. Res. Board Can.
33:2845-2849.
Webb, P. W.
1981. Responses of northern anchovy, Engraulis mordax, lar-
vae to predation by a biting planktivore, Amphiprion per-
cula. Fish. Bull., U.S. 79:727-735.
1982. Avoidance responses of fathead minnow to strikes
by four teleost predators. J. Comp. Physiol. 147:371-
378.
869
OBSERVATIONS ON THE REPRODUCTIVE BIOLOGY OF THE
COWNOSE RAY, RHINOPTERA BONASUS, IN CHESAPEAKE BAY12
Joseph W. Smith and John V. Merriner3
ABSTRACT
Cownose rays, Rhinopterabonasus, are abundant in Chesapeake Bay during summer. We made obser-
vations on the reproductive biology of specimens collected primarily from commercial pound nets and
haul seines from May through October 1976-78. Clasper development suggested that males began to
mature at disc widths (DW) of 75-85 cm. Males judged as mature averaged about 90 cm DW. Macroscopic
inspection of the oviducts suggested that females began to mature at 85-92 cm DW. Females judged
as mature averaged 96 cm DW. Only the left reproductive tract in female cownose rays appeared func-
tional and only one embryo per gravid female was observed. A total of 67 embryos ranging 18-440 mm
DW were collected and the sex ratio of the embryos was 1:1. Gravid females carried three-quarter term
embryos in May and parturition occurred in late June and July. Full-term embryos averaged about 40
cm DW. Gestation of another group of embryos began by August. Growth of these embryos was rapid
and they were relatively large when cownose rays left the Chesapeake Bay in October. Cownose rays
exhibited aplacental viviparity. Yolk reserves supplied the initial energy demands of the embryos (up
to about 20 cm DW), but histotrophic secretions of uterine villi provided nutrition for the young through
the remainder of gestation.
The cownose ray, Rhinoptera bonasus, a large
myliobatoid ray, which attains a maximum weight
of 23 kg, is abundant in Chesapeake Bay during
summer (Schwartz 1965; Musick 1972) where it
preys heavily on commercially important shellfish
(Merriner and Smith 1979). Because of the severe
damage to shellfish beds and the paucity of infor-
mation on the biology of the cownose ray, the
Virginia Institute of Marine Science began a study
on the life history of the cownose ray in 1976. Prior
to our work, information on the cownose ray's
reproductive biology was primarily limited to obser-
vations of single gravid females, usually included in
more general literature (Gudger 1910; Bigelow and
Schroeder 1953; Joseph 1961; Hoese 1962; Bearden
1965; Orth 1975), and size at maturity was unknown
(Bigelow and Schroeder 1953). Schwartz's (1967)
brief abstract represented the most complete state-
ment on the species' reproductive cycle. Here, we
report on the reproductive biology of the cownose
ray, specifically on 1) the estimated size at matur-
1 Based on part of a thesis submitted by the senior author in par-
tial fulfillment of the degree of Masters of Arts at the College of
William and Mary, Williamsburg, VA 23185.
Contribution No. 1305 from the Virginia Institute of Marine
Science and the College of William and Mary School of Marine
Science, Gloucester Point, VA 23062.
3The College of William and Mary, School of Marine Science,
Gloucester Point, VA 23062; present address: Southeast Fisheries
Center Beaufort Laboratory, National Marine Fisheries Service,
NOAA, Beaufort, NC 28516-9722.
ity for both sexes, 2) the definition of the gestation
period, and 3) the description of the embryonic
development.
MATERIALS AND METHODS
Most cownose rays were taken from pound nets
in the lower Chesapeake Bay during three summers,
1976-78, but some rays came from haul seines used
in spring along the Virginia-North Carolina coast,
and from gill nets and rod and reel catches. Disc
width (DW = distance between tips of the pectoral
fins) was measured in mm on a measuring board.
References to specimen size (including embryos)
hereafter are disc width measurements.
We judged male cownose rays sexually mature
if 1) the clasper rhipidion was fully developed and
easily spread and 2) clasper cartilages were well
calcified (rigid). We measured clasper length as the
distance from the junction of the clasper and pelvic
fin to the distal end of the clasper. Criteria modi-
fied from Smith (1975) were used to determine the
following stages of sexual maturity for females:
1) immature - ovaries thin and flaccid; uterus thin
and elongate, lining appears rugous.
2) maturing - ovary slightly developed, yellowish
ova visible, ova <1 cm diameter; uterus somewhat
dilated, trophonemata (uterine villi) small, general-
ly <0.5 cm long.
Manuscript accepted May 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
871
FISHERY BULLETIN: VOL. 84, NO. 4
3) mature - ovary with large yellowish ova >1 cm
diameter; uterus well-developed and rich in tropho-
nemata, generally >1 cm long.
Uteri and oviducts were opened and inspected for
ova or embryos. Embryos were weighed and mea-
sured for disc width (mm). Yolk-sac volume (mL) was
measured by volumetric displacement in a graduated
cylinder.
RESULTS AND DISCUSSION
Like many other elasmobranch populations which
occur along the east coast of the United States, cow-
nose rays are highly migratory and exhibit a north-
ward coastal migration in spring and a southward
movement in fall (Schwartz 1965; Smith 1980). Our
earliest spring collection of adult rays occurred dur-
ing 2-5 May 1977 on the North Carolina Outer
Banks. Our latest fall collection of adult males was
on 7 September 1978 in the lower York River, while
the latest fall collection of adult females occurred
on 12 October 1977 near Cape Henry, VA, at the
mouth of the Chesapeake Bay. Adult rays were
absent from pound net catches in the lower bay after
mid-October; furthermore, they were unavailable to
us until the following spring when they migrated
back into Chesapeake Bay.
Size at Maturity
At the onset of sexual maturity, terminal cartilage
elements develop distally on the claspers of male
elasmobranchs (Bigelow and Schroeder 1953), and
the allometric growth of these appendages has been
used to determine the attainment of sexual matur-
ity in various elasmobranchs (e.g., Clark and Von
Schmidt 1965; Struhsaker 1969; Gilbert and Heath
1972). In male cownose rays the ratio of clasper
length to disc width increases slightly at 75-85 cm
DW suggesting the onset of sexual maturity (Fig.
1). Males <75 cm (n = 68) appear immature; their
testes are thin, white and ribbonlike and their
claspers are narrow and flexible. Males ranging
80-98 cm (x = 89.8 cm; n = 115) appear mature;
their testes are pinkish white in color and greatly
swollen, and their claspers are rigid and well-cal-
cified. Based on clasper length to disc width ratio
and cursory observations of the testes, we estimated
that male cownose rays begin sexual maturation at
about 80 cm and most are probably mature at disc
widths >84 cm.
Considerable discrepancies exist in the literature
concerning size of female cownose rays at sexual
maturity. Gudger (1910) claimed a female about 60
cm wide gave birth to a pair of young. Bearden
(1965) reported four premature young from a female
measuring 712 mm (disc width?) taken in South
Carolina. Joseph (1961) and Orth (1975) collected
gravid females in Chesapeake Bay of 89 and 90 cm,
respectively. We classified females <84 cm (n = 86)
as immature (immature ovaries are thin and flac-
cid, and immature uteri are thin and elongate).
Females that we judged as mature ranged 84.5-100
cm (x = 96 cm; n = 117). Mature ovaries possess
yellowish ova >1 cm in diameter; the left uterus of
mature females is well-developed and rich in tropho-
nemata (uterine villi), which are generally >1 cm
long, red in color, and spatulate distally. We clas-
sified eight specimens (range: 84-92 cm) as matur-
ing females. Although ova <1 cm in diameter are
visible in the ovary, the left uterus is not well-
developed and the trophonemata are generally <0.5
cm long. The smallest gravid female measured 87
cm. Based on these observations we estimated
that female cownose rays begin sexual maturation
at 85-90 cm and are mature at disc widths >90
cm.
Only the left reproductive tract appears functional
in female cownose rays. There is no macroscopic
evidence of follicular development in the right ovary.
The right uterus in mature specimens shows some
distension (ca. 3 cm wide), but does not exceed the
breadth of the left uterus. Embryos and ova occur
only in the left uterus, although we found an empty
shell capsule in the right uterus of several gravid
females. Nonfunctional right reproductive tracts
have been reported in the roughtail stingray, Dasya-
tis centroura, (Struhsaker 1969) and the bluntnose
stingray, D. sayi (Gudger 1912; Hamilton and Smith
1941; Hess 1959).
Reproductive Cycle
Numerous literature accounts reported on the cap-
ture of singular gravid cownose rays (Smith 1907;
Gudger 1910; Bigelow and Schroeder 1953; Joesph
1961; Hoese 1962; Bearden 1965; Orth 1975) and
these provided fragmentary information on the ray's
gestation cycle. Schwartz's (1967) abstract defined
June through October as the breeding cycle and
closely parallels our results, although we disagreed
on size at parturition. We collected 67 embryos
(range: 18-440 mm; sex undetermined for 3 speci-
mens) from the lower Chesapeake Bay and vicinity.
Data for 19 embryos (all specimens sexed, length
undetermined for 8 specimens) taken in April 1978
near Cape Lookout, NC, were provided to us by W.
872
SMITH and MERRINER: REPRODUCTIVE BIOLOGY OF COWNOSE RAY
S. Otwell4 (Fig. 2). Only one embryo per gravid
4W. S. Otwell, formerly of North Carolina State University Food
Science Laboratory, Morehead City, NC; presently at University
of Florida, Food Science Department, Gainesville, FL 32611, pers.
commun. April and May 1978.
female was observed. The overall sex ratio of em-
bryos (40o":439) did not differ significantly from 1:1.
Gravid female rays migrate into Chesapeake Bay
in spring with well-developed embryos that we
designated as approximately three-quarter term.
44 -i
Figure 1.— Relationship of clasper length
(mm) to disc width (cm) for 188 male Rhi-
noptera bonasus.
12 -
8 -
4
0
40 -
x = 2 Values
n = 188
38 -
32-
28 -
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24 -
20 -
or
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• • ••
• x»
XXX AM •
••• X«5t •• •
•• ••«XX XX X
• XX X «H«I. •
i ' i ■ i ■ i ' r
40 50 60 70 80
DISC WIDTH (cm)
90
100
450
400
350
£300
>-
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m
u.
o
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O
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250
200
150
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• One Value
+ Two Volues
SEPT ' OCT
"jAN ' FEB ' MAR
APR ' MAY ' JUNE ' JULY
AUG
NOV
DEC
Figure 2.— Relationship of disc width (mm) to date of capture for Rhinoptera bonasus embryos collected 1976 through
1978.
873
FISHERY BULLETIN: VOL. 84, NO. 4
Embryos collected in early May on the Outer Banks
and in the lower York River average 259 mm (range:
221-276 mm; n = 7), and those collected from Cape
Lookout, NC, in mid- April (Otwell fn. 4) average 264
mm (range: 222-281 mm; n = 11) (Fig. 2). By late
June and early July the embryos are full term (x
= 413 mm; n = 4). Parturition occurs at this time
and the first free-swimming young appear in pound
net catches. Embryo weight gain in spring is note-
worthy; three-quarter term embryos in April and
May average 310 g (range: 192-392 g; n = 16), while
the weight of full-term individuals in late June in-
creases fourfold averaging 1,291 g (range: 1,134-
1,409 g; n = 3). Schwartz (1967) reported that term
individuals average 305 mm DW, however, embryos
we considered full term are considerably larger (ca.
400 mm) and the smallest free-swimming ray we col-
lected was 323 mm. Perhaps, the embryos Schwartz
(1967) considered full term were taken in early June
and were not yet ready for parturition.
Female rays ovulate following parturition. We
found encapsulated uterine eggs in specimens taken
on 28 June and 21 July. In early August the embryos
are 20-30 mm wide and have lost the shell capsule.
By late August they average 125 mm (Figs. 2, 3).
When adult rays leave the Chesapeake Bay in late
September and early October, the embryos are
relatively large, up to 220 mm.
Reproductive cycles of large elasmobranchs are
often difficult to describe because during certain
stages of pregnancy, individuals may be inaccessible
as a result of schooling and migratory behavior
(Holden 1974). Since cownose rays leave Chesapeake
Bay by November and do not return until May, we
could not determine precisely the length of gesta-
tion. Nevertheless, an 11-12 mo gestion period
seems most probable. Within this context, the rapid
embryonic growth observed in summer would slow
during winter. A slowdown or cessation of intra-
uterine growth would be expected if gravid females
experience high energy demands during an exten-
sive migration to distant wintering grounds, possibly
northern South America as suggested by Schwartz
(1965). Thus, the embryos from late summer and fall
Figure 3.— Series of Rhinoptera bonasus embryos ranging from 18 to 140 mm disc width collected in late summer and fall.
874
SMITH and MERRINER: REPRODUCTIVE BIOLOGY OF COWNOSE RAY
would be born the following summer when the adults
return to Chesapeake Bay, a gestation period of
11-12 mo beginning in July or August and ending
in June or July.
The relatively large size of cownose ray embryos
in late September and early October suggests the
possibility of two 5-6 mo gestation periods. Partu-
rition might occur on the cownose rays' wintering
grounds followed by the gestation of another brood
of embryos destined for birth the following summer.
This hypothesis is not unprecedented, since the
presence of well-developed young in the spiny
butterfly ray, Gymnura altavela, during May in
Delaware Bay and during February off the coast of
North Carolina (27 fathoms) led Daiber and Booth
(1960) to propose two 5-6 mo gestation periods per
year for this species. Precise definition of the cow-
nose ray gestation cycle will require collecting
gravid female rays on their wintering grounds.
Embryonic Development and Nutrition
The shell capsule of the cownose ray, which we
observed twice in utero, is of a greenish amber, thin
diaphanous material, and is about 10 cm long. One
capsule held a single ovum, while the capsule from
a second female contained three ova. Ova are yellow,
extremely flaccid, and about 3-4 cm in diameter.
The embryos in late summer and fall possess yolk
stalks and yolk sacs, although these often become
detached during collection (Fig. 3). The smallest em-
bryos we collected are about 20 mm wide, batoid in
appearance, and unencapsulated. Numerous exter-
nal branchial filaments (ca. 15-30 mm long), which
emerge from the gill slits, are highly conspicuous
on small embryos (18-75 mm). These filaments are
absent in embryos larger than 89 mm.
Three-quarter term embryos are upright in the
uterus (ventral surface of the embryo on the ven-
tral wall of the uterus) with the rostrum pointed for-
ward. The pectoral fins are folded dorsally. The tail
and heavily sheathed spine are bent forward along
the dorsum of the disc. The yolk sac and stalk are
almost completely absorbed; only about 3 mm of the
umbilicus protrudes from the abdomen.
Full-term embryos are similarly oriented. How-
ever, the umbilicus is completely absorbed, leaving
only a small scar that is evident on free-swimming
young. Pigmentation is that of the adults, i.e.,
chocolate-brown dorsally, white ventrally, and black
caudally. Several tooth plates were discovered in the
left uterus from which a full-term young was re-
moved, confirming Bigelow and Schroeders' (1953)
report that tooth replacement begins in utero.
During the early stages of gestation the uterus
is rigid and thick-walled, but it gradually expands
to accommodate the developing young. Just prior
to parturition, it is extremely distended (ca. 15 cm
at its greatest breadth), thin-walled, and flaccid.
Myliobatoids overcome spatial restrictions in utero
by rolling the pectoral fins dorsally or ventrally,
along the anterioposterior axis (Gudger 1951), and
some studies report that larger than average
females carry more and larger offspring (e.g., Babel
1967). Although we observed multiple encapsulated
ova in cownose rays, and others have cited the oc-
currence of multiple embryos in utero (Smith 1907;
Gudger 1910; Bearden 1965), we never found more
than one embryo per gravid female. Setna and
Sarangdhar (1949) and James (1962, 1970) made
similar observations for the Javanese cownose ray,
R. javanica, from the Indian Ocean. Our data for
term embryos (n = 4) are insufficient to corrolate
embryo size with parent's size; however, we suspect
that in general only one cownose ray embryo is car-
ried to term.
Embryonic nutrition is from yolk and histotrophe.
Yolk of the late summer and fall embryos (n = 33)
gradually diminishes between August and October
(Fig. 4), and most yolk reserves are probably util-
ized when embryos are about 20 cm. Histotrophe,
a viscid, yellowish secretion of the uterus (as also
cited by Schwartz 1967), also nourishes the embryos.
The amount of histotrophe, although not quantified,
increases considerably as gestation progresses. Tro-
phonemata, the uterine villi that produce histo-
trophe, are deep red, flattened in cross section and
spatulate distally. They attain their greatest length
(ca. 2-3 cm) in females with near full-term embryos.
The trophonemata occasionally invade the gill slits.
In summarizing chondrichthyan, fetal-maternal
relationships, Wourms (1977) noted that the effi-
ciency of placental analogues, the villiform tropho-
nemata, far surpasses that of the yolk-sac placenta
exhibited by some carcharhinids. In cownose ray em-
bryos, yolk apparently provides initial nutritional re-
quirements. Embryos may augment yolk supplies
during the first month of gestation by absorbing
histotrophe via the external branchial filaments, as
was suggested for Urolophus halleri by Babel
(1967). After October, histotrophe supplies nourish-
ment for the remainder of the gestation period,
probably engulfed via the mouth, spiracles, and gill
slits.
Viviparity and the use of nursery areas that are
relatively free of predators, e.g., Chesapeake Bay,
no doubt protect young cownose rays. Large car-
charhinids, of which batoids are purported to be a
875
FISHERY BULLETIN: VOL. 84, NO. 4
I6-1
14 -
1 12"
10-
8-
Ld
2
Z3
_J
o
>
<
V)
5 4
o
2-
»
— I 1 1 1 1 1 1 1 1 1 1 1
0 20 40 60 80 100 120 140 160 180 200 220 240
EMBRYO DISC WIDTH (mm)
Figure 4.— Relationship of yolk-sac volume (mL) to disc width (mm) for Rhinoptera
bonasus embryos collected in late summer and fall.
favorite prey (Darnell 1958; Budker 1971) are abun-
dant seaward of the Virginia capes during summer
(Lawler 1976), but generally only the sandbar shark,
Carcharhinus plumbeus, and the bull shark, C.
leucas, frequent the Chesapeake Bay proper
(Schwartz 1960; Musick 1972). Although gravid
female sandbar sharks utilize the eastern shore of
the Chesapeake Bay (Lawler 1976), they may not
pose a threat to cownose rays, since the female sand-
bar sharks generally abstain from feeding while on
their pupping grounds and males tend to avoid such
areas (Springer 1960). Bull sharks (Schwartz 1959)
may represent the only major predators of rays in
Chesapeake Bay during summer.
ACKNOWLEDGMENTS
We thank J. A. Musick, G. R. Huntsman, A. B.
Powell, W. R. Nicholson, J. Colvocoresses, and two
anonymous reviewers for their comments and
critical review of the various drafts of this manu-
script. Numerous students and staff at Virginia In-
stitute of Marine Science lent valuable assistance
during various phases of this study, especially J.
Gourley, R. Lambert, R. K. Dias, E. F. Lawler, R.
J. Orth, and C. E. Richards. Captains Buddy Pon-
ton, George Ross, Benny Belvin, and Herman
Greene kindly provided "stingers" from their com-
mercial catches. W. S. Otwell and F. J. Schwartz
generously shared their life history notes on the
cownose ray.
Support for the study was provided by the Sea
Grant program of the Virginia Institute of Marine
Science (Grant Nos. 04-6-158-44-047 and 04-7-158-
44-109). Additional financial assistance was provided
by the Gulf and South Atlantic Fisheries Develop-
ment Foundation, Inc., Tampa, FL.
LITERATURE CITED
Babel, J. S.
1967. Reproduction, life history, and ecology of the round
stingray, Urolvphus halleri Cooper. Calif. Dep. Fish Game,
Fish Bull. 137:1-104.
Bearden, C. M.
1965. Elasmobranch fishes of South Carolina. Contrib.
Bears Bluff Lab. 42:1-19.
BlGELOW, H. B., AND W. C. SCHROEDER.
1953. Fishes of the Western North Atlantic. Pt. 2. Sawfishes,
guitarfishes, skates, rays, and chimaeroids. Mem. Sears
Found. Mar. Res., Yale Univ. 1:1-588.
Budker, P.
1971. The life of sharks. Columbia Univ. Press, N.Y., 222 p.
Clark, E., and K. von Schmidt.
1965. Sharks of the central Gulf Coast of Florida. Bull. Mar.
Sci. 15:13-83.
Daiber, F. C, and R. A. Booth.
1960. Notes on the biology of the butterfly rays, Gymnura
altavela and Gymnura micrura. Copeia 1960:137-139.
Darnell, R. M.
1958. Food habits of fishes and larger invertebrates of Lake
Pontchartrain, Louisiana, an estuarine community. Publ.
Inst. Mar. Sci. Univ. Tex. 5:353-416.
Gilbert, P. W., and G. W. Heath.
1972. The clasper-siphon sac mechanism in Squalus acanthias
and Mustelus canis. Comp. Biochem. Physiol. A Comp.
Physiol. 42:97-119.
Gudger, E. W.
1910. Notes on some Beaufort fishes-1909. Am. Nat. 44:
395-403.
1912. Natural history notes on some Beaufort, N.C., fishes,
1910-11. No. I. Elasmobranchii— with special reference to
utero-gestation. Proc. Biol. Soc. Wash. 25:141-156.
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SMITH and MERRINER: REPRODUCTIVE BIOLOGY OF COWNOSE RAY
1951. How difficult parturition in certain viviparous sharks
and rays is overcome. J. Elisha Mitchell Sci. Soc. 67:56-86.
Hamilton, W. J., Jr., and R. A. Smith.
1941. Notes on the sting-ray, Dasyatis say (LeSueur).
Copeia 1941:175.
Hess, P. W.
1959. The biology of two sting rays, Dasyatis centroura
Mitchill 1815 and Dasyatis say Lesueur 1871, in Delaware
Bay. M.S. Thesis, Univ. Delaware, Newark, 42. p.
Hoese, H. D.
1962. Sharks and rays of Virginia's seaside bays. Chesa-
peake Sci. 3:166-172.
Holden, M. J.
1974. Problems in the rational exploitation of elasmobranch
populations and some suggested solutions. In F. R. Harden-
Jones (editor), Sea fisheries research, p. 117-137. Wiley,
N.Y.
James, P. S. B. R.
1962. Observations on shoals of the Javanese cownose ray
Rhinoptera javanica Muller and Henle from the Gulf of Man-
nar with additional notes on the species. J. Mar. Biol.
Assoc. India 4:217-223.
1970. Further observations on shoals of the Javanese cownose
ray Rhinoptera javanica Muller and Henle from the Gulf of
Mannar with a note on the teeth structure in the species.
J. Mar. Biol. Assoc. India 12:151-157.
Joseph, E. B.
1961. An albino cownose ray, Rhinoptera bonasus (Mitchill)
from Chesapeake Bay. Copeia 1961:482-483.
Lawler, E. F.
1976. The biology of the sandbar shark Carcharhinus plum-
beus (Nardo, 1827) in the lower Chesapeake Bay and adja-
cent waters. M.A. Thesis, College of William and Mary,
Williamsburg, 48 p.
Merriner, J. V., and J. W. Smith.
1979. A report to the oyster industry of Virginia on the
biology and management of the cownose ray (Rhinoptera
bonasus, Mitchill) in lower Chesapeake Bay. Spec. Rep.
Appl. Mar. Sci. Ocean Eng. 216, 33 p. Va. Inst. Mar. Sci.
Musick, J. A.
1972. Fishes of Chesapeake Bay and the adjacent coastal
plain. In M. L. Wass (editor), A check list of the biota of
lower Chesapeake Bay, p. 175-212. Va. Inst. Mar. Sci.,
Spec. Rep. No. 65.
Orth, R. J.
1975. Destruction of eelgrass, Zostera marina, by the cow-
nose ray, Rhinoptera bonasus, in the Chesapeake Bay.
Chesapeake Sci. 16:205-208.
Schwartz, F. J.
1959. Two eight-foot cub sharks, Carcharhinus leucas (Muller
and Henle), captured in Chesapeake Bay, Maryland. Copeia
1959:251-252.
1960. Additional comments on adult bull sharks, Carcharhi-
nus leucas (Muller and Henle), from Chesapeake Bay,
Maryland. Chesapeake Sci. 1:68-71.
1965. Inter-American migrations and systematics of the
western Atlantic cownose ray, Rhinoptera bonasus. [Abstr.]
Meet. Assoc. Isl. Mar. Lab. Caribb., 1 p. 6th Meet., Isla
Margarita, Venez. 20-22 Jan.
1967. Embryology and feeding behavior of the Atlantic cow-
nose ray Rhinoptera bonasus. [Abstr.] Meet. Assoc. Isl.
Mar. Labs. Carib. 1 p. 7th Meet., Barbados, W.I., 24-26
Aug..
Setna, S. B., and P. N. Sarangdhar.
1949. Breeding habits of Bombay elasmobranchs. Rec. In-
dian Mus. (Calcutta) 47:107-124.
Smith, H. M.
1907. The fishes of North Carolina. N.C. Geol. Econ. Surv.
2:47.
Smith, J. W.
1980. The life history of the cownose ray, Rhinoptera bonasus
(Mitchill 1815), in lower Chesapeake Bay, with notes on the
management of the species. M.A. Thesis, College of
William and Mary, Williamsburg, 151 p.
Smith, M. S.
1975. A. P. Knight Groundfish Cruise No. 74-2, October
15-17, 1974 (Data Record). Fish. Res. Board Can. Manuscr.
Rep. Ser. No. 1336, 13 p.
Springer, S.
1960. Natural history of the sandbar shark, Eulamia milber-
ti. U.S. Fish Wildl. Serv., Fish. Bull. 61:1-38.
Struhsaker, P.
1969. Observations on the biology and distribution of the
thorny stingray, Dasyatis centroura (Pisces:Dasyatidae).
Bull. Mar. Sci. 19:456-481.
Wourms, J. P.
1977. Reproduction and development in chondrichthyan
fishes. Am. Zool. 17:379-410.
877
NORTHERN ANCHOVY, ENGRAULIS MORDAX, SPAWNING IN
SAN FRANCISCO BAY, CALIFORNIA, 1978-79, RELATIVE TO
HYDROGRAPHY AND ZOOPLANKTON PREY OF ADULTS AND LARVAE
Michael F. McGowan1
ABSTRACT
Eggs and larvae of Engraulis mordax were sampled by nets monthly for one year. Either eggs or larvae
were caught every month. Both were most abundant when water temperature was high. Mean egg abun-
dance did not differ among stations but larvae were more abundant within the San Francisco Bay at
high and low salinity than near the ocean entrance to the Bay. Larvae longer than 15 mm were collected
over the shoals in spring and autumn but were in the channel during winter. Zooplankton and
microzooplankton were abundant relative to mean California Current densities. Adult spawning biomass
in the Bay was 767 tons in July 1978, based on egg abundance and fecundity parameters of oceanic animals.
San Francisco Bay was a good spawning area for northern anchovy because food for adults and larvae
was abundant and because advective losses of larvae would have been lower in the Bay than in coastal
waters at the same latitude.
The northern anchovy, Engraulis mordax, is the
most abundant fish in San Francisco Bay (Aplin
1967), but little is known about the seasonal dura-
tion or areal extent of northern anchovy spawning
there (Eldridge 1977; Sitts and Knight 1979; Wang
1981). In the California Current, spawning is
thought to be related to abundance of food for adults
(Brewer 1978) or to seasonal patterns of abundance
of food for larvae (Lasker 1978). Dense patches of
appropriate food for larvae are believed to be neces-
sary for survival of larvae (Lasker 1975; Scura and
Jerde 1977). Zooplankton are generally more abun-
dant in estuaries than in coastal and oceanic waters.
Therefore, San Francisco Bay, the largest estuary
on the west coast of North America, could be a
favorable habitat for spawning northern anchovy
and their developing larvae.
The northern anchovy could affect plankton
dynamics in the San Francisco Bay (the Bay) by
preying on zooplankton and by excreting concen-
trated nutrients for phytoplankton. It is the target
of a seasonal bait fishery (Smith and Kato 1979), and
it is an important forage fish for many other species
(Recksiek and Frey 1978). Quantitative estimates
of the adult stock size and numbers of eggs and lar-
vae are needed to understand the ecology of this
anchovy in the Bay.
This paper reports the results of a 1-yr survey of
Cooperative Institute for Marine and Atmospheric Studies,
Rosenstiel School of Marine and Atmospheric Science, University
of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149.
the northern anchovy eggs and larvae, zooplankton,
and microzooplankton in San Francisco Bay. Dis-
tribution and abundance of eggs and larvae were
related to water temperature, salinity, turbidity,
stratification, abundances of potential adult prey,
and potential larvae prey. The suitability of the Bay
for spawning and development of larvae was as-
sessed. An estimate of spawning stock abundance
within the Bay was calculated from egg abundance,
and the impact of this biomass of anchovies on the
zooplankton was estimated.
MATERIALS AND METHODS
Study Site
San Francisco Bay consists of three major parts
(Fig. 1): 1) Central Bay opens to the Pacific Ocean
through the Golden Gate at lat. 37°49'N, long.
112°29'W; 2) North Bay receives the drainage from
the Sacramento and San Joaquin Rivers and in-
cludes Suisun, San Pablo, and Richardson Bays;
3) South Bay is the largest single embayment, ex-
tending some 27 nmi from Coyote Creek in the south
to the Oakland-San Francisco Bay Bridge in the
north. The following description of San Francisco
Bay was taken from Conomos and Peterson (1977).
Mean depth is 6 m at mean lower low water, or 2
m if the large expanses of mudflats are included.
There is a 10 m deep dredged ship channel in the
northern part. Tides are mixed semidiurnal ranging
from 1.7 m at the Golden Gate to 2.7 m at the south-
Manuscript accepted July 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
879
FISHERY BULLETIN: VOL. 84, NO. 4
122°30"
122c
i
38°-
37°30-
SAN FRANCI
GULF OF THE
FARALLONES
Miles 0
L
5
_L_
Kilometers
10
10
_L_
1 r
SAN FRANCISCO BAY
Figure 1.— Locations of stations and the areas represented by each station sampled monthly May 1978-April
1979.
ern end of South Bay. The tidal prism is 27% of the
Bay volume. Maximum tidal currents occur in the
channels and may be 225 cm/s (4.5 kn) at the Golden
Gate. More than 90% of the freshwater entering San
Francisco Bay enters North Bay from the Sacra-
mento and San Joaquin Rivers. Less than 10%
enters South Bay from small tributary streams and
sewage. Because of the difference in freshwater in-
flow the northern and southern reaches are very dif-
ferent types of estuary. North Bay is partially-to-
well-mixed with true two-layer estuarine circulation.
South Bay, dependent for water exchange on tidal
circulation and occasional incursions of freshwater
from the north during wet winters, resembles a
coastal lagoon.
The heterogeneous nature of San Francisco Bay
requires that stations be representative of the
diverse areas of the Bay. The stations (Fig. 1) were
located in the channel adjacent to the shoals in the
South Bay in 5-6 m of water (stations 1 and 2); just
north of San Bruno Shoal in 3 m of water (station
3); east of Treasure Island over a dredge borrow pit
in 10 m of water (station 4); in midchannel just south
of the Richmond-San Rafael Bridge in 10-13 m of
water (station 5); and north of Lime Point just in-
side the Golden Gate Bridge in 25-35 m of water
(Station 6). These sites were near those of a previous
trawl study (Aplin 1967) and they represented loca-
tions from South Bay, Central Bay, the outflow from
North Bay, and the Pacific Ocean entrance to the
Bay.
All South Bay stations were sampled in one day,
all Central Bay stations were sampled on another
day, usually the day following the South Bay sam-
pling. This schedule and the pattern of tidal flow in
the Bay (Tidal Current Chart, San Francisco Bay
1973) enabled all stations to be sampled before noon
at approximately slack tide, low water. This sched-
ule controlled for the effects of time of day, tide,
and currents which can affect catches of ichthyo-
plankton (Eldridge 1977). Additional samples were
taken in October 1978 and April 1979 at station 3
and over the shoals adjacent to this station.
Duplicate oblique ichthyoplankton tows and dupli-
cate surface microzooplankton tows were made
monthly at six stations for one year, May 1978-April
880
McGOWAN: SPAWNING OF NORTHERN ANCHOVY
1979. Ichthyoplankton and zooplankton samples
were collected from a 5 m Boston Whaler with a 1
m diameter, cylinder-cone net of 0.308 mm mesh
nylon with a 0.200 mm mesh cod end. The net was
attached to a sled which kept the lower rim of the
net 10 cm above the bottom and which had a tow-
bridle that did not obstruct the mouth of the net.
A frame attached to the transom permitted the sled
to be launched and retrieved over the stern while
underway. The sled was lowered to the bottom while
underway at 1-2 kn, towed at the bottom for 1 min,
and then retrieved at a constant rate and constant
wire angle. Tow time, excluding that spent lower-
ing the net to the bottom, was approximately 6 min.
The gear was effective because it often caught an-
chovies and herring longer than 30 mm, a size not
usually captured in towed gear (Clarke 1983) or in
a plankton purse seine (Murphy and Clutter 1972).
A calibrated flowmeter suspended off-center in
the mouth of the net measured the amount of water
filtered during the tow. Volumes calculated from the
flowmeter readings were similar to a hypothetical
volume calculated from net mouth area and tow
distance: approximately 300 m3/tow.
Microzooplankton was collected with a 0.5 m diam-
eter net with 0.080 mm mesh, which was towed just
submerged at the surface for 2 min during the ich-
thyoplankton tow. Because the flowmeter in this net
frequently malfunctioned, hypothetical volumes
calculated from mouth diameter and tow length (ap-
proximately 25 m3/tow) were used to standardize
catches of microzooplankton. The net probably did
not filter as much water as calculated so
microzooplankton were underestimated. All samples
were preserved with 2% formaldehyde in seawater
buffered with sodium borate.
Water turbidity was measured with a Secchi disk
(Tyler 1968). Water samples for salinity and tem-
perature measurements were taken with a Van
Dorn water sampler from 1 m below the surface and
from 1 m above the bottom. The temperature was
measured to 0.1°C with a laboratory thermometer,
and salinity was measured to 0.5°/oo with a temper-
ature-compensated refractometer.
Laboratory Procedures
Northern anchovy eggs were easily recognized
and distinguished from other regional pelagic fish
eggs by their oval shape and their size, approxi-
mately 0.75 mm x 1.25 mm. Eggs were not as-
signed to stages, but some of the embryos were
developed enough to be identified as those of north-
ern anchovies. Northern anchovy eggs were counted
under a dissecting microscope; at the same time, fish
larvae were picked from the samples. The northern
anchovy can be separated from other similar look-
ing larvae by its myomere count (43-47), its gut
length, and its median fin positions (Miller and Lea
1972; McGowan and Berry 1984).
All northern anchovy larvae <10 mm long were
measured to the nearest 0.1 mm using an ocular
micrometer. Longer larvae were measured to 1 mm
using vernier calipers or a plastic ruler graduated
in millimeters. The distance from the tip of the snout
to the tip of the notochord was measured in pre-
flexion larvae, standard length in larger specimens.
Zooplankton were subsampled from a 500 mL
pharmaceutical beaker by stirring and taking an ali-
quot with a 1 mL or 2 mL Stempel pipet. Zooplank-
ton were identified to major taxonomic group under
the dissecting microscope using standard references
such as Smith (1977). All holoplanktonic, meroplank-
tonic, and nektonic invertebrates were considered
to be zooplankton if they were suitably sized prey
for adult anchovies. Isopods were included; adult
shrimp and gelatinous invertebrates were not.
Plankton was allowed to settle in water in a grad-
uated cylinder to estimate zooplankton volume.
Microzooplankton were subsampled from a stirred
beaker with a pipet. A settling chamber and inverted
compound microscope with movable stage were used
to count microzooplankton (0.050-0.200 mm
diameter) at 100 x magnification. Dinoflagellates
known to be eaten by anchovy larvae were counted
as microzooplankton.
Precision Estimates
The precision of the microzooplankton counts was
estimated by the method of Lund et al. (1958). If
the counts are treated as a Poisson variable then
the 95% confidence limits for a single count are
Upper limit = X + 2.42 + 1.96(Z + 1.5)1/2
Lower limit = X + 1.42 - 1.96(X + 0.5)1/2.
The limits are approximately ±20% if 100 organ-
isms are counted. Confidence intervals for micro-
zooplankton counts in this study range from + 50%
at the lowest count (5) to + 9% at the highest count
(659).
The precision of the zooplankton subsampling esti-
mates was evaluated by taking triplicate subsam-
ples, with replacement, from 10 randomly selected
samples. The mean coefficient of variation (standard
deviation divided by the mean) of the triplicates was
0.29.
881
FISHERY BULLETIN: VOL. 84, NO. 4
The precision of the duplicate tows was evaluated
by comparing numbers of eggs, larvae, and zoo-
plankton settled volumes from the May, June, and
July tows. No statistical difference was detected
between first and second tows (2-tailed P = 0.407,
Wilcoxon Matched Pairs test, Hull and Nie 1981:
228). The mean coefficient of variation for these
paired tows was 0.22. Because there were no statis-
tical differences between these duplicates, only one
of each pair of the remaining samples was sorted.
Data Analysis
Eggs, larvae, zooplankton, microzooplankton, and
plankton volume per 1,000 m3 were calculated
based on flowmeter readings. Temperature and
salinity stratification variables were created by
taking the difference between surface and bottom
values. Salinity stratification represented the inten-
sity of estuarine circulation or freshwater runoff;
temperature stratification represented water
column stability and revealed atmospheric tempera-
ture extremes.
Distributions of the variables were examined for
skewness, kurtosis, and unreasonable range limits
indicative of keypunch errors. Normality of the
original variables and of \og(X + 1) transformations
was tested (Kolmogorov-Smirnov test; Hull and Nie
1981:224). Variances of the transformed variables
were not heteroscedastic. Biological and environ-
mental variables were plotted against month, sta-
tion, and each other to look for spatial patterns,
seasonal trends, and nonliner relationships (espe-
cially nonmonotonicity) between pairs of variables.
Analysis of variance (ANOVA) was used to assess
the effects of month of the year and station loca-
tion on numbers of eggs and numbers of larvae.
Stepwise multiple linear regression was used to ex-
amine which of the other variables could account
statistically for the variability in numbers of eggs
and larvae. Logarithmic transformations of stan-
dardized numbers of eggs, larvae, zooplankton, and
microzooplankton were used in the regressions and
in the ANOVA' s.
Ichthyoplankton abundance is often expressed as
numbers of ichthyoplankton under an area of sea
surface by multiplying density per cubic meter times
water depth (Smith and Richardson 1977). In deep
water tows are made below the depth range of most
eggs and larvae, so the tow depth is used as the ef-
fective water depth. Standardizing a unit of sea sur-
face area allows comparisons of total numbers of
eggs and larvae in the water column from areas with
different water depths. Abundance standardized to
area of sea surface was used to estimate total egg
production. However, larvae that were relatively
uncommon in deep water could be as abundant as
more concentrated larvae in shallow water, but ex-
posed to different concentrations of predators and
prey; therefore, densities of larvae and plankton
were used to examine relationships between ich-
thyoplankton, other plankton, and environmental
variables.
The method used to estimate spawning stock bio-
mass was a direct estimate because it incorporated
batch fecundity from histological data (Hunter and
Goldberg 1980) and daily egg production estimates
from ichthyoplankton surveys (Parker 1980).
Parker's equation for the direct estimate of biomass
from egg abundance is
5 = P{ab'c)-ld
where 5
P
a
= spawning biomass in tons
= egg production in eggs/day
= 3.96 x 108 egg/ton
b'
= 0.159 the observed daily spawning
fraction
c
= 0.550 the proportional biomass of
females
d
= 1.080 a correction for potential mis-
classification of daily spawning frac-
tion.
Parker (1980) estimated the coefficient of varia-
tion of the estimate of spawning stock to be 0.614.
Most of this statistical error was due to error in the
estimate of egg production. Daily egg production
was estimated in my study by dividing the egg abun-
dance by the number of days needed to hatch at the
ambient temperature (interpolated from Zweifel and
Lasker 1976, fig. 7).
Numbers per square meter of Bay surface were
calculated by multiplying density per cubic meter
times water depth at the station. The areas repre-
sented by the stations were estimated from the chart
of the Bay in Conomos and Peterson (1977). Total
numbers of eggs and larvae were calculated from
estimates per square meter times the area repre-
sented by the sample.
RESULTS
Eggs and Larvae
Either eggs, larvae, or both were present every
month of the year. Eggs were present every month
except December and January. Only one egg was
882
McGOWAN: SPAWNING OF NORTHERN ANCHOVY
collected in February and very few were collected
in November. Larvae were present every month and
at every station each month with four exceptions:
during June, no larvae were collected at station 1,
the southernmost station; during July and August
no larvae were collected at station 6, the Golden
Gate Bridge station; during March no larvae were
collected at station 3 in South Bay. Eggs were pres-
ent on each of the occasions when larvae were
absent from the samples.
Egg density varied from 0 to 55,000 per 1,000 m3
(mean = 3,000). The greatest number of eggs in a
single sample was 14,640 at station 2 in July. Occur-
rence of eggs was seasonal: they were abundant in
summer and absent in winter (Fig. 2).
Larvae varied from 0 to 4,400 per 1,000 m3
(mean = 259). The greatest number of larvae in a
single sample was 1,420 in September at station 2.
Larval abundance was also seasonal with peak den-
sity in late summer and fall (Fig. 2).
Two-way ANOVA of log-transformed standard-
ized densities of eggs and larvae were performed
with month and station as fixed factors in separate
analyses. The interaction mean square (not signifi-
cant) was used as the denominator in the F-tests
because there was just one observation per cell of
the design (Montgomery 1976:156). Densities of
eggs differed significantly among months (P <
0.001, Table 1) but not among stations (P = 0.104).
Densities of larvae were significantly different
among months (P = 0.010) and among stations (P
= 0.014) (Table 2).
Seasonal patterns of abundance of eggs and lar-
Table 1 . — Analysis of variance of northern anchovy eggs:
month by station.
Source of
Sum of
Mean
Signif-
variation
squares
df
square
F
icance
Residual
42.23
54
0.78
Constant
286.22
1
286.22
366.02
0.000
Month
128.93
11
11.72
14.99
0.000
Station
7.56
5
1.51
1.93
0.104
Month x
station
0.48
1
0.48
0.61
0.437
Table 2.— Analysis of variance of northern anchovy larvae:
month by station.
Source of
Sum of
Mean
Signif-
variation
squares
df
square
F
icance
Residual
25.77
54
0.48
Constant
220.65
1
220.65
462.43
0.000
Month
13.72
11
1.25
2.61
0.010
Station
7.59
5
1.52
3.18
0.014
Month x
station
1.16
1
1.16
2.43
0.125
vae were unmistakeable, but differences among sta-
tions were not as clear so three hypotheses were
tested: 1) stations 1, 2, and 3, South Bay stations,
differed from stations 4, 5, and 6; 2) stations 4 and
6, Golden Gate and Central Bay stations, differed
from stations 1, 2, 3, and 5, South Bay stations plus
the station at the outflow of San Pablo Bay; 3) sta-
tions 3, 4, and 6, the stations most influenced by
ocean water, differed from stations 1, 2, and 5, the
Bay stations. These hypotheses were tested using
linear contrasts (Nie et al. 1975:425), a procedure
that compared the geometric means of the groups
of stations.
None of the three contrasts was significant for
eggs but all three were significant (P < 0.05) for lar-
vae. The difference between the mean of stations
4 and 6 and the mean of stations 1, 2, 3, and 5 was
highly significant (P = 0.001).
Further comparisons of mean densities of larvae
were done using Duncan's Multiple Range test. This
a posteriori procedure identified groups of means
which did not differ significantly from each other
at a specified level (Nie et al. 1975:427). The rank
order of the stations in increasing mean density of
larvae was 4,6, 1,3,5,2. Three groupings were pro-
duced by the Duncan procedure at the 0.05 level.
The mean of stations 4 and 6 was smaller than the
mean of the other four. The mean of stations 5 and
2 was greater than that of the other four. Station
4 was significantly lower and station 2 significant-
ly higher than the mean of the other four stations.
A summary of the analyses of variance follows.
Eggs and larvae were seasonal in abundance, eggs
more strongly than larvae. Numbers of eggs, which
would be subject to passive drift and dispersal, were
not significantly different among locations in the
Bay. Larvae did differ in abundance among the six
stations. Based on a priori and a posteriori tests,
station 4 and station 6, the stations most influenced
by oceanic water, had low densities of larvae while
the other stations within the Bay had high mean den-
sities of larvae. This pattern was true for station
5, near the Richmond-San Rafael Bridge, as well as
for stations 1, 2, and 3 in the South Bay. Among
the within-bay stations, station 1, the southernmost,
ranked lowest in both egg density and larval den-
sity although it was not statistically different from
the other inner stations— 2, 3, and 5.
The stations also differed in the proportion of eggs
to larvae. While the ratio of eggs to larvae was
generally greater than 10:1, at station 3 the ratio
of the mean number of eggs to mean number of lar-
vae was <10:1 (Fig. 3). The proportions were sta-
tistically different among stations (Chi-square P <
883
FISHERY BULLETIN: VOL. 84, NO. 4
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884
McGOWAN: SPAWNING OF NORTHERN ANCHOVY
EGGS
10000-
9000
8000
7000
6000--
5000
4000
3000
2000
Figure 3.— Relative abundances of northern -|000
anchovy eggs and larvae at each station show-
ing the difference between station 3 and the q
other stations.
LARVAE
1000
900
MEAN CATCH EGGS AND LARVAE
AT EACH STATION
NUMBERS ARE PER 1000 METERS CUBED
♦ LARVAE
-I 1 1 i 1
2 3 4 5 6
STATION
0.01 with 5 degrees of freedom). Station 3 deviated
most from the expected ratio. Station 1 also differed
by having relatively fewer larvae than expected.
Zooplankton
Zooplankton catch varied from 13.6-9,560 indivi-
duals/m3. Mean catch was 1,170/m3. No seasonal
pattern was apparent (Fig. 2). There was a gradual
increase in zooplankton abundance over the course
of the study. This linear trend was significant (P <
0.01). Copepods, especially A cartia spp., dominated
Table 3.— Zooplar
ikton: relative density, May
1978-
April 1979
mean
Taxon
±1 SE
nm 3
%
Copepoda
Acartia
1,120
+
192
96.05
harpacticoida
4.67
+
1.55
0.40
other
3.48
±
0.75
0.30
shrimp zoeae
3.82
+
1.28
0.33
crab zoeae
12.27
±
4.27
1.04
mysids
1.31
+
1.16
0.10
amphipods
0.39
+
0.16
0.03
pelecypods
1.10
+
0.35
0.09
chaetognaths
0.59
+
0.23
0.05
polychaetes
1.26
+
0.50
0.11
isopods
0.23
+
0.12
0.02
barnacle nauplii
9.18
+
2.04
0.78
barnacle cyprids
6.18
+
1.49
0.52
gastropods
0.74
+
0.37
0.06
cumaceans
0.08
+
0.05
0.01
cladocerans
0.81
+
0.31
0.07
the catches (Table 3). Brachyuran (crab) zooeae and
cirrepedian (barnacle) nauplii and cyprids were occa-
sionally abundant. Potential predators on northern
anchovy larvae, such as chaetognaths and pontellid
copepods, were often present but in relatively low
numbers. Counts of zooplankton for each sample are
reported in McGowan (unpublished M. A. Thesis, San
Francisco State University, San Francisco, CA).
Zooplankton catch was significantly correlated
with all variables except surface salinity and salin-
ity stratification. Negative correlations were ob-
served with egg density, surface temperature,
temperature stratification, and Secchi depth. Posi-
tive correlations were found with larvae and
microzooplankton .
Microzooplankton
Microzooplankton catch at the surface (0.080 mm
mesh net) varied from 1 to 300 per liter (mean =
28.8). No clear seasonal trend was apparent (Fig.
2). Copepod nauplii were the most abundant micro-
zooplankton followed by tintinnids and rotifers
(Table 4). Dinoflagellates such as Ceratium and
Peridinium were occasionally more abundant than
copepod nauplii. The spiny, armored Ceratium
species were not included in the density estimates
because northern anchovy larvae prefer unarmored
forms (Scura and Jerde 1977). Microzooplankton
density was negatively correlated with Secchi disk
depth (r = -0.34, P = 0.004) and positively corre-
885
FISHERY BULLETIN: VOL. 84, NO. 4
Table 4.— Microzooplankton: relative density, May
1978-April 1979.
Taxon
mean
+ 1 SE
n-1
copepod nauplii
15.14
±
1.82
54.97
barnacle nauplii
0.56
+
0.09
2.03
polychaete larvae
0.36
±
0.08
1.31
tintinnids
6.56
+
2.68
23.82
rotifers
1.24
+
0.45
4.50
harpacticoid copepods
0.03
+
0.02
0.11
ostracods
0.01
+
0.01
0.04
gastropod veligers
0.04
+
0.02
0.15
Peridinium
3.59
±
1.45
13.03
lated with zooplankton density (r = 0.27, P = 0.027).
All interpretation of the microzooplankton data was
done under the assumption that estimates of volume
filtered are accurate.
Environmental Variables
The mean surface water temperature during this
study was 15.2°C. The coldest reading was 8.0°C
at station 2 in January; the warmest was 22.5 °C at
station 1 in August (Fig. 2). Water temperature near
the bottom varied from 8° to 21.5°C (mean =
15.0°C). Mean temperature stratification, the dif-
ference between the surface and bottom tempera-
tures, was 0.2°C. Stratification was generally pres-
ent June through October, especially at station 5.
Mean stratification during these months was 0.5°C
(Fig. 2). During February and March 1979 the sur-
face temperature was lower, on average, than the
temperature near the bottom thus showing the influ-
ence of air temperature on the surface water tem-
perature. Surface salinity varied from 3 to 31°/oo
(mean = 23.6%o). Bottom salinity was 14-31%o
(mean = 24.8%o). The low readings for both sur-
face and bottom salinity occurred at station 5 dur-
ing March 1979. Surface salinity at station 1 was
usually low, showing the influence of freshwater in-
flow at the south end of the Bay (Fig. 2). Salinity
at station 6 was relatively high, showing the oceanic
influence at the Golden Gate. Surface salinity at
other stations reflected their relative positions be-
tween these two influences. The lowest surface
salinity was always at station 5 due to the Sacra-
mento River discharge. During March 1979, salin-
ity at stations 4 and 6 also showed the effects of high
freshwater discharge which lowered the salinity at
station 5 to 3%o. Salinity was slightly lowered this
month at station 3 in South Bay also. Surface salin-
ity followed a seasonal pattern; it was high from July
through January and low in the winter and spring
months. Relatively high salinity corresponded to
high temperature July through October. Salinity
stratification was generally <2%o except at station
5 where the average stratification was 4.7°/oo (Fig.
2).
Surface salinity was negatively correlated with
salinity stratification, (r = -0.62, P < 0.001), and
positively correlated with Secchi depth (r = 0.39,
P = 0.001). Salinity stratification was negatively
correlated with Secchi depth (r = - 0.29, P = 0.012).
Turbidity
Light penetration was lowest at stations 1 and 5,
and highest at stations 6, 4, and 3 (Fig. 2). The mean
depth of light penetration during this study was 1.1
m with a range of 0.1-2.5 m. The data suggest a
weak seasonal trend with light transmission higher
in summer and lower in winter. The variable with
the strongest linear association with Secchi depth
was zooplankton density. Light penetration was in-
versely related to zooplankton density (r = -0.58).
Relationships Among Varibles
Northern anchovy egg abundances were positively
associated with surface temperature, temperature
stratification, and Secchi disk depth and negative-
ly correlated with zooplankton density (Table 5).
Eggs were positively associated with larvae but this
correlation was not significant at the 5% level (P
= 0.053). Larvae were positively correlated with
surface temperature and zooplankton density (Table
5). They were negatively correlated with Secchi
depth. Thus, eggs and larvae both were significantly
correlated with zooplankton and Secchi depth but
in opposite directions: eggs were associated with
clearer water and lower zooplankton density, lar-
vae with more turbid water and higher zooplankton
density.
Stepwise Multiple Regression
Surface temperature alone explained 65% of the
variability in egg density (r2 = 0.651). The combi-
nation of microzooplankton density with surface
temperature explains an additional 1.5% of the vari-
ability of egg density. The addition of all other
variables only increased the amount of variability
explained to 68% (r2 = 0.678). The predictive
regression model using the independent variables
whose addition to the model improved its prediction
by more than 1% is
E = -2.20 + 0.317T - 0.502M
886
McGOWAN: SPAWNING OF NORTHERN ANCHOVY
Table 5.— Bivariate correlations between northern anchovy eggs, larvae, and other
variables. EGGS: log (eggs-m-3); LARV: log (larvae -m"3); ZOOP: log (zooplank-
tersm-3); MICR: microzooplankton; TEMP: surface water temperature; SALI: sur-
face water salinity; TSTR: temperature stratification; SSTR: salinity stratification; SECC:
Secchi disk depth.
EGGS
LARV
ZOOP
MICR
TEMP
SALI
TSTR
SSTR
LARV
0.23 +
ZOOP
-0.33**
0.29*
MICR
-0.11
-0.02
0.27*
TEMP
0.81**
0.31**
-0.46**
0.02
SALI
0.18
0.08
-0.20
-0.16
0.19
TSTR
0.40**
0.17
-0.25*
-0.02
0.46**
0.06
SSTR
-0.10
0.07
0.05
0.09
-0.03
-0.62**
0.12
SECC
0.35**
-0.34**
-0.58**
-0.34**
0.32**
0.39**
0.20
-0.29*
* Significant at P
= 0.05.
"Significant at P
= 0.01.
* P =
0.053.
where E = log (eggs/1,000 m3 + 1)
T = surface temperature (°C)
M = log (microzooplankton/^ + 1), (Table 6).
No single variable explained the majority of the
variability in larval density (Table 7). Secchi depth
was the single best predictor, accounting for 11%
of the variance of larval density (r2 = 0.113). The
combination of surface temperature with Secchi
depth increased the coefficient of determination to
0.306. All of the variables combined explained just
50% of the variability of larval density (r2 =
0.498). Five variables improved the prediction of the
set of independent variables by more than 1% when
added to the model. The predictive equation for lar-
val density based on using these five is
L = -0.842 - 0.591X + 0.1267/ + 0.515Z
Table 6. — Stepwise multiple regression: northern anchovy
egg density vs. biological and environmental variables.
- 0.57LW + 0.029S
where L
X
T
Z
M
S
+ 1)
log (larvae/1,000 m3
Secchi depth (m)
surface temperature (°C)
log (zooplankton/1,000 m3
log (microzooplankton/^ +
surface salinity (%>o).
+ 1)
1)
The results of the multiple regressions show that
northern anchovy egg density could be predicted
largely by surface water temperature. Larval den-
sity could not be predicted well by a single variable
or by the five variables which, when combined, ac-
counted for only 49% of the variability.
Spawning Stock Estimates
Based on estimates of egg production, the spawn-
Independent
Multiple
Change in
variable
r2
Surface temperature
0.651
0.651
Microzooplankton
0.666
0.015
Salinity stratification
0.670
0.004
Surface salinity
0.672
0.002
Secchi depth
0.675
0.003
Zooplankton
0.677
0.002
Temperature stratification
0.678
0.001
Table 7.— Stepwise multiple regression: northern anchovy
larval density vs. biological and environmental variables.
Independent
Multiple
Change in
variable
r2
Secchi depth
0.113
0.113
Surface temperature
0.306
0.194
Zooplankton
0.392
0.085
Microzooplankton
0.459
0.067
Surface salinity
0.486
0.028
Salinity stratification
0.495
0.009
Temperature stratification
0.498
0.003
ing stock biomass of northern anchovies in the part
of San Francisco Bay sampled in this study ranged
from undetectable in December 1978 and January
1979 (no eggs collected) to 696 t (metric tons) (767
short tons) in July 1978. If the area of the Bay which
is <2 m deep were included, the estimate of July
biomass would have been 2,030 1 (2,240 short tons).
Length Frequencies of Larvae
Monthly samples could contain larvae from the
current month and 2 previous ones because meta-
morphosis is not complete until 35 mm, age 74 days
at 16°C (Hunter 1976). However, larvae longer than
15 mm were not taken at the standard stations from
August through October, although eggs and smaller
887
FISHERY BULLETIN: VOL. 84, NO. 4
larvae had been abundant since June (Fig. 4). Lar-
vae >15 mm long were found over the shoals near
station 3 in October and April (Fig. 5). Larvae longer
than 15 mm were taken in the channel from Novem-
ber through February, months with little or no
spawning. Large larvae and juveniles, which had ap-
parently overwintered, were present when spawn-
ing resumed in March and April.
DISCUSSION
Previous suggestions that northern anchovy
spawn in San Francisco Bay were based on the pres-
ence of small larvae (Eldridge 1977; Sitts and Knight
1979), juveniles (Smith and Kato 1979), or the
spawning season in the California Current (Hubbs
1925). Anchovy eggs collected in this study provide
conclusive evidence that the northern anchovy
spawns in San Francisco Bay because eggs could not
drift upstream to station 5 or into South Bay as far
as station 1 or 2. Peak spawning based on the abun-
dance of eggs was May through September when
adult anchovies are known to be plentiful in the Bay
(Aplin 1967).
Spawning in San Francisco Bay differed from an-
chovy spawning in the sea. Most spawning of the
central subpopulation of northern anchovy in the
California Current takes place January- April when
the 10 m temperature isl4°-16°C; not June through
October when water temperature is 16°-19°C
MAY
NOVEMBER
N=237
N=260
-
i
1 I 1
1 i i
I I I I I
JUNE
DECEMBER
N=56
— 1 r—
N=
=32
I I 1
r
II ill
I 111
JULY
JANUARY
N=162
N=156
—
~~1— .
l l I l I 1
i i — | 1 1
_
AUGUST
FEBRUARY
-
N=483
N=222
. 1
1 i i i 1 l
SEPTEMBER
i 1 1 1 1 1 1
MARCH
N=2313
N=
1 1
=62
100-n
ii i i in
1 1 — | 1
O 75_
OCTOBER
APRIL
< 50-
O
N=156
N=161
gS 25-
—
U~1
c
) 5 10 15 20 25 30 35
ST
ANC
ARC
• LE
NGT
H C
LASS (mn
l)
Figure 4.— Length-class frequencies of larvae and juvenile northern anchovies for
each month of the study.
888
McGOWAN: SPAWNING OF NORTHERN ANCHOVY
OCTOBER 1978
APRIL 1979
CHANNEL N=97
10 15 20 25 30
STANDARD LENGTH CLASS (mm)
35
Figure 5.— Length-class frequencies of larvae and juvenile northern anchovies for October 1978 and April 1979 showing
the different sizes caught in the channel versus those in shallow water.
(Smith and Lasker 1978). The northern subpopula-
tion spawns off Oregon and Washington from mid-
June to mid-August when 1 m temperatures are
14°-17°C (Richardson 1980). These two subpopula-
tions overlap at San Francisco (Vrooman et al. 1981)
and the spawning season in the Bay overlapped the
spawning seasons of both subpopulations. But
spawning in the Bay took place at higher tempera-
tures than usual for either population in the ocean
(13°-18°C, Brewer 1976). Few eggs were taken in
the Bay from December 1978 to March 1979 when
water temperature was below 13°C. However, at
station 3 in March 1979, 477 eggs were taken at a
water temperature of 11.5°C. Peak spawning in the
Bay was in July, August, and September when the
mean water temperature was 19.0°, 19.8°, and
19.2°C, respectively. The highest catch of eggs oc-
curred at station 2 in July at 21.0°C. Eggs were also
plentiful at station 1 in August at 22.5° C. During
June, July, and August, eggs were least abundant
at stations 4 and 6, where water temperature was
relatively low. During September and October, egg
densities at stations 4 and 6 peaked, as did water
temperature at these stations. Sitts and Knight
(1979) found larvae shorter than 4 mm at 18°-22°C
in the Sacramento-San Joaquin estuary in July and
August. Although much of the northern anchovy
spawning took place in the Bay within the previously
reported temperature range and some took place at
low temperatures, most occurred in water warmer
than in the coastal spawning regions. The strong
correlation of egg abundance with temperature in-
cludes potential confounding effects of presumed
seasonal influx of adults, apparent "preference" for
spawning within the Bay, and differences in dilu-
tion due to tidal exchange which affected stations
4 and 6 more than the other stations. Therefore the
correlations are descriptive, perhaps predictive, but
not causal.
In the California Current, temperature, upwell-
ing, and stable stratification of the water column
are thought to interact to produce favorable condi-
tions for anchovy larvae (Lasker 1975). In San Fran-
cisco Bay there is no upwelling, but salinity or fresh-
water outflow variability might influence ecological
conditions. Freshwater flow may have an indirect
effect by promoting blooms of certain phytoplankton
or by retaining particles through estuarine circula-
tion (Cloern 1979). Relatively high salinity coincided
with warm temperatures at the beginning of the
spawning season, but spawning ceased in Novem-
ber when water temperature decreased to 13 °C,
although salinity remained high until February. Sitts
and Knight (1979) found larvae shorter than 10 mm
at low salinity (<10%o) and relatively high temper-
ature (>18°C). They found only large larvae (>10
mm) in November when water temperature fell
below 13°C.
In this study, only temperature had a strong direct
relationship with abundance of eggs and larvae;
889
FISHERY BULLETIN: VOL. 84, NO. 4
peak abundance tracked the seasonal temperature
cycle closely. Temperature stratification was most
pronounced in June-October when spawning was
greatest, especially at station 5 where salinity
stratification was also most noticeable.
Offshore transport of eggs and larvae is believed
to be one of the environmental hazards to anchovy
reproductive success (Bakun and Parrish 1982).
Peak spawning in the Bay took place in June-
August, the months of greatest offshore directed
Ekman transport at the latitude of San Francisco
(Parrish et al. 1981). Larvae, retained in San Fran-
cisco Bay by estuarine circulation or behavior, would
not be subject to offshore drift into areas of low
plankton density. Therefore, they may have a higher
probability of survival than larvae in the California
Current and they might survive during bad years
for oceanic larvae.
Within San Francisco Bay there were apparent
differences between spawning habitat and larval
habitat. Eggs and small larvae were more abundant
in warm, clear, thermally stratified water with
relatively less plankton; large larvae were found in
shallow, warm, less stratified, plankton-rich water
with reduced light penetration. Negative correla-
tions between zooplankton and the eggs of zooplank-
tivorous fishes were attributed to predation on the
zooplankton by de Ciechomski and Sanchez (1983).
Cannibalism on larvae by adult northern anchovies
and competition between adults and juveniles are
two reasons why separate habitats would be adap-
tive. Because spawning and nursery habitats differ
in location and environmental properties, it is not
surprising that multiple regression variables mea-
sured in the spawning habitat did not predict lar-
val abundance. It may be that spawning areas are
selected by adults, perhaps for feeding (Brewer
1978) or for water clarity, while larger larvae seek
different conditions where their survival is deter-
mined by other factors than those which affect first-
feeding larvae. If variable mortality on the larger
larvae determines eventual recruitment, then
recruitment may be largely decoupled from spawn-
ing and first-feeding conditions. This could explain
why predictions of recruitment from larval surveys
(which do not adequately sample large larvae and
juveniles) have not been reliable.
The conditions where larvae were more abundant
are more characteristic of shallow nearshore water
than of the California Current. Juveniles and young
of the year are also relatively more abundant near-
shore in California (Parrish et al. 1986). In 1978,
when spawning was restricted to nearshore areas,
apparent recruitment was high relative to 1979
when spawning was offshore (Hewitt and Methot
1982). The 1978 spawning season for California Cur-
rent anchovy was not typical; storms prevented
favorable conditions for larvae until March in south-
ern California (Lasker 1981). Nearshore areas might
be refugia during anomalous years and they could
contribute a disproportionate number of recruits
every year (Brewer and Smith 1982).
It might be argued that the 20-30 mm larvae found
nearshore in the Southern California Bight (Brewer
and Smith 1982) merely avoided the nets in stan-
dard CalCOFI tows, but I found a similar pattern
with respect to length frequencies when comparing
samples taken in the channels and in shallow water
in San Francisco Bay. That is, larger larvae were
found in shallower zooplankton-rich areas. Estuaries
and nearshore areas may provide conditions favor-
able enough for survival of larvae and juveniles to
compensate for low mean food density and for occa-
sional years of unfavorable oceanographic conditions
in the California Current.
San Francisco Bay northern anchovy larvae,
especially those which overwinter, are subject to dif-
ferent ecological conditions than those in the Califor-
nia Current, thus they may have slightly different
morphology and meristics (Hempel and Blaxter
1961; Blaber et al. 1981). The San Francisco Bay
subspecies Engraulis mordax nanus Hubbs (1925)
may be an ecotype of E. mordax.
A female northern anchovy has enough energy
stored as fat for 17 of its 20 annual batches of eggs,
but protein for egg production must come from
feeding during the spawning season (Hunter and
Dorr 1982). The primary food of northern anchovy,
zooplankton, was abundant in the Bay. I found a
mean density of 1 zooplankter/L with a 0.308 mm
mesh net, but this is an underestimate of cope-
podites and small copepods because of the relative-
ly large mesh size. By comparison, Hutchinson
(1981) found at least order of magnitude greater
densities at nearby stations over the same time
period using 0.080 and 0.064 mm mesh nets. An-
chovy feed by biting individual organisms or by
filter-feeding if particle density is high enough. The
laboratory-determined threshold for filter-feeding
is 5-18 particles (0.236 mm wide) per liter (Hunter
and Dorr 1982). My zooplankton density estimate,
which was biased conservatively, is of the order of
magnitude required to stimulate filter-feeding.
Therefore, I conclude that zooplankton prey for
adult northern anchovies were abundant in the Bay
during this study.
For the Bay to be a good larval nursery area it
should have abundant microzooplankton prey for lar-
890
McGOWAN: SPAWNING OF NORTHERN ANCHOVY
vae. I found a mean density of 28.8 per liter using
a 0.080 mm mesh net (probably a conservative esti-
mate because of net clogging and meter malfunc-
tioning). This is higher than would be expected in
the California Current using the same mesh size (<1
per liter, Arthur 1977). It is comparable to the 36
per liter found with a finer mesh net (Arthur 1977).
It is an underestimate of available prey for larvae
because they consume particles as small as 0.040
mm, and there is a peak of biomass of small plankton
in the California Current at 0.070 mm (Arthur 1977),
just below the mesh size of my net. Sitts and Knight
(1979) found a mean density of 32.3 copepod nau-
plii/L in a 1-yr study in the Sacramento-San Joaquin
estuary using 0.060 mm mesh. Hutchinson (1981)
found approximately 10 nauplii/L over the same
period of time as this study. (I calculated this value
from her data for density of nauplii at 1 m depth
at her stations 19 and 30 which correspond to my
stations 6 and 2.) My microzooplankton estimates
did not adequately represent the rotifers, tintinnids,
and other small larval prey which were collected in
high numbers with finer mesh nets (Hutchinson
1981). These organisms are known to be eaten by
northern anchovy larvae and I observed tintinnids
in the guts of some larvae.
Larvae reared in the laboratory generally require
more than 1,000 prey items/L for good survival, but
some survival occurs at lower densities. Houde
(1978) obtained 1% survival to metamorphosis of
Anchoa mitchilli with a prey density of 27 per liter.
Northern anchovy larvae in the sea which obtain
enough food to survive also obtain enough to grow
rapidly (Methot and Kramer 1979). The existence
of dense patches of food has been suggested to ac-
count for the discrepancy between average food den-
sities observed in the sea and those needed in the
laboratory. Dense patches of larval prey might not
be needed in the Bay where I found mean prey den-
sity higher than that typical of the California Cur-
rent. However, dense patches of microzooplankton
would be expected in the Bay because blooms of
their prey, phytoplankton, occur (Cloern 1982).
Dense patches of microzooplankton, undetected by
my sampling design, would make San Francisco Bay
a very good feeding area for larval northern an-
chovies. Because the water was warmer in the Bay
than in the California Current, larvae could search
a larger volume of water per unit time, they would
encounter high densities of prey and would be ex-
pected to survive in greater numbers and to grow
rapidly. Therefore, San Francisco Bay may be a
good feeding area for larvae as well as for spawn-
ing adults.
To my knowledge, my estimates of spawning bio-
mass of northern anchovies in the Bay are the first
such estimates. Are they reasonable, and what are
the implications of this biomass of anchovies in the
Bay? The estimate based on egg abundance assumes
that parameters estimated for California Current
anchovies apply to San Francisco Bay anchovies. I
argue they do because parameters for the estimate
were obtained from anchovies at the peak of spawn-
ing in the California Current in 1978, the year my
study began. I believe these parameter values may
be applied to the anchovy population in San Fran-
cisco Bay because the seasonal pattern of spawn-
ing and abundance of anchovies in the Bay indicates
that most of these anchovies are seasonal migrants
from the California Current stocks. No actual mea-
surements of batch fecundity of anchovy in the Bay
have been taken so the values used are the best
available. Errors in estimating egg and larval abun-
dances are probably more important than small
changes in the estimates of batch fecundity. The
egg-based estimate could be high if adults leave the
Bay immediately after spawning or if they spawn
more frequently due to greater food availability. The
estimate could be low if they spawn infrequently
because the season is later than the regular spawn-
ing season in the California Current or if higher
temperatures greatly increase metabolic needs.
The estimate is conservatively biased because I
merely divided the number of eggs caught by the
number of days to hatch at the measured tempera-
ture without considering mortality. During the
months with peak egg abundance the estimated time
to hatch was 2 d. If egg mortality was 0.184 da-1
(Picquelle and Hewitt 1984), then the estimate was
approximately 25% low. The estimate would be high
if eggs were present only in the channel and not over
the area used to calculate total abundance. However,
station 3, in shallow water near San Bruno Shoal
in South San Francisco Bay, had high egg densities;
therefore, eggs were distributed in some shallow-
water areas. Stations 1 and 2, which had high egg
densities, represented small areas, while stations 4
and 6 with low densities represented large areas.
San Pablo Bay and the rest of the North Bay were
not included in the biomass estimate. Potential
biases in the egg-based stock estimate either cancel
one another or give a conservative estimate.
My estimate is consistent with information from
other studies. I found mean values of 3,360 eggs/
1,000 m3 and 259 larvae/1,000 m3. Hutchinson
(1981) found 4,730 eggs/1,000 m3 (my calculations
from her stations 19 and 30). Sitts and Knight (1979)
calculated a mean larval abundance of 490 per 1,000
891
FISHERY BULLETIN: VOL. 84, NO. 4
m3. The estimates of larval densities are similar to
estimates for the Southern California Bight near-
shore CalCOFI area in 1978-79 (461 per 1,000 m3,
calculated from table 4 of Brewer and Smith 1982,
assuming average tow depth = 210 m; two-thirds
of the stations were >210 m according to their table
2). The mean density of eggs in the Bay was much
higher than in the Southern California Bight near-
shore CalCOFI area (310 per 1,000 m3, Brewer and
Smith 1982). The seasonal northern anchovies fish-
ery in the Bay took approximately 481 tons for
frozen and live bait (Smith and Kato 1979). My esti-
mate is adequate to permit such a yield.
Northern anchovy females need a daily ration of
4-5% of their body weight of copepods per day to
support growth and reproduction (Hunter and
Leong 1981). Approximately 5% of caloric intake
goes into growth. Using these values, 38.35 tons of
copepods per day would be consumed by the July
biomass of 767 tons of anchovies. Growth would be
about 1.92 tons per day. Doing similar calculations
for each month and summing for the 12 mo of this
study result in an estimate of 3,260 tons of cope-
pods consumed and a net annual production of 158
tons of anchovy growth. If the egg estimates based
on the area of the Bay, including the shallow areas
were used, the consumption of copepods and growth
estimates would be approximately doubled. These
calculations are a first order estimate of the impact
of a carnivorous planktivore on zooplankton in the
Bay. The energy converted to anchovy growth
would be removed from the Bay, so the estimate of
net growth is also a minimum estimate of a sink for
Bay production as growth of a transient consumer.
In San Francisco Bay where plankton production
from a limited area is being consumed by a large,
transient anchovy population, grazing by anchovy
could conceivably limit zooplankton abundance
seasonally. Although it is impossible to distinguish
between grazing and interannual differences with-
out estimates of zooplankton production, zooplank-
ton was more abundant in winter 1978-79 when
adult anchovies were absent.
A large biomass of planktivores could have other
effects on the ecology of the Bay. Selective feeding
by clupeoids on larger organisms in lakes can affect
the zooplankton community structure (Brooks and
Dodson 1965). Northern anchovy schools can also
have an impact on nutrient cycling. Smith and Epley
(1982) calculated that ambient ammonium concen-
tration would be nearly doubled behind an anchovy
school in the Southern California Bight. McCarthy
and Whitledge (1972) estimated that nitrogen excre-
tion by the Peruvian anchoveta is an order of mag-
nitude greater than zooplankton excretion, so fish
excretion may be the major source of regenerated
nitrogen nutrients for phytoplankton production.
These high nitrogen inputs would be patchy (Blax-
ter and Hunter 1982) and their importance would
depend on whether or not background levels of
nutrients were limiting. Nutrients may not be limit-
ing in San Francisco Bay where light penetration
and residence time control phytoplankton dynamics
(Cloern 1979). Laboratory studies of copepod pro-
ductivity, anchovy predation, and nutrient regenera-
tion are needed to define quantitatively the impact
of the northern anchovy on plankton dynamics in
the Bay. A complete description of the trophic role
of anchovy in the Bay should include estimates of
zooplankton consumption by larvae, cannibalism by
adults, and predation on adult and larval anchovies.
CONCLUSION
San Francisco Bay is a favorable area for north-
ern anchovy spawning because it has abundant food
for adults, protection from advective loss for eggs,
and abundant food for larvae. There is apparent
habitat partitioning between spawning adults and
larger larvae which could adaptively reduce preda-
tion and competition. Recruitment to the Califor-
nia Current stocks may be determined more by
events in the nursery habitat of larvae and juveniles
than by conditions favorable for spawning adults and
first-feeding larvae; therefore, further work in estu-
aries and nearshore areas is warranted.
ACKNOWLEDGMENTS
This study was done under the direction of Mar-
garet G. Bradbury as partial fulfillment of the re-
quirement for the M.A. in Biology at San Francisco
State University. I thank her and the other members
of my committee, Robert Berrend and Thomas
Niesen, for advice and assistance in completing the
work. Michael Hearne supplied the plankton net and
assisted in all the field sampling. The figures were
drafted by J. Javech. The preparation of the manu-
script was supported in part by the National Oceanic
and Atmospheric Administration under Cooperative
Agreement #NA 84-WC-H-06098.
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894
THE SPAWNING FREQUENCY OF SKIPJACK TUNA,
KATSUWONUS PEL AMIS, FROM THE SOUTH PACIFIC
J. Roe Hunter,1 Beverly J. Macewicz,1
and John R. Sibert2
ABSTRACT
Histological criteria to age postovulatory follicles were developed from examination of laboratory-spawned
skipjack tuna; the criteria were used to estimate the frequency of spawning of skipjack tuna from the
South Pacific. Examination of 87 skipjack tuna from field collections taken in October-November indicated
that spawning occurred nearly every day. The fraction of mature females with postovulatory follicles,
<24 hours old, was 0.85 (standard deviation = 0.071) indicating that the mean interval between spawn-
ings was only 1.18 days.
Estimates of the frequency of spawning of multi-
ple spawning fishes are essential for understanding
their reproductive biology. To estimate annual
reproductive effort or fecundity, and how these
variables are related to size or age structure of a
population requires knowledge of the frequency of
spawning and the number of eggs produced per
spawning. Batch fecundity, the number of eggs pro-
duced per spawning, has been estimated for skipjack
tuna a number of times (see review by Matsumoto
et al. 1984) but the spawning rate of the skipjack
is unknown. Thus spawning frequency is one of the
missing links in an assessment of the reproduction
of skipjack populations.
It has long been recognized that skipjack tuna
spawn more than once in a season because more
than one mode of advanced oocytes are found in
active ovaries (Brock 1954; Bunag 1956; Joseph
1963; Raju 1964; Simmons 1969; Batts 1972; Cayre
1981; Goldberg and Au 1986). The frequency of
occurrence of female black skipjack tuna, Euthyn-
nus lineatus, throughout the spawning season with
ovaries containing hydrated oocytes led Schaefer
(1986) to conclude that the average interval be-
tween spawnings of black skipjack in the eastern
tropical Pacific was 2.1-5.7 d depending on the
region.
Over the last 6 years, two methods have been
developed for measuring the spawning rate of multi-
ple spawning marine fishes: One method is based
on the frequency of ovaries containing hydrated
Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038.
2South Pacific Commission, P.O. Box D5, Noumea, CEDEX,
New Caledonia.
oocytes and the other is based on the frequency with
which they contain postovulatory follicles of known
age (Hunter and Macewicz 1985a). These methods
have been used to measure the rate of spawning in
a number of marine fishes: Engraulis mordax
(Hunter and Goldberg 1980; Hunter and Macewicz
1980); Engraulis ringens (Alheit et al. 1984); Hypso-
blennius jenkinsi (Present 1985); Sardinella brasi-
liensis (Isaac-Nahum et al. 1985); Seriphus politus
(DeMartini and Fountain 1981); and Euthynnus
lineatus (Schaefer 1986). Postovulatory follicles
were used in most studies, but DeMartini and Foun-
tain (1981) and Schaefer (1986) used the incidence
of females with hydrated oocytes to estimate spawn-
ing frequency. The hydrated oocyte method may
produce a biased estimate in some species because
of increased vulnerability of hydrated females to net-
ting gear (Alheit et al. 1984).
The objective of this paper was to estimate the
spawning rate of South Pacific skipjack tuna by
applying some of these techniques. It was not possi-
ble to use the hydrated ovary method in our study
because fish were not caught during the period of
the day when the ovary was hydrated. Instead, we
used the incidence of females having ovaries con-
taining postovulatory follicles to estimate the fre-
quency of spawning of skipjack tuna. This method
requires ovaries to be preserved immediately in for-
maldehyde solution when the fish is caught, a
histological examination of the ovary, and the devel-
opment of a staging system for estimating the age
of the postovulatory follicle. Our histological classi-
fication included not only an assessment of spawn-
ing frequency but also an assessment of the extent
of ovarian atresia. The atretic condition of the ovary
is a sensitive index of the reproductive state of
Manuscript accepted June 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
895
FISHERY BULLETIN: VOL. 84, NO. 4
females during the spawning season and can be used
to identify females approaching the end of their
spawning season as well as those in postspawning
condition (Hunter and Macewicz 1985b).
METHODS
Skipjack tuna were captured either by pole and
line or were catches associated with moored fish at-
traction devices or free floating natural flotsam.
Two sets of collections of skipjack tuna were ana-
lyzed: a group of 12 females taken near Noumea,
New Caledonia on 23 February 1984; and a group
of 87 females taken in 8 different collections at
various locations in the South Pacific from 20 Octo-
ber to 30 November 1984 (Table 1). Our samples
were opportunistically taken and spanned a great
latitudinal range (0°-23°S). At present the peak
spawning months of skipjack tuna are poorly defined
over this range of latitudes. Spawning is known to
occur throughout the year in some areas (Nishikawa
et al. 1985), but regional differences may exist in
the peak months of spawning, and the spawning
season also varies with skipjack size (Naganuma
1979). Naganuma concluded from analysis of gono-
somatic indices (GSI) that peak spawning period for
small skipjack tuna (40-60 cm) in the South Pacific
is October to December. Argue et al. (1983) ex-
amined 11,000 adult skipjack tuna for cannibalism
of juveniles (15-70 mm) and for GSI over the same
latitude range as this study, but covering 80° of
longitude (140°W-140°E). They found that canni-
balism and female GSI was highest between Octo-
ber and March in this broad area. More data are
needed to identify the regional variation about this
general pattern.
The 8 collections of gonads (collections 2-9, Table
Table 1 .—Characteristics of 9 collections of female skipjack tuna
taken in the South Pacific in 1984.
Collec-
Time of
Fork
length
tion
day
Mean
Range
Lat.*
Long.2
number
Date
(h)
N
(cm)
(cm)
Gear1
S
E
1
2-23-84
0800
12
47
44-51
PL
23.00 167.00
2
10-20-84
0745
7
49
46-50
PS
16.
178-179
3
10-23-84
0700
6
48
46-52
PS
16.
178-179
4
10-24-84
0700
8
49
46-52
PS
16.
178-179
5
10-25-84
0700
7
50
47-52
PS
16.
178-179
6
10-26-84
0700
14
49
45-51
PS
16.
178-179
7
10-27-84
0645
8
48
46-50
PS
16.
178-179
8
11-19-84
0755
25
50
44-62
PS
03.41
144.08
9
11-30-84
1955
12
56
49-60
PS
0.03 147.46
1) were treated statistically as 8 "clusters" of ran-
dom samples of unequal size. The mean proportion
of postovulatory follicles <24 h old was calculated
as the total number of females with such follicles
divided by the total number of mature females.
Cochran (1977) pointed out that estimation of vari-
ance by the simple binomial probability formula can
produce serious errors. The variance was calculated
by the appropriate formula recommended by Coch-
ran (1977).
Three female skipjack tuna were spawned in cap-
tivity (23°-24°C; June 1985) at the Kewalo Research
Facility of the National Marine Fisheries Service
using the stress spawning technique of Kaya et al.
(1982). One fish (48 cm fork length [FL]) was
sacrificed at the time of spawning, another (43.8 cm
FL) 12 h later and the third (44 cm FL) 24 h after
spawning. The ovaries of these females were used
to establish histological criteria for the aging of
the postovulatory follicles of the sea-caught
females.
Ovaries were preserved in 10% Formalin3 and
embedded in Paraplast. Histological sections were
cut at 5-6 /^m and stained with Harris hematox-
ylin followed by eosin-phloxine-B counter stain
(H&E).
Histological Classification
To estimate reproductive condition of skipjack
tuna, we used two histological classification systems:
one for estimating spawning frequency and the
other for assessing the likelihood that a female will
continue to spawn (atretic state of the ovary). Each
ovary was classified histologically according to both
systems. These classification systems were devel-
oped for northern anchovy, Engraulis mordax, by
Hunter and Goldberg (1980) and Hunter and
Macewicz (1980, 1985a, b) and are used here with
a few modifications appropriate to skipjack tuna
ovarian structure and their rates of postovulatory
follicle resorption. The descriptions of postovulatory
follicles of different ages are from the three captive
Hawaiian skipjack tuna. As these fish resorbed their
postovulatory follicles much more rapidly than did
the northern anchovy, we used stages of shorter
duration. The atretic classification system remains
unchanged, except for a few minor details of histo-
logical structure based on our observations of sea-
caught fish. We believe that the reproductive inter-
pretations we associate with the atretic classes are
PL = pole and line; PS = purse seine catch of skipjack tuna attracted
to either a fish attraction device moored in waters of 350-450 m deep or natural
flotsam.
Latitude and longitude given in degrees and minutes when available.
3Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
896
HUNTER ET AL.: SPAWNING FREQUENCY OF SKIPJACK TUNA
meaningful because the oocyte resorption seems to
follow a similar sequence of stages in most teleosts
(Bretschneider and Duyvene de Wit 1947; Lambert
1970). The rate a skipjack tuna ovary passes from
one atretic state to another is not specified and
would require an additional study of captive fish.
The characteristics of the two classification systems
are outlined below.
Spawning Frequency
Hydrated and Migratory Nucleus Stages
Ovaries with many translucent hydrated oocytes
(oocytes enlarged by fluid uptake just prior to ovula-
tion) are classified in the hydrated stage. Spawn-
ing is considered to be imminent. In northern an-
chovy, spawning takes place in <12 h after the onset
of hydration. No skipjack tuna with hydrated
oocytes were taken in our field collections. Female
skipjack tuna were taken with ovaries in the migra-
tory nucleus stage. This stage occurs just before the
onset of hydration and is characterized by the migra-
tion of the nucleus to the animal pole of the oocyte
and the beginning of the fusion of its yolk globules
(Fig. 1).
Age 0-H Postovulatory Follicles
Ovaries with new postovulatory follicles with no
signs of follicle degeneration are classed as age 0-h
postovulatory follicles. Hydrated oocytes may occa-
sionally be present. Estimated elapsed time from
spawning is 0-2 h. No skipjack tuna taken at sea
were in this stage, but from the laboratory speci-
men (Fig. 2a, b) we can discern the following histo-
logical characteristics: The new postovulatory
follicle has an irregular, convoluted shape. The
granulosa epithelial cell layer of the follicle appears
as an irregularly looped cord of slightly hypertro-
phied cuboidal cells with prominent healthy nuclei
linearly arranged. The granulosa appears only loose-
ly attached to the thecal connective tissue layer.
Although the theca is less convoluted than the gran-
ulosa layer, it is distinct, contains blood capillaries
and appears thicker than the thecal layer seen in
northern anchovy.
Figure 1.— Skipjack tuna oocyte with migratory nucleus (n) and
large oil droplet (o); bar = 0.1 mm.
Age 12-H Postovulatory Follicles
Twelve-hour-old postovulatory follicles (Fig. 2c,
d) show signs of degeneration similar to that ob-
served in northern anchovy after about 24 h. Histo-
logical characteristics include the follicle which is
smaller with fewer convolutions; a lumen which is
evident; the degenerating granulosa which is no
longer a recognizable unbroken cord of cells, but
rather the cells are scattered in clumps in the lumen
or may be irregularly attached to the theca; and
some pycnotic or irregular nuclei which are evident.
The theca has begun to disintegrate although it still
remains thick and distinct. Deterioration of the
theca is indicated by its overall smaller size, a more
filamentous rather than cohesize cellular arrange-
ment, and some irregular nuclei.
Age 24-H Postovulatory Follicles
Ovaries containing 24-h-old postovulatory follicles
showed pronounced signs of degeneration similar
to that observed in northern anchovy 48 h after
spawning. At this stage the follicle is much smaller
than that at 12 h but a lumen is still evident (Fig.
2e, f). Only few granulosa cells remain; they usual-
ly have pycnotic nuclei and generally are loosely at-
tached to the thecal layer. The thecal layer is still
fairly thick although it contains some pycnotic
897
FISHERY BULLETIN: VOL. 84, NO. 4
Figure 2.— Degeneration of postovulatory follicles of skipjack tuna spawned in the laboratory. Arrow in left panel indicates the
postovulatory follicle that is seen under a higher magnification in right panel, a and b, 0 h after spawning (no deterioration); c and
d, 12 h after spawning (pronounced degeneration); and e and f, 24 h after spawning (little remains of the degenerating postovulatory
follicle). Bar = 0.1 mm; g = granulosa epithelial cell layer; t = thecal cell layer; b = red blood cell(s); and a = early alpha stage atretic
oocytes.
898
HUNTER ET AL.: SPAWNING FREQUENCY OF SKIPJACK TUNA
nuclei, and lymphocytes, and has a more filamen-
tous composition.
Nonspawning (mature)
Ovaries with many yolked oocytes and containing
no hydrated oocytes or postovulatory follicles were
classified as nonspawning. They may contain post-
ovulatory follicles in advanced stages of degenera-
tion which cannot be readily distinguished from late
stage corpora atretica. Elapsed time from spawn-
ing was more than 24 h. Also classified as nonspawn-
ing (mature) were females in postspawning condi-
tion. The ovaries of such females contained no
yolked oocytes, but atretic follicles (beta stage) were
present indicating that the ovary was active recently
(see next section).
Immature
Ovaries containing no yolked oocytes and no a
or ft stage atretic structures were classed as im-
mature.
Atretic States
It is well known in seasonal spawning fishes that
a low incidence of atresia (resorption of the oocyte
and its follicle) occurs throughout the spawning
season, but it becomes marked as the spawning
season closes and the remaining advanced oocytes
in the ovary are resorbed. During the initial atretic
phase (a), the oocyte is resorbed and any yolk
globules are broken down and resorbed by the
hypertrophying granulosa cells of the follicle (Bret-
schneider and Duyvene de Wit 1947; Lambert 1970).
In the next stage (/?), all the yolk is gone, and there
remains a small, rather compact structure with one
or more cavities. The structure is composed of
granulosa and theca cells with penetrating blood
vessels. Further stages of follicle resorption have
been described by the same authors, but the inci-
dence and extent of a and (5 stages have proven to
be the most useful in the classification of atretic
states of ovaries (Hunter and Macewicz 1985b). The
characteristics of a and p atretic structures are
described and illustrated for northern anchovy by
Hunter and Macewicz (1985b) and a atretic oocytes
of skipjack tuna are essentially similar. However,
P atresia differs from northern anchovy in contain-
ing numerous spherical vacuoles scattered through-
out the follicle. The vacuoles are the remnants of
the oil droplet which takes longer than yolk to resorb
and in H&E sections appear empty. Occasionally,
a large beta stage follicle may be seen in which the
granulosa and thecal cells have proliferated.
Listed below are the characteristics of the four
atretic states we used to classify skipjack tuna
ovaries along with what is known regarding the
spawning potential of northern anchovy classed in
these states.
Atretic State 0
Yolked oocytes present, with no a atresia of
yolked oocytes; p stage atresia may be present, but
it cannot be distinguished with certainty from late
stage postovulatory follicles (>24 h old). Female
northern anchovy in this state have a high poten-
tial of spawning.
Atretic State 1
Less than 50% of the yolked oocytes are in the
a stage of atresia. The frequency of spawning for
northern anchovy classed in this state is less than
half of that for females classed in atretic state 0.
Thus, atretic state 1 indicates a decline in spawn-
ing rate.
Atretic State 2
Fifty percent or more of the yolked oocytes are
in the a stage of atresia. The frequency of spawn-
ing for female northern anchovy classed in this state
is very low and indicates that cessation of spawn-
ing is imminent.
Atretic State 3
Ovaries contain p stage atresia and no yolked
oocytes. Such fish have completed their spawning
season since they have no yolked oocytes. The pres-
ence of p stage atresia indicates that oocyte resorp-
tion has taken place and thereby distinguishes such
recently mature but postspawning fish from imma-
ture females. In northern anchovy, atretic state 3
may persist for 30 d.
RESULTS AND DISCUSSION
All postovulatory follicles in sea-caught skipjack
were less degenerated than those observed in a
laboratory specimen examined 24 h after spawning,
indicating that all of those in the sea collections were
<24 h old. The fraction of mature females with post-
ovulatory follicles <24 h old ([55 + 18J/86, Table 2)
was 0.85 with the standard deviation estimated to
899
FISHERY BULLETIN: VOL. 84, NO. 4
Table 2.— Numbers of female skipjack tuna in various spawning
and atretic states. The 8 collections taken in the South Pacific
between 20 October and 30 November 1984.
Age (A)
Postovulatory
Collec-
follicles
Total
tion
number
Atretic
state1
(n)
Non-
mature
A< 12 12 < A< 24
spawning
females
2
0
0
0
2
2
1
1
0
2
3
2
0
0
1
1
3
0
0
1
1
Total
1
0
6
7
3
0
1
0
1
2
1
4
0
0
4
2
0
0
0
0
3
0
0
0
0
Total
5
0
1
6
24
0
3
0
0
3
1
3
0
0
3
2
1
0
0
1
3
0
0
0
0
Total
7
0
0
7
5
0
3
0
0
3
1
2
0
0
2
2
1
1
0
2
3
0
0
0
0
Total
6
1
0
7
6
0
9
0
0
9
1
5
0
0
5
2
0
0
0
0
3
0
0
0
0
Total
14
0
0
14
7
0
3
0
0
3
1
5
0
0
5
2
0
0
0
0
3
0
0
0
0
Total
8
0
0
8
8
0
8
5
0
13
1
5
2
1
8
2
31
0
2
3
3
0
0
1
1
Total
14
7
4
25
9
0
0
44
52
6
1
0
66
0
6
2
0
0
0
0
3
0
0
0
0
Total
0
10
2
12
2-9
0
27
9
5
41
1
25
8
3
36
2
3
1
3
7
3
0
0
2
2
Total
55
18
13
86
'Atretic State 0
State 1
State 2
State 3
no alpha stage atresia of yolked oocytes.
alpha stage atresia of yolked oocytes present, but <50%
affected.
alpha stage atresia present, 50% or more yolked
oocytes affected.
no yolked oocytes present and beta stage atresia
present.
One female skipjack tuna in collection 4 was immature.
3A female with hydrated oocytes and age 0 h postovulatory follicles.
"Three of these females had oocytes in migratory nucleus stage.
5Two of these females had oocytes in migratory nucleus stage.
Five of these females had oocytes in migratory nucleus stage.
be 0.071 (Cochran 1977; see methods). This means
that the average interval between spawnings
(1/0.85) was only 1.18 d. Only one female was imma-
ture, reducing the denominator for the above frac-
tion spawning from 87 to 86. If we consider only
those females with yolked oocytes and no or minor
atresia (atretic states 0 and 1) the fraction spawn-
ing is 0.90, implying a mean interval of 1.11 d
between spawnings. This indicates that the spawn-
ing rate of female skipjack tuna in prime reproduc-
tive condition is very close to daily.
High levels of ovarian atresia were much more
common among the 12 females taken in February
than those taken in October-November, indicating
that the February fish were nearing the end of their
spawning season. Females with highly atretic
ovaries (state 2) and postspawning ovaries (state 3)
constituted 66% of the fish in the February collec-
tions (Table 3), but they made up only 10% of the
fish taken in October-November. The February col-
lection was the only one taken by pole and line. It
is possible that pole-and-line fishing may be selec-
tive against spawning fish (Iverson et al. 1970;
Matsumoto et al. 1984) although some spawning fish
were taken in this collection.
The most unusual feature of the February collec-
tion was that the spawning fraction was high, 0.25
for a group where 50% of the fish were in post-
spawning condition, had no yolked oocytes, and
were incapable of spawning (atretic state 3). The
spawning fraction was 1.0 for the three females with
no or minor atresia because all three had postovula-
tory follicles. Thus skipjack tuna with active ovaries
appear to spawn nearly every day. It appears that
those unable to maintain this rate may discontinue
spawning and resorb the ovary because females with
active ovaries, showing no evidence of spawning,
were rare in all collections. Postspawning females
Table 3. — Numbers of female skipjack tuna in various spawning
and atretic states. This single collection was taken 23 February
1984.
Collec-
tion
number
Atretic
state1
Postovulatory
follicles
12 h
24 h
Non-
spawning
Total
mature
females
1
0
1
2
3
Total
0
0
0
0
0
0
1
2
6
9
2
2
2
6
12
'Atretic State 0 = no alpha stage atresia of yolked oocytes.
State 1 = alpha stage atresia of yolked oocytes present, but <50%
affected.
State 2 = alpha stage atresia present, 50% or more yolked
oocytes affected.
State 3 = no yolked oocytes present and beta stage atresia
present.
900
HUNTER ET AL.: SPAWNING FREQUENCY OF SKIPJACK TUNA
might reactivate their ovary sometime later in the
year if their physiological condition favored repro-
duction. Evidence for northern anchovy indicates
that the transitions from spawning to postspawn-
ing states and vice versa can occur rapidly. In the
laboratory at 16 °C, northern anchovy can resorb all
advanced oocytes within a few weeks (Hunter and
Macewicz 1985b) and can produce an active ovary
in 30 d (Hunter and Leong 1981). Owing to the
higher water temperatures and high metabolism of
skipjack tuna they are probably capable of even
faster reproductive cycling.
Histological examination of females taken late in
the day (1955 h, collection 9) provided additional
evidence for daily spawning. Eight of 10 females
with postovulatory follicles in this collection also had
oocytes in the migratory nucleus stage. This stage
is the precursor to hydration. Thus, fish which had
spawned <24 h before were beginning to hydrate
a new batch of eggs which presumably would be
spawned in <12 h. The migratory nucleus stage was
observed only in this collection probably because it
was the only one taken in the evening, whereas all
others were taken in the morning (0645-0755). The
rarity of females with hydrated oocytes in our col-
lections and the age of the postovulatory follicles
imply that spawning usually took place at night.
Spawning in daylight hours has been observed by
fishermen and scientists, however (Iverson et al.
1970; Matsumoto et al. 1984).
A single female taken during the morning (collec-
tion 8) had small (0.70 mm) early stage hydrated
oocytes (hydrated oocytes in which the yolk globules
had not fully fused). This female, the only one with
hydrated oocytes in our collections, also had new
postovulatory follicles despite the fact that the
hydrated oocytes were not fully advanced. This
female may have been induced to hydrate and spawn
by the stress of capture or may be simply an excep-
tion to the rule. To capture significant numbers of
females with hydrated oocytes would probably re-
quire sampling after 2100 h. It is important to cap-
ture eventually some females in the hydrated stage
because it is the best way to confirm that all oocytes
in the most advanced modal group, the group of
oocytes considered to be the next spawning batch
(Hunter and Goldberg 1980), are in fact spawned.
Counts of hydrated eggs are also the easiest and
most accurate method of estimating batch fecundity
(Hunter et al. 1985).
The "stress" spawning technique of Kaya et al.
(1982) was used to produce the spawned skipjack
tuna for the aging of postovulatory follicles. In this
technique females captured at sea and placed in a
tank spawn spontaneously, usually about 8 h after
capture presumably because of the stress of capture
and handling. Spawning typically takes place at
about 2400 h, which, by our estimate, appears to be
close to the usual time of spawning. It now seems
likely that many of these fish are naturally express-
ing their daily spawning activity. On the other hand,
eggs less than the normal size range, 0.8-1.17 mm
(Matsumoto et al. 1984), are occasionally spawned,
indicating that stress may induce premature hydra-
tion in some individuals. That the skipjack tuna do
not continue to spawn in the tanks is due probably
to the stress of captivity. Our examination of a cap-
tive skipjack 24 h after spawning indicated that
nearly all remaining oocytes containing yolk were
in the early stages of alpha atresia (Fig. 2e). Similar-
ly, female northern anchovy nearly always resorb
their advanced oocytes a few days after capture
although they will subsequently mature and spawn
(Leong 1971; Hunter and Macewicz 1985b).
If female skipjack tuna spawn at the frequency
we observed (85% of the females per day), the cost
of reproduction and annual fecundity will be high
because skipjack tuna appear to have a long spawn-
ing season. The relative batch fecundity of skipjack
(number of eggs per spawning per body weight) is
about 100 eggs per gram (Matsumoto et al. 1984;
Goldberg and Au 1985). Skipjack tuna eggs are
about the same size as those of Scomber japonicus
which average in weight 0.04 mg (unpubl. data, Na-
tional Marine Fisheries Service, Southwest Fish-
eries Center). We estimate the cost of a single
spawning (excluding the metabolic cost of egg
maturation and reproductive behavior) to be about
2% of the body weight per spawning (Scomber egg
dry weight x relative batch fecundity x conversion
to wet weight; 4 x 10 ~5 x 100 x 5 = 0.02). If a
female spawned every 1.18 d over 3 mo (90 d), it
would produce about 7,600 eggs per gram body
weight at an average daily cost of 1.7% of the body
weight per day; a 4 kg skipjack tuna would spawn
about 30 million eggs over this period.
If the collections used in this study were an un-
biased sample of the South Pacific skipjack tuna
population, then little doubt exists that spawning
occurs almost daily when they have active ovaries.
This preliminary study provides the tools necessary
for a population-wide assessment of reproduction.
We established the time-specific, histological criteria
for assessment of spawning rate, and the method
was applied to a small sample. A great deal more
remains to be done for a proper assessment of
reproduction in skipjack tuna. Specifically, many
more samples at different times of day, using a
901
FISHERY BULLETIN: VOL. 84, NO. 4
variety of fishing gears, are needed to insure that
sampling biases do not exist; a wide range of skip-
jack tuna sizes or ages need to be sampled so that
the age-specific reproductive effort can be esti-
mated; and females with hydrated oocytes need to
be collected to verify that nearly all oocytes in the
most advanced mode are hydrated and spawned.
The last point seems particularly important because
our estimated body weight cost of reproduction is
high and is very sensitive to the estimate of batch
fecundity. It may never be practical to analyze histo-
logically sufficient numbers of specimens to estimate
spawning frequency for all months and ages since
some spawning occurs the year around (Nishikawa
et al. 1985). On the other hand, it may be practical
to calibrate the gonosomatic index (GSI) in peak
spawning months using histological criteria and to
use the GSI as a calibrated index of spawning fre-
quency during months of low spawning frequency.
We do not intend to continue this work but we en-
courage those working on the biology of tunas to
include such studies in their research plans.
ACKNOWLEDGMENTS
We thank the SWFC Honolulu Laboratory of the
National Marine Fisheries Service, and particular-
ly Christofer Boggs, for providing the samples of
recently spawned skipjack tuna from the Kewalo
Research Facility. We also thank Robert Gillett and
Richard Farman (South Pacific Commission) for col-
lecting the wild fish and Robert Kearney and Kurt
Schaefer (Inter- American Tropical Tuna Commis-
sion) for reading the manuscript.
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903
SURVIVAL AND GROWTH OF STRIPED BASS, MORONE SAXATILIS,
AND MORONE HYBRID LARVAE:
LABORATORY AND POND ENCLOSURE EXPERIMENTS1
Edward D. Houde2 and Lawrence Lubbers IIP
ABSTRACT
Survival and growth of striped bass, Morone saxatilis, and its hybrids were compared in the first 30
days after hatching to determine if the reported heterosis of hybrid striped bass is evident in the larval
stage. Larvae of striped bass (SB); striped bass x white bass (WBX), M. saxatilis 9 x M . chrysops or;
and striped bass x white perch (WPX), M. saxatilis 9x1, americana c, were reared under controlled
conditions in the laboratory (19°C, 3°/oo) and under ambient conditions in freshwater pond enclosures.
In the laboratory SB had a significantly higher mean survival rate at 30 days of age than either hybrid.
In the pond enclosures neither mean survival nor size at 30 days differed significantly among the types
of larvae. Mean rates of growth in length, which ranged from 0.28 to 0.36 mm d"1 in the laboratory
and from 0.30 to 0.32 mm d"1 in the enclosures did not differ significantly among the types of larvae.
Mean rates of growth in weight of 15.0 to 19.0% d"1 were not significantly different in the laboratory,
but the rates did differ significantly in the pond enclosures, where the WBX (17.9% d~ x) and WPX (17.3%
d"1) rates were significantly higher than the SB (15.5% d"1). If 30-day-old fry were to be reared in
hatcheries, there is no clear production advantage for hybrids. A possible initial expression of hybrid
vigor, recognized by faster rates of growth in weight, was evident in WBX and WPX at 1 month of
age in the pond enclosures but not in the laboratory tanks.
A series of recruitment failures (Cooper and Polgar
1981; Boreman and Austin 1985) has stimulated the
development of hatcheries to culture juvenile striped
bass, Morone saxatilis, or its hybrids for stocking
in the Chesapeake Bay region. The striped bass and
the striped bass x white bass, M. chrysops, hybrid
have been cultured for stocking in freshwater and
estuarine systems for several years and also have
potential for commercial aquaculture (Bonn et al.
1976; Kerby et al. 1983). A second hybrid, striped
bass x white perch, M. americana, has been pro-
duced (Bayless 1972; Kerby and Joseph 1979)
although its potential is less known. The striped bass
x white bass hybrid demonstrates an apparent
heterosis and usually grows and survives better dur-
ing the first two years of life than does striped bass
under similar culture conditions (Logan 1968; Ware
1975; Williams et al. 1981; Kerby et al. 1983).
'Contribution No. 1721, Center for Environmental and Estuarine
Studies of the University of Maryland.
2University of Maryland, Center for Environmental and Estu-
arine Studies, Chesapeake Biological Laboratory, Solomons, MD
20688-0038.
3University of Maryland, Center for Environmental and Estu-
arine Studies, Chesapeake Biological Laboratory, Solomons, MD;
present address: Maryland Department of Natural Resources,
Tidewater Administration, Tawes State Office Building, Annapolis,
MD 21401.
The objective of our experiments was to determine
if the apparent heterosis of the striped bass x white
bass hybrid is established in the larval stage,
between hatching and 30 d posthatch. We compared
growth and survival of striped bass, striped bass x
white bass, and striped bass x white perch (referred
to hereafter as "striped bass", "white bass hybrid",
and "white perch hybrid") in laboratory experiments
and in fine-mesh enclosures within hatchery ponds.
METHODS
Laboratory Experiments
Larvae originated from eggs of a single female
striped bass, 15.4 kg, gillnetted in the Patuxent
River, transported to the Manning Hatchery, Cedar-
ville, MD, on 24 April 1982 and spawned by injec-
tion of human chorionic gonadotropin on 27 April.
Sperm from 2 male striped bass (Patuxent River),
12 male white bass (Tennessee Fish Commission),
and 2 male white perch (Patuxent River) were used
to fertilize portions of the spawned eggs. Embryos
were incubated in 114 L polyethylene incubation
chambers and larvae were held there in 15°-16°C
freshwater until 6 d after hatching when some were
brought to the Chesapeake Biological Laboratory.
Manuscript accepted July 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
905
FISHERY BULLETIN: VOL. 84, NO. 4
Rearing Systems
The striped bass and hybrid larvae were reared
from 6 to 30 d after hatching in 36 L, rectangular
glass aquaria. Each aquarium was lighted by two
61 cm, 40-W fluorescent lights 25 cm overhead on
a 12-h light-12-h dark cycle. Immersion heaters con-
trolled the temperature. For additional control, the
aquaria sat in a shallow, refrigerated waterbath. An
airstone in each aquarium provided oxygen and kept
food dispersed.
Temperature was maintained at 19° ± 1°C. Salin-
ity was held at 3°/oo by diluting 5 ^m filtered Patux-
ent River water with well water. All larvae were
fed Artemia nauplii, eggs of which originated from
Shark Bay, Australia. Water quality was maintained
by replacing half of the water in each aquarium on
alternate days. Feces, dead Artemia, and dead lar-
vae were siphoned off each day. Ammonia levels
were checked on 13 May (16 d after hatching) and
were <0.25 ppm in all tanks. The pH in the nine rear-
ing tanks ranged from 8.0 to 8.4 on 11 May (14 d
after hatching) and from 8.3 to 8.4 on 26 May (29
d after hatching).
Food Levels, Larval Densities, and Sampling
Two Artemia nauplii levels, 100 L_1 and 500
Lr1, were tested. The lower level is similar to zoo-
plankton densities in Chesapeake Bay subestuaries
where striped bass larvae occur (Miller 1978). For
each of the larval types duplicate experiments were
run at the 500 L_1 level but only a single experi-
ment was run at 100 Lr1. Food was first offered at
6 d after hatching when the experiments started.
Artemia nauplii concentrations in each aquarium
were checked twice daily by counting the num-
ber in pipetted 100 cc aliquots. Food levels were
maintained and adjusted by adding suspensions
of Artemia of known concentration to the aquar-
ia.
In each aquarium, 144 larvae were stocked at an
initial, relatively low density of 4.0 Lr1. Some
larvae were preserved in 5% Formalin4 at the start
of experiments (6 d after hatching). Three or four
larvae from each aquarium were sampled and
preserved on days 8, 10, 13, 16, 19, and 25 for
growth rate determination. Samples (15-27 larvae)
of survivors were preserved at 30 d when ex-
periments were terminated. Preserved larvae were
4Reference to trade names does not imply endorsement by the
National Marine Fisheries Service.
measured and wet- weighed (nearest 0.1 mg after
blotting).
Analysis
The expected number of survivors in each experi-
ment is the number that would have survived had
no larvae been sampled and preserved during the
experiments. If Z = F + M, where Z is instanta-
neous total mortality and F is preservation mortal-
ity, then M is mortality from all other causes. The
expression Nt = N0 e~(F+M)t applies, where Nt is
number of survivors at age t (30 d) and N0 is initial
number of stocked larvae (144 at 6 d). Knowing N0,
Nt , Z, and F, we solved for M and then estimated
expected survivors, if no larvae had been preserved,
as N't = N0 e~m. Analysis of variance was used to
test for survival differences among types of larvae
and between food levels.
Lengths and weights of the three types of larvae
were compared at 6 d after hatching and when ex-
periments terminated. In addition, lengths and
weights at the 100 L_1 and 500 L_1 food levels
were compared to determine if food concentration
affected mean sizes. Comparisons were carried out
using analysis of variance followed by the SNK
multiple comparison test.
Growth in length was described by linear regres-
sions of standard length on days after hatching, lt
= a + bt, where lt is estimated length (mm) at age
t and b is daily growth rate (mm day-1). Growth in
weight was determined from the exponential regres-
sion of wet weight (mg) on days after hatching, Wt
= W0 eGt, where Wt is estimated weight at age t
and G is the instantaneous daily growth coefficient
(day-1). Percent daily weight gains were calculated
as 100 (eG - 1). Weight-length relationships were
obtained from the power function, W = aLb, where
Wis wet weight (mg), I is standard length (mm), and
a and b are coefficients from the fitted regression.
Enclosure Experiments
Cubic enclosures, 1.32 m on each side, open at the
top, and constructed of wood frames and 500 yon
Nitex mesh, were submerged to a depth of 1.12 m
in a 1-acre, freshwater pond of 1.5 m mean depth
at the Manning Hatchery. The nine enclosures, each
holding 2 m3, were placed in the pond from 3 to 5
d before larvae were stocked. Enclosures were
assigned to the striped bass and two hybrids using
a linearized Latin-square design (Steel and Torrie
1960) with three replicates for each type of larva.
The larvae were progeny of a single 10.4 kg female
906
HOUDE and LUBBERS: SURVIVAL AND GROWTH OF STRIPED BASS
striped bass from the Patuxent River. Sperm from
Patuxent River male striped bass were used to fer-
tilize eggs. The hybrids resulted from fertilization
by Tennessee white bass males and Patuxent River
white perch males.
Larvae were held in hatchery troughs and fed
Artemia nauplii from 6 to 8 d after hatching. A total
of 2,500 9-d-old larvae were stocked in each en-
closure on 12 May 1983. Larvae were sampled by
dipnet and preserved in 5% Formalin at 13, 17, 20,
23, and 27 d after hatching. At 30 d all survivors
from each enclosure were counted and samples pre-
served. Temperatures in the pond ranged from
18.5° to 22.0°C during the course of the experiment.
Pond Zooplankton
The kinds and abundances of potentially edible
zooplankton were sampled on each day that larvae
were collected, using a 15 cm diameter, 72 pm mesh
plankton net that was lifted vertically in each
enclosure. For comparison, zooplankton also was
collected in three vertical lifts of the net outside the
enclosures.
Analysis
Survival, lengths and weights at age, growth
rates, and weight-length relationships were cal-
culated as for the laboratory experiments. Variance,
covariance, and regression analyses were used to
test for differences in means among the striped bass
and two types of hybrid larvae.
RESULTS
Laboratory Experiments
Survival
Survival at 30 d after hatching ranged from 45.8
to 85.4% (Table 1). Mean percentage survivals were
striped bass, 84.7%; white bass hybrid, 60.4%; and
white perch hybrid, 73.1%. The mean expected
number of survivors differed significantly among
types of larvae (ANOVA, P < 0.05). Mean survival
of striped bass was significantly higher than that
of the white bass hybrids (SNK multiple comparison
procedure, P < 0.05). There were no detectable dif-
ferences in mean survival between the two Artemia
nauplii feeding levels (ANOVA, P > 0.05).
Size-at-Age
The white perch hybrid larvae were significantly
shorter and weighed less than either striped bass
or white bass hybrid larvae when the experiments
began at 6 d after hatching, before larvae had been
fed (Table 2; ANOVA, P < 0.05).
At 30 d after hatching there were some statistical-
ly significant differences in mean lengths and
weights among the three types of larvae, and be-
tween the two food levels, but no clear result was
obtained (Table 2). No significant differences among
mean lengths or weights of the white bass hybrid
larvae were detected between the 100 L_1 and 500
L_1 food levels. But, the striped bass and white
Table 1.— Survival at 30 d after hatching of striped bass (SB), striped bass x white bass (WBX),
and striped bass x white perch (WPX) larvae in laboratory experiments at two food levels.
Larvae
and
experiment
numbers
Artemia
concentration
(number L"1)
Number
preserved
Number
of
survivors
Expected
number1
of
survivors
Expected
instantaneous
daily mortality
rates (Z)
Expected
percentage
survival
SB-1
SB-2
SB-3
SB mean
WBX-1
WBX-2
WBX-3
WBX mean
WPX-1
WPX-2
WPX-3
WPX mean
500
500
100
500
500
100
500
500
100
20
106
123
0.0066
85.4
18
108
123
0.0066
85.4
19
104
122
0.0069
83.3
106.0
2122.0
0.0069
84.7
18
58
66
0.0325
45.8
20
93
108
0.0120
75.0
18
76
87
0.0210
60.4
75.7
87.0
0.0210
60.4
22
85
100
0.0152
69.4
18
100
114
0.0097
79.2
18
89
102
0.0144
70.8
91.3
105.3
0.0130
73.1
'Expected number of survivors is the adjusted number, accounting for samples of larvae that were preserved dur-
ing the experiment (see Methods).
2The SB mean differed significantly from the WBX and WPX means (Analysis of variance followed by SNK multiple
comparison procedure, P < 0.05).
907
FISHERY BULLETIN: VOL. 84, NO. 4
Table 2.— Mean standard lengths and wet weights of larvae of striped bass (SB), striped bass
x white bass (WBX), and striped bass x white perch (WPX) from specimens preserved at
6 d after hatching, immediately before the experiments began and at 30 d after hatching when
the experiments were terminated.
SIX DAYS
Mean length (mm)
Mean wet weight (mg)
and standard error
and standard
error
Number
Larvae
preserved
X
Sj
X
s*
SB
15
5.49
0.06
0.95
0.04
WBX
19
5.29
0.03
0.96
0.03
WPX
17
15.20
0.06
10.85
0.02
THIRTY DAYS
Mean wet i _
weiaht
Larvae
and
experiment
Artemia
concen-
tration
Number
Mean length (mm)
and standard error
(mg)
and standard error
number
(number L"1)
preserved
X
%
X
«*
SB-3
100
18
212.39
0.17
225.7
1.4
SB-1
500
20
314.26
0.17
"49.1
2.2
SB-2
500
19
314.57
0.17
450.4
1.8
SB mean
13.74
41.7
WBX-3
100
15
13.02
0.30
30.1
2.1
WBX-1
500
18
12.68
0.26
28.8
2.2
WBX-2
500
19
12.73
0.38
29.3
3.6
WBX mean
12.81
29.4
WPX-3
100
21
211.86
0.25
221.1
1.6
WPX-1
500
18
13.22
0.31
33.6
2.2
WPX-2
500
27
13.15
0.22
35.0
2.2
WPX mean
12.74
29.9
'Differ significantly, P < 0.05, from both SB and WBX. ANOVA followed by SNK multiple comparison
procedure.
2Differ significantly, P < 0.05, from the 500 L~1 means. ANOVA.
3Differ significantly, P < 0.05, from all WBX and WPX mean lengths. ANOVA followed by SNK multiple
comparison procedure.
"Differ significantly, P < 0.05, from all WBX and WPX mean weights. ANOVA followed by SNK multiple
comparison procedure.
perch hybrid larvae were longer and heavier at the
500 L"1 level (ANOVA, P < 0.05). At the 500 L"1
food level the striped bass were significantly heavier
than either hybrid (ANOVA and SNK multiple com-
parison procedure, P < 0.05). The mean lengths of
30-d-old striped bass at 500 L_1 food level were
significantly longer than the mean lengths of the
hybrids (Table 2) (ANOVA and SNK multiple com-
parison procedure, P < 0.05).
Growth Rates
From 6 to 30 d after hatching larvae grew in
length at mean rates ranging from 0.28 to 0.36 mm
d_1 (Table 3, Fig. 1). There were no significant dif-
ferences in the growth-in-length rates among the
three types of larvae at the 500 L_1 Artemia food
level.
The exponential regressions of mean weights on
age (Table 3, Fig. 2) gave instantaneous growth
coefficients ranging from 0.1396 to 0.1739 d_1,
equivalent to 15-19% d~: weight gains. None of the
coefficients differed significantly from each other
(ANCOVA, P > 0.50).
There were no significant differences in weight-
length relationships among types of larvae or be-
tween food levels (ANCOVA, P > 0.50). An average
relationship, based on the total regression compo-
nent of the ANCOVA, is W = 7.17 x 10 "4 J4-2399.
Enclosure Experiments
Survival
Survival of striped bass and hybrid larvae at 30
d after hatching ranged from 13.1 to 33.8% in the
nine enclosures. At 30 d there was no indication that
striped bass or either hybrid was superior in sur-
vival capability. The mean percentage survivals for
the three types of larvae ranged from 22.0 to 28.5%
(Table 4B) and did not differ significantly (ANOVA
on arcsin mean percent survivals). The mean over-
all survival rate for the three kinds of larvae was
25.0%.
908
HOUDE and LUBBERS: SURVIVAL AND GROWTH OF STRIPED BASS
Table 3.— Linear regressions describing growth in length and exponential
regressions describing growth in weight of striped bass (SB), striped bass x
white bass (WBX), and striped bass x white perch (WPX) during the period
6-30 d after hatching. In the linear regression, / is standard length in mm, t
equals days after hatching, b equals growth rate in mm, and a is the y-axis
intercept. In the exponential regressions, W is wet weight in mg, f equals days
after hatching, G is the instantaneous growth coefficient, and W0 is the
theoretical weight in mg at time zero.
Larvae and
experiment
number
Artemia
concentration
(number L~1)
LENGTH
Equation
/ = a + bt
Standard
error
of b
SB-3
100
V = 3.64 +
0.29f
0.01
0.99
SB-1
500
/ = 3.13 +
0.36f
0.02
0.99
SB-2
500
/ = 3.20 +
0.36r
0.01
0.99
WBX-3
100
/ = 3.10 +
0.34f
0.02
0.98
WBX-1
500
/ = 3.36 +
0.32f
0.01
0.99
WBX-2
500
/ = 3.31 +
0.32f
0.02
0.98
WPX-3
100
V = 3.70 +
0.28f
0.02
0.98
WPX-1
500
/ = 3.18 +
0.32r
0.01
0.99
WPX-2
500
/ = 3.22 +
WEIGHT
0.32f
0.01
0.99
Larvae and
Artemia
Equation
Standard
Percent
experiment
concentration
error
gain
number
(number L"1)
W = W0 eG'
of G
r2
(°/o d"1)
SB-3
100
W
= 0.51 e01472f
0.0158
0.94
15.9
SB-1
500
W
= 0.41 e01713'
0.0141
0.96
18.7
SB-2
500
W
= 0.42 e° 1739f
0.0146
0.96
19.0
WBX-3
100
W
= 0.41 e0158u
0.0147
0.95
17.1
WBX-1
500
w
= 0.41 e01576f
0.0145
0.95
17.1
WBX-2
500
w
= 0.31 e01645f
0.0154
0.95
17.9
WPX-3
100
w
= 0.48 e° 1396(
0.0123
0.96
15.0
WPX-1
500
w
= 0.33 e° 1625'
0.0073
0.96
17.6
WPX-2
500
w
= 0.35 e° 1520'
0.0091
0.98
16.4
'Differ significantly from SB-1 and SB-2, P< 0.01.
comparison procedure.
ANCOVA followed by SNK multiple
The mean instantaneous mortality rates during
the 9-30 d after hatching ranged from 0.0601 to
0.0713 d-\ equivalent to 5.8 to 6.9% d"1 (Table
4B). Cannibalism probably occurred during the last
10 d of the experiment. Some large survivors had
small larvae in their stomachs when the experiments
ended.
Size-at-Age
When larvae were stocked in the enclosures at 9
d after hatching, white bass hybrid larvae were
significantly heavier (ANOVA, P < 0.01) and slight-
ly, but not significantly, longer than white perch
hybrid and striped bass larvae (Table 4A). Because
all larvae had been fed Artemia nauplii in the hatch-
ery for 3 d prior to stocking it is not known if the
sizes at stocking reflect the relative weights and
lengths of the three kinds of larvae before they
began to feed.
At 30 d after hatching mean lengths of striped
bass and hybrid larvae from the enclosures ranged
from 12.58 to 12.96 mm SL (Table 4C). Mean wet
weights ranged from 38.38 to 43.28 mg (Table 4C).
There were no significant differences in mean
lengths or weights among the three types of larvae
or among the nine enclosures (ANOVA, P > 0.25).
Growth Rates
Mean rates of growth in length for the striped bass
and hybrid larvae ranged from 0.30 to 0.32 mm d_1
(Table 4D; Fig. 3). There were no significant differ-
ences in the rates among types of larvae or among
replicate enclosures (ANCOVA, P > 0.10).
The common, instantaneous rates of growth in
weight were 0.1444 for striped bass (= 15.5% d_1),
0.1650 for white bass hybrids (= 17.9% d"1) and
0.1593 for white perch hybrids (= 17.3% d"1). The
rates of growth (Table 4E; Fig. 4) differed signifi-
cantly among the three types of larvae (ANCOVA,
P < 0.05) but not among enclosures (P > 0.10). The
909
FISHERY BULLETIN: VOL. 84, NO. 4
13
11-
100 Artemia, liter" 1
E
E
o) 5
c ~^-
o
-J 15r
CO
■D
« 13r
CO
11
9
500 Artemia, liter-1
_i i i_
6 8 10 13 16 19 25
Days after Hatching
30
Figure 1.— Mean standard lengths +2 standard errors of striped bass
(SB), striped bass x white bass (WBX), and striped bass x white perch
(WPX) larvae from 6 to 30 d after hatching, reared at two food levels in
the laboratory.
white bass hybrid and white perch hybrid rates were
significantly higher than that for striped bass lar-
vae (SNK multiple comparison procedure, P <
0.05).
Weight-Length Relationships
The wet weight-standard length relationships dif-
fered significantly among the three types of larvae
(ANCOVA, P < 0.001). The power coefficient of the
white bass hybrid larvae was higher than those of
the striped bass and white perch hybrid larvae (SNK
multiple comparison test, P < 0.01) (Table 4F).
Pond Zooplankton
Copepod nauplii and adults (Diaptomus spp. and
other calanoid species) and cladocerans (Bosmina,
Scapholebris, Ceriodaphnia, and Daphnia) were
abundant in the pond and in the enclosures (Fig. 5).
The summed cladoceran and copepod densities
declined rapidly in the pond from >1,000 L_1,
when the larvae were stocked, to approximately 400
L_1 during the last 10 d of the experiment. Den-
sities within the enclosures declined from approx-
imately 1,000 L_1 at the time larvae were stocked
to 100 L_1 when the experiments ended.
Samples of 12-20 larvae of each type were ex-
amined for stomach contents on day 30. The small-
est larvae of each type had eaten cladocerans and
copepods. The largest individuals had eaten chirono-
mid larvae and zooplankton. Two of 20 individuals
of striped bass and white bass hybrids had eaten fish
larvae, proof that cannibalism was occurring.
DISCUSSION
Neither striped bass nor hybrid larvae, in the lab-
910
HOUDE and LUBBERS: SURVIVAL AND GROWTH OF STRIPED BASS
Table 4.— Summary of data and analyses from 2 m3 enclosure experiments in the Manning Hatchery pond, 1983. Three replicate
enclosures were run for each type of larva: Striped bass (SB), striped bass x white bass (WBX), and striped bass x white perch (WPX). A)
Mean standard lengths and wet weights at 9 d after hatching, prior to stocking in enclosures. B) Percent survivals at 30 d after hatch-
ing. C) Mean lengths and weights at 30 d after hatching. D) Growth-in-length equations (/, = standard length in mm at age f; f =
days after hatching; Sb = standard error of the regression coefficient; r2 = coefficient of determination). E) Exponential, growth-in-
weight equations (Wt = wet weight in mg at age f ; f = days after hatching; SG = standard error of the exponential coefficient; r2 =
coefficient of determination). F) Power function equations of the wet weight-standard length relationships (W = wet weight in mg; / =
standard length in mm; Sb = standard error of the power coefficient; r2 = coefficient of determination).
A.
Type of larva
n
Standard length
(mm)
Wet weight (mg)
x s5
D.
Type of larva
Equation
I, = a + bt
n
sb
X
s~x
r2
SB
13
6.12
0.06
1.15 0.08
SB
1, =
3.09 + 0.30f
253
0.0136
0.66
WBX
13
6.19
0.14
11.66 0.11
WBX
It =
3.22 + 0.31 f
245
0.0130
0.70
WPX
15
5.87
0.13
1.33 0.11
WPX
k =
2.96 + 0.32f
263
0.0100
0.79
B.
Type of larva
SB
Percent survival
x s*
22.1 3.4
Instantaneous
mortality
rate (d~1)
0.0713
E.
Type of larva
Equation
Wt = WQ eGt
n
sG
r2
SB
Wt
= 0.37 e° 1444'
253
0.0044
0.81
WBX
22.0
6.2
0.0695
WBX
2W,
= 0.26 e° 1650'
245
0.0041
0.87
WPX
28.5
2.1
0.0601
WPX
2Wt
= 0.30 e° 1593r
263
0.0037
0.88
C.
Type of larva
n
Standard length
(mm)
Wet weight (mg)
x s-x
F.
Type of larva
Equation
W = alb
n
sb
X
s*
r2
SB
78
12.58
0.24
38.38 3.57
SB
w
= 6.23 x in-4/.42879
253
0.0469
0.97
WBX
78
12.90
0.23
43.28 3.86
WBX
w
= 2.27 x 10"4L47114
245
0.0536
0.97
WPX
78
12.96
0.12
39.73 1.23
WPX
w
= 5.44 x 1(T4L43496
263
0.0512
0.97
'Significant at P < 0.05. ANOVA.
zThe WBX and WPX exponential coefficients differed significantly, P < 0.05, from the SB coefficient. ANCOVA followed by SNK multiple comparison procedure.
3The WBX power coefficient differed significantly, P < 0.05, from the SB and WPX coefficients. ANCOVA followed by SNK multiple comparison procedure.
oratory and in freshwater pond enclosures, demon-
strated clearly superior growth or survival. The
apparent heterosis in young-of-the-year and sub-
adult white bass hybrids (Logan 1968; Ware 1975;
Bonn et al. 1976; Williams et al. 1981; Kerby et al.
1983) was not evident during the first month after
hatching. Survival and growth rates of the three
types of larvae were relatively high in all of our ex-
periments, indicating that striped bass and its
hybrids may have near-equal production potential
up to 30 d of age.
Larvae grew and survived surprisingly well at the
relatively low food concentrations that we offered
in the laboratory. There was evidence that striped
bass and white perch hybrid larvae grew faster at
the 500 L_1 than at the 100 L_1 Artemia concen-
tration but there was no significant difference in size
of white bass hybrid larvae reared at those two food
levels. Survival of all three types of larvae did not
differ between the two food levels, demonstrating
that high survival and favorable growth can be ob-
Figure 2.— Mean wet weights ± 2 standard errors of striped bass (SB),
striped bass x white bass (WBX), and striped bass x white perch
(WPX) larvae from 6 to 30 d after hatching, reared at two food levels
in the laboratory.
E
J?
a>
"3
5
Days after Hatching
911
FISHERY BULLETIN: VOL. 84, NO. 4
14
12
E
£
c
o
10
CO
■a
| 8
W
50
© SB
a WBX
A WPX
I ±2 SE
9 13 17 20 23
Days after Hatching
27 30
Figure 3.— Mean standard lengths (±2 standard errors) of striped
bass (SB), striped bass x white bass (WBX), and striped bass x
white perch (WPX) larvae on seven dates in 2 m3 enclosure ex-
periments, Manning Hatchery pond.
tained for Morone larvae at low Artemia concentra-
tions, if those concentrations are maintained at the
nominal levels. Our laboratory survival rates at low
food levels were higher than those reported for
striped bass larvae in the literature (e.g., Doroshev
1970; Miller 1978; Rogers and Westin 1981; Eld-
ridge et al. 1981, 1982), which generally had in-
dicated that nominal Artemia concentrations nearly
an order of magnitude higher than 500 L_1 were
required to obtain high survival rates.
The laboratory and pond enclosure methods to
assess striped bass and hybrid larvae performance
differed in many respects and could have influenced
results. Besides great differences in enclosed vol-
umes (36 L vs. 2 m3), environmental factors and
foods differed. Laboratory experiments were run at
19.0 °C and 3%o salinity, because low salinities are
known to improve striped bass larvae survival (Bonn
et al. 1976; Kerby et al. 1983). Temperature in-
creased from 18.5° to 22.5°C in the Manning Hatch-
ery freshwater pond during the 3-wk experiment.
The laboratory-reared fish were fed only Artemia
nauplii at controlled concentrations while enclosure
fish had a variable zooplankton diet.
40
^ 30
E
x:
O)
"3
20
10
© SB
a WBX
a WPX
I ±2 SE
9 13 17 20 23
Days after Hatching
27 30
Figure 4.— Mean wet weights (±2 standard errors) of striped bass
(SB), striped bass x white bass (WBX), and striped bass x white
perch (WPX) larvae on seven dates in 2 m3 enclosure experiments,
Manning Hatchery pond.
Survival of all larvae was lower in the pond en-
closures than in the laboratory tanks (Tables 1, 4).
White bass hybrids had the lowest mean survival
rate in the laboratory but they survived as well as
striped bass and white perch hybrids in the pond
enclosures. At the relatively high 500 L_1 Artemia
level laboratory-reared striped bass larvae were
longer and heavier than either of the hybrids at 30
d after hatching. In the pond enclosures no signifi-
cant differences in mean lengths or weights among
the three types of larvae were detected at 30 d. The
weight-length relationship of pond enclosure, white
bass hybrid larvae had a relatively high exponen-
tial coefficient, indicating that they were heavier at
a given length than the other types of larvae. Mean
weights of both hybrids at 30 d were considerably
heavier in the pond enclosures than in the labora-
tory tanks. Relatively great size variability in the
912
HOUDE and LUBBERS: SURVIVAL AND GROWTH OF STRIPED BASS
Zooplankton Densities at Cedarville
Inside Enclosures
1000
17 20 23
Days after Hatching
Figure 5.— Mean densities of copepods and cladocerans inside and outside of
the 2 m3 enclosures used for striped bass and hybrid larvae experiments in the
Manning Hatchery pond.
enclosures may have resulted in part from canni-
balism and consumption of chironomids by some lar-
vae, promoting their relatively rapid growth.
Although mean weights and lengths of 30-d-old
striped bass and the two hybrids from the pond
enclosures did not differ, the instantaneous rate of
growth in weight of striped bass larvae was signifi-
cantly lower than that of either hybrid (Table 4E).
Had the enclosure experiments proceeded for a few
more days the hybrids would have attained larger
size than the striped bass. For example, at 35 d after
hatching the striped bass would have weighed 20
mg less than either hybrid. The heterotic effect may
begin to express itself at approximately 1 mo of age.
Alternatively, the freshwater environment, increas-
ing temperatures, and the prey available in the pond
may have selectively favored growth of hybrids dur-
ing the last few days of the experiment.
If 30-d-old fry are to be produced for stocking,
there is no apparent immediate advantage to rear
hybrids rather than striped bass. Our laboratory and
pond enclosure studies did not demonstrate advan-
tages in survival or production of hybrids. The pond
enclosure results did suggest that hybrids may begin
to achieve an advantage in growth rates just prior
to 1 mo of age. Important questions about compar-
ative energetics, nutrition, and genetics still remain
to be answered to understand the biology of larval
M. saxatilis or its hybrids and the consequences of
their possible release into natural systems such as
Chesapeake Bay.
ACKNOWLEDGMENTS
The research was supported by contracts F26-82-
003 and F31-83-008 from the Maryland Department
of Natural Resources, Tidewater Administration,
Tidal Fisheries Division. Assistance in the labora-
tory was provided by H. Hornick, W. Roosenburg,
and V. Saksena. Larvae were supplied by the Mary-
land DNR Manning Hatchery at Cedarville. The
assistance of DNR personnel, particularly M.
Beaven, H. King, and J. Stringer, is gratefully
acknowledged. We appreciate the critiques of early
913
drafts of the manuscript provided by E. J. Chesney,
H. King, J. Kraeuter, and L. C. Woods III.
LITERATURE CITED
Bayless, J. D.
1972. Artificial propagation and hybridization of striped bass,
Morone saxatilis (Walbaum). South Carolina Wildl. Mar.
Resour. Dep., 135 p.
Bonn, E. W., W. M. Bailey, J. C. Bayless, K. E. Erickson,
and R. E. Stevens.
1976. Guidelines for striped bass culture. Southern Div.,
Am. Fish. Soc, 103 p. plus app.
BOREMAN, J., AND H. M. AUSTIN.
1985. Production and harvest of anadromous striped bass
stocks along the Atlantic coast. Trans. Am. Fish. Soc.
114:3-7.
Cooper, J. C, and T. T. Polgar.
1981. Recognition of year-class dominance in striped bass
management. Trans. Am. Fish. Soc. 110:180-187.
Doroshev, S. I.
1970. Biological features of the eggs, larvae and young of the
striped bass [Roccus saxatilis (Walbaum)] in connection with
the problem of its acclimatization in the USSR. J. Ichthyol.
10:235-248.
Eldridge, M. B., J. A. Whipple, and M. J. Bowers.
1982. Bioenergetics and growth of striped bass, Morons sax-
atilis, embryos and larvae. Fish. Bull., U.S. 80:461-474.
Eldridge, M. B., J. A. Whipple, D. Eng, M. J. Bowers, and
B. M. Jarvis.
1981. Effects of food and feeding factors on laboratory-
reared striped bass larvae. Trans. Am. Fish. Soc. 110:
111-120.
FISHERY BULLETIN: VOL. 84, NO. 4
Kerby, J. H., and E. B. Joseph.
1979. Growth and survival of striped bass and striped bass
x white perch hybrids. Proc. Annu. Conf. Southeastern
Assoc. Fish Wildl. Agencies 32:715-726.
Kerby, J. H., L. C. Woods III, and M. T. Huish.
1983. Culture of the striped bass and its hybrids: A review
of methods, advances and problems. In R.F. Stickney and
S. P. Meyers (editors), Proceedings of the Warmwater Fish
Culture Workshop, p. 23-54. World Maricult. Soc, Spec.
Publ. 3.
Logan, H. J.
1968. Comparison of growth and survival rates of striped bass
and striped bass x white bass hybrids under controlled en-
vironments. Proc. Annu. Conf. Southeast Assoc. Fish
Game Comm. 21:260-263.
Miller, P. E.
1978. Food habit study of striped bass post yolk-sac larvae.
Johns Hopkins Univ., Chesapeake Bay Inst., Spec. Rep. 68,
49 p.
Rogers, B. A., and D. T. Westin.
1981. Laboratory studies on effects of temperature and
delayed initial feeding on development of striped bass larvae.
Trans. Am. Fish. Soc. 110:100-110.
Steel, R. G. D., and J. H. Torrie.
1960. Principles and procedures of statistics. McGraw-Hill
Book Co., Inc., N.Y., 481 p.
Ware, F. J.
1975. Progress with Morone hybrids in fresh water. Proc.
Annu. Conf. Southeast Assoc. Fish Game Comm. 28:48-
54.
Williams, J. E., P. A. Sandifer, and J. M. Lindbergh.
1981. Net-pen culture of striped bass x white bass hybrids
in estuarine waters of South Carolina: a pilot study. J.
World Maricult. Soc. 12:98-110.
914
ASPECTS OF THE REPRODUCTIVE BIOLOGY,
SPATIAL DISTRIBUTION, GROWTH, AND MORTALITY OF
THE DEEPWATER CARIDEAN SHRIMP, HETEROCARPUS LAEVIGATUS,
IN HAWAII
Murray D. Dailey1 and Stephen Ralston2
ABSTRACT
The recent rapid development of fisheries for the Heterocarpus laevigatas in Hawaii and elsewhere in
the tropical Pacific has created the need for biological information to manage the resource. This study
reports on a 16-month sampling program of commercial shrimp catches in Hawaii, during which the depth
of capture, carapace length (CL), sex, and reproductive condition of 7,368 H. laevigatas were determined.
The overall sex ratio of H. laevigatus was 1:1.16 in favor of females and depended on the depth
sampled; there were relatively fewer females as depth increased. Seasonal variation in sex ratio was
evident which may have been due to changing catchability and availability or a sex related dispersion
pattern. Sex ratio also depended on size category, displaying a standard pattern with no evidence of
protandry.
Females mature at 40 mm CL (64% of asymptotic length) and ovigerous individuals are found year
round. However, the main reproductive season is from August-February, with over 50% of females
carrying eggs from October-January. Mature shrimp may undergo a depth related seasonal migration
in synchrony with breeding. Mature males and females were found deeper (700 m) during the reproduc-
tive season than not (550 m). Females apparently settle in deep water and migrate gradually to shallower
water as they grow.
Seasonal length-frequency data suggest H. laevigatus is not semelparous. Separate analyses of CL-
frequency distributions of male and female shrimp indicate their von Bertalanffy asymptotic sizes are
57.9 and 62.5 mm CL, respectively. Growth coefficients (K) estimated by modal progression were 0.35
and 0.25 per year for males and females, and total instantaneous mortality rates were 1.51 and 0.73
per year, respectively.
The deepwater caridean shrimp, also known as
"ono" or smooth nylon shrimp, Heterocarpus laevi-
gatus, (Family Pandalidae) occurs throughout the
tropical Pacific Ocean, where it is found in benthic
deepwater habitats (450-900 m) (Wilder 1977; King
1983). While early trapping surveys in the Hawaiian
Islands revealed its local abundance (Clarke 1972;
Struhsaker and Aasted 1974), little information was
available concerning its biology. These early studies
did show, however, that H. laevigatus was poten-
tially of commercial importance, with a preliminary
maximum sustained yield estimate of 454-907 metric
tons (t) derived for the Hawaiian Archipelago
(Department of Land and Natural Resources 1979).
More recently the Western Pacific Regional Fishery
Management Council3 (WPRFMC) has revised this
estimate to 400-4,000 t.
■Hawaiian Fishing Research Company, 737 Bishop Street, Suite
2910, Honolulu, HI 96813; present address: Department of
Biology, California State University at Long Beach, Long Beach,
CA 90840.
2Southwest Fisheries Center Honolulu Laboratory, National
Marine Fisheries Service, NOAA, 2570 Dole Street, Honolulu, HI
96822-2396.
Manuscript accepted July 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
A commercial trap fishery for this species sub-
sequently developed in the Hawaiian Islands, and
in 1984 the WPRFMC began the process of develop-
ing a fishery management plan for the Heterocar-
pus shrimp resources of the region. Landings from
the Hawaiian fishery exceeded 135 t in 1983 but
have declined sharply since, although commercial
interest in the resource remains great (WPRFMC
fn. 3). Recent research surveys in Hawaii have now
more clearly defined this species' depth, temporal,
and geographic distributions (Oishi 1983; Hawaiian
Divers 19834; Gooding 1984), although the life
history of H. laevigatus remains largely unknown.
The only substantive biological studies to date were
3Western Pacific Regional Fishery Management Council. 1984.
Status of fisheries assessment of development and management
needs for selected crustacean species in the western Pacific region.
Unpubl. manuscr., 60 p. Southwest Fisheries Center Honolulu
Laboratory, National Marine Fisheries Service, NOAA, 2570 Dole
Street, Honolulu, HI 96822-2396.
4Hawaiian Divers. 1983. Deepwater shrimp utilization study
for Hawaii. Report prepared under NOAA Cooperative Agree-
ment No. 80-ABH-00065 for the Southwest Region, Western
Pacific Program Office, National Marine Fisheries Service, NOAA,
Honolulu, HI, 47 p.
915
FISHERY BULLETIN: VOL. 84, NO. 4
completed in the Marianas (including Guam) and Fiji
(Wilder 1977; King 1983; King and Butler 1985;
Moffitt and Polovina5).
Evidence also exists to show that this species is
highly susceptible to trapping (Ralston 1986) and,
according to commercial fishermen, depletion of the
resource has occurred over certain fishing grounds
in Hawaii (S. Barrows6). Because estimates of the
shrimp's productive capacity which are currently
available are preliminary at best and a fishery has
developed rapidly, this study set out to examine
aspects of the life history of the Hawaiian stock of
H. laevigatus to obtain information useful in devel-
oping a basis for management of the fishery.
METHODS
All sampling was conducted by commercial fishing
vessels owned by the Hawaiian Shrimp Company
(Easy Rider, Mokihana, and the Easy Rider Too)
over the 16-mo period from August 1983 to Novem-
ber 1984. During this time, six 35-60 d cruises were
completed and samples were obtained during 9 of
the 12 calendar months (Table 1). Fishing was con-
ducted throughout much of the Hawaiian Archi-
pelago, from Gardner Pinnacles south to the Island
of Hawaii (Fig. 1). Samples were collected at all of
the seven main islands (Hawaii, Kauai, Lanai, Maui,
Molokai, Niihau, and Oahu) and from Necker,
French Frigate Shoals, and Gardner Pinnacles in
the Northwestern Hawaiian Islands.
All shrimp were caught during overnight sets of
baited pyramidal traps, which measured 1.5 x 1.8
m with a funnel opening at the top center. Fishing
was targeted between depths of 500 and 700 m,
5Moffitt, R. B., and J. J. Polovina. The distribution and yield
assessment of the deepwater shrimp resource in the Marianas.
Manuscr. in prep. Southwest Fisheries Center Honolulu Labora-
tory, National Marine Fisheries Service, NOAA, 2570 Dole Street,
Honolulu, HI 96822-2396.
6S. Barrows, Hawaiian Shrimp Company, 737 Bishop Street,
Suite 2910, Honolulu, HI 96813, pers. commun. 1985.
Table 1 .—Temporal and geographic distribution of Heterocarpus
laevigatus samples (FFS = French Frigate Shoals).
Year
Month
Location
Sample size
1983
Aug.
Oahu
79
1983
Sept.
Oahu
26
1983
Oct.
FFS
188
1983
Nov.
FFS
1,942
1984
Jan.
Oahu
285
1984
Mar.
Niihau, Kauai
530
1984
April
Hawaii
631
1984
May
Lanai, Maui, Molokai
1,389
1984
June
Necker
842
1984
Sept.
Gardner Pinnacles, FFS, Necker
1,438
1984
Nov.
Necker
18
although some catches were made in both shallower
and deeper water because of the trap drift. The best
catch rates were found in areas of hard rough bot-
tom; otherwise, all sampling sites were to all ap-
pearances similar.
Systematic subsamples of the catch were taken
from every other trap on every second fishing day
by randomly scooping approximately 0.9 kg (2 lb)
of shrimp from traps prior to emptying. Samples
were placed in double bags with tags recording date,
location, depth, and condition, and were then frozen
and packed for transfer to the laboratory. There all
shrimp were identified to species; sexed; examined
for embryos on the pleopods; measured to the near-
est 0.1 mm for carapace length (CL), carapace width
(CW), and total length (TL); and weighed to the
nearest 0.1 g on a top loading scale. The data were
then keypunched and stored for analysis.
Size-frequency distributions of H. laevigatus were
analyzed by the regression method of Wetherall et
al. (in press) to estimate maximum size (Lm of the
von Bertalanffy growth equation) and the ratio of
total instantaneous mortality rate (Z) to von Berta-
lanffy growth coefficient (K). Additionally, the
growth coefficient of H. laevigatus was estimated
by following the progression of size modes evident
in three large samples taken: 1) 24 October to 6
November 1983, 2) 24 April to 11 May 1984, and
3) 3 September to 6 November 1984. Sample sizes
of N = 2,021, 1,991, and 1,438 were obtained in
these respective samples, accounting for 74% of all
shrimp measured in the study. Modal progression
of size distributions was determined by the
ELEFAN I computer program of Pauly (1982).
RESULTS
A total of 7,368 H. laevigatus were measured and
examined for CL, sex, and the presence of eggs
(Table 1). Of these 3,956 were females (32.6% of
which were ovigerous) and 3,412 were males. This
corresponds to an overall male to female sex ratio
of 1:1.16, departing significantly from equality (P
< 0.0001). Measurements of TL, CW, and weight
were obtained from 5,920 of the shrimp sampled.
Due to an imbalance in sampling, the effects of
location and time on the distribution of H. laevigatus
could not be completely separated. We therefore
assume that all samples were drawn from statis-
tically homogeneous locations in order to isolate and
examine temporal and depth effects. The strength
of this assumption is based largely on our personal
observations and those of fishermen that seasonal
change seems to account for most major population
916
DAILEY and RALSTON: BIOLOGICAL DEVELOPMENT OF HETEROCARPUS LAEVIGATUS
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FISHERY BULLETIN: VOL. 84, NO. 4
variations in Hawaii, as well as evidence from the
Mariana Archipelago which shows that populations
of if. laevigatus are affected to a greater degree by
temporal factors than geographic ones (Polovina7).
Morphometries
The results of performing functional regressions
(Ricker 1973) on the three linear size measurements
(CL, CW, TL) are given in Table 2. Estimates of
slope and intercept are provided for all possible per-
mutations of these variables. Separate analyses for
males (M), females without eggs (F0), and females
with eggs (FE) were not performed because all have
similar gross morphologies (but see King and Mof-
fitt 1984). As expected, the data were well described
with a linear fit.
The relationship between weight and CL was ex-
amined by analysis of covariance (BMDP 1977) to
determine whether the M, F0, and FE subgroups
have different weight-length relationships. Results
showed all three were characterized by differing
slopes in the regression of loge (weight) on \oge (CL)
(F = 86.46, df = 2, 5912, P« 0.0001). Parameter
estimates with standard errors and other regression
statistics are presented in Table 3 for each of the
three subgroups. Note that the reduced r2 of the
7J. J. Polovina, Southwest Fisheries Center Honolulu Labora-
tory, National Marine Fisheries Service, NOAA, 2570 Dole Street,
Honolulu, NI 96822-2396, pers. commun. June 1985.
FE group is due to a substantial reduction in the
range of CL over which the data were fitted. The
results of performing functional regressions of loge
(weight) on loge (CL) are also given.
During the analysis an anomalous bimodal distri-
bution of weight at length emerged. The bimodality
was not due to sexual class (M, F0, or FE) and
clearly diminished to a unimodal weight distribution
as CL increased from 15 to 40 mm. We have no ex-
planation for these data.
Reproductive Biology
The reproductive season of H. laevigatus was esti-
mated by plotting the percentage of ovigerous
females relative to total females against the month
sampled. For the data which overlapped 1983 and
1984 no interannual difference was evident (i.e., the
timing of reproduction was similar), so the data were
pooled by month between these years. The results
are presented in Figure 2 where the data have been
further aggregated into 2-mo "seasons". For each
the percentage of females bearing eggs is plotted
with its 95% confidence interval and associated sam-
ple size given above.
The data show an increased incidence of ovigerous
females from August to February (>30% of
females). In particular over 50% of all sampled
females carried eggs from October to January.
Relatively few shrimp were caught with eggs dur-
ing the period from April to July (<10%). Moreover,
Table 2. — Parameter estimates of functional regressions on linear size
measurements. All measurements in millimeters and all sample sizes n
= 5,920.
Dependent
Independent
Inter-
Correlation
variable
variable
Slope
cept
coefficient
Total length
Carapace length
2.864
10.182
0.963
Carapace width
Carapace length
0.613
-5.562
0.964
Carapace length
Total length
0.349
-3.536
0.963
Carapace length
Carapace width
1.630
9.098
0.964
Carapace width
Total length
0.214
- 7.737
0.902
Total length
Carapace width
4.673
36.153
0.902
Table 3. — Functional and predictive length-weight regressions for Heterocarpus
laevigatus. The natural logarithm of weight in grams is fitted to the natural logarithm
of carapace length in mm. The standard errors of the slope (b) and intercept (a) are
given by Sb and Sa respectively.
Slope Intercept Sb Sa n r2
Males
Females
without eggs
Females
with eggs
Predictive
Functional
Predictive
Functional
Predictive
Functional
2.755
2.910
2.605
2.745
1.815
2.470
- 6.809
-7.358
-6.252
-6.757
-2.986
-5.498
0.0176 0.0629 2,788 0.8976
0.0185 0.0671 2,202 0.8999
0.0550 0.2114 928 0.5401
918
DAILEY and RALSTON: BIOLOGICAL DEVELOPMENT OF HETEROCARPUS LAEVIGATUS
01
o>
D/J
F/M A/M J/J
Time of Year
A/S
0/N
Figure 2.— Seasonal incidence of ovigerous Heterocarpus laevigatus females in the
Hawaiian Islands. Vertical bars represent 95% confidence intervals and sample sizes
are presented above. Site locations vary.
when the analysis was restricted to mature females
only (see next section) the seasonal pattern of egg-
bearing was unchanged. From these results we
conclude that in Hawaiian waters H. laevigatus
reproduces during the fall and winter seasons
(August-February).
The size at maturity of female shrimp was deter-
mined by aggregating the female data into 5 mm
CL classes and plotting the incidence of ovigerous
females against CL class (Fig. 3). Only samples ob-
tained during the reproductive season were included
in the analysis. As before, the overall percentage
100
Carapace Length - mm
Figure 3.— Size at maturity for female Heterocarpus laevigatus sampled during the
reproductive season. Vertical bars represent 95% confidence intervals and sample
sizes are presented above.
919
FISHERY BULLETIN: VOL. 84, NO. 4
with 95% confidence limits and sample sizes are
provided.
The data show that the 55-60 mm CL class en-
compassed the largest shrimp observed. Virtually
all (95%) females >50 mm CL that were sampled
during August-February bore eggs. Conversely, up
to 35 mm CL no more than 1% of the shrimp ex-
amined were ovigerous. The figure shows further
that at a CL of 40 mm the percentage of ovigerous
females is one-half its maximum value, with 48% of
all sampled females bearing eggs. We conclude that
females become sexually mature at this size
(Gunderson et al. 1980). We have no data on matura-
tion in males.
The data presented in Figure 4 show the sex ratio
of shrimp as it depends on size (CL mm). Plotted
are the percentage females, with 95% confidence
intervals and sample sizes, against 5 mm CL size
classes. The data clearly show that H. laevigatus
maintains a relatively uniform sex ratio from 10 to
45 mm CL, but that females predominate in the
largest length categories (45-65 mm CL).
Because some studies (Clarke 1972; Wilder 1977)
have indicated that Heterocarpus females may
experience mass mortality after egg bearing, we ex-
amined the relationship of sex ratio to season (Table
4). Presented for each 2-mo sampling period are the
number of females and total number of shrimp
sampled, the proportion which are female, and the
standard error of the proportion. The results show
that an unusually high fraction (0.72) of the shrimp
sampled during the peak of the reproductive season
(December-January) are female. Note that the in-
cidence of females in trap samples declines signifi-
cantly to a value of 0.45 in April-May as the breeding
season wanes. At first inspection these data support
the contention that females experience increased
mortality after bearing eggs, i.e., that//, laevigatus
may be semelparous.
Table 4.— Sex ratio of Heterocarpus laevigatus by month sampled.
The standard error of the proportion is given by Sp .
Number
Proportion
Month
of females
of females
n
sP
December-January
207
0.72
285
0.026
February-March
293
0.55
530
0.022
April-May
923
0.45
2,020
0.011
June-July
459
0.54
842
0.017
August-September
857
0.55
1,542
0.013
October-November
1,217
0.56
2,148
0.011
Spatial Distribution
The relationship between the sex ratio of H. laevi-
gatus and sampling depth is provided in Table 5.
These results demonstrate that the relative abun-
dance of the two sexes is not independent of depth
(X2 = 165.6, df = 16, P < 0.001). As depth in-
creases (440-760 m) there is a significant decline in
the percentage of females in our samples (P = 0.05).
100
Carapace Length - mm
Figure 4.— Sex ratio as a function of carapace length. Vertical bars represent 95%
confidence intervals and sample sizes are presented above.
920
DAILEY and RALSTON: BIOLOGICAL DEVELOPMENT OF HETEROCARPUS LAEVIGATUS
Table 5.— Sex ratio and size of Heterocarpus laevigatas by depth
(M is for males, F0 for females without eggs, and FE for females
with eggs). Sp is the standard error of the proportion.
Depth
(m)
Number
of
females
N
Proportion
of
females
sP
Carapace length
All M F0 FE
440
41
71
0.58
0.059
40
34
43
48
60
9
11
0.81
0.116
39
36
40
—
80
65
141
0.46
0.042
38
33
42
49
500
155
230
0.67
0.031
42
34
45
49
20
287
430
0.66
0.023
43
40
45
46
40
419
943
0.44
0.016
37
35
40
49
60
193
487
0.39
0.022
37
36
38
45
80
280
500
0.56
0.022
39
35
42
47
600
282
498
0.56
0.022
38
35
38
. 46
20
284
463
0.61
0.023
39
35
34
48
40
325
581
0.55
0.021
38
37
32
47
60
109
210
0.51
0.034
37
34
35
44
80
95
167
0.56
0.038
39
37
35
48
700
90
222
0.40
0.033
36
36
31
43
20
399
738
0.54
0.018
39
38
32
47
40
68
126
0.53
0.044
40
37
33
48
60
14
46
0.30
0.068
34
34
28
42
The results presented in Table 5 also show the
distribution of mean size (CL mm) by depth (m) for
all H. laevigatus caught, and for the M, F0, and
FE subgroups. For all shrimp combined, average
size decreases slightly with increasing depth fished.
The trend for decrease in size with increasing depth
is not evident in the M subgroup. However, the F0
class demonstrates a strong relationship of decreas-
ing mean CL with depth. For the FE category the
decline is much less apparent, if at all. Thus the
overall decline in mean CL of all shrimp combined,
is clearly due to an overriding influence of females
without eggs. We interpret these trends, or lack
thereof, to indicate that young (i.e., small) females
may move from deep to shallow water as they
mature.
There is some evidence that the depth distribu-
tion of H. laevigatus changes with reproductive
activity (i.e, season). Figure 5 presents the depth
distributions for reproductively competent (>40 mm
CL) male and female shrimp, classified into samples
taken outside (March- July) and during the reproduc-
tive season (August-February). Note that depth
distributions of both male and female shrimp are
60
40-
20-
>
- 40
«
cc
20-
M ALE S
> 40 mm CL
400
FEMALES
> 40 mm CL
800
Depth
Figure 5.— Seasonal distributions of large (>40 mm) male and female Heterocarpus
laevigatus by depth. The dashed line represents the spawning season distribution (May-
February) and the solid line represents the distribution during the nonspawning season
(March-July).
921
FISHERY BULLETIN: VOL. 84, NO. 4
shifted 150 m deeper when the females are ovig-
erous. Although the data are not corrected for what
may have been differences in fishing effort by depth,
it is true that fishing was targeted to depths of max-
imum shrimp abundance. Based on these findings,
and the results presented in Table 5, our data are
consistent with a hypothesis of gradual movement
of small females from deep to shallow water, with
mature shrimp moving between depths of 550 and
700 m in synchrony with the ovigerous cycle of
females.
Growth and Mortality
Clarke (1972) and King (1983) have suggested that
Heterocarpus spp. may breed once and die. Indeed
the results already presented in Table 4 may be con-
sidered consistent with the hypothesis that at least
female H. laevigatus are semelparous. To further
address this question we examined the size struc-
ture of male and female shrimp classified as follows:
1) during the latter half of the reproductive season
(January-February) and 2) immediately following
the reproductive season (March-July). If postrepro-
ductive mortality of shrimp was severe, a decrease
in the relative abundance of large, breeding adults
would be expected as the reproductive season
waned.
The results presented in Figure 6 conflict with this
expectation, where it is apparent that the propor-
tional representation of large reproductive in-
dividuals (>40 mm CL) is actually greater imme-
20
15
10 -
&
15-
10-
5-
FEMALES
MALES
I
10
20 30 40
Carapace Length -mm
60
Figure 6.— Relative size-frequency distributions of male and female Heterocarpus
laevigatus during the peak and postreproductive seasons. The solid line represents
the peak season (January-February), males N = 78, females N = 207; the dashed
line is based on data collected immediately after the peak season (March-July) males
AT = 1,717, females N = 1,675.
922
DAILEY and RALSTON: BIOLOGICAL DEVELOPMENT OF HETEROCARPUS LAEVIGATUS
diately following than during the latter half of the
reproductive season.
The total sample CL-frequency distribution of
males and females combined was analyzed by the
regression method of Wetherall et al. (in press) to
estimate Lm and Z/K. When all shrimp are pooled
(N = 7,368), an estimate of Lx = 61.7 mm CL
results. Further, the ratio of total mortality rate to
von Bertalanffy growth coefficient (Z/K) is esti-
mated to be 2.6. Calculations were repeated for
separate male and female subgroups, where it was
found that L = 57.9 and 62.5 mm CL and ZIK =
00
4.3 and 2.9 for males and females, respectively.
These results indicate that males generally grow to
a smaller size than females.
The results of analyzing the progression of CL size
modes in frequency distributions of male and female
H. laevigatus provided preliminary estimates of K
= 0.35 yr-1 for males and 0.25 yr-1 for females.
The former result must be viewed with caution,
however, because two "solutions" were detected by
the computer search algorithm (Pauly 1982) which
differed little in fit. One of these, K = 0.70 yr-1,
we believe to be unjustifiably high in light of the
minor difference (8%) between the L^ of males and
the L^ of females obtained from the regression
analysis. Note that estimates of K and Lk typical-
ly show a strong inverse correlation (Gallucci and
Quinn 1979). These results, in conjunction with the
estimates of ZIK for male and female shrimp pre-
sented earlier, provide the basis for preliminary
estimation of total mortality rate. We estimate Z
= 1.51 yr-1 for males and 0.73 yr-1 for females,
corresponding to annual survivorship fractions of
22% and 48% per year, respectively. These data in-
dicate that males grow faster while experiencing a
substantially greater total mortality rate than
females.
DISCUSSION
Earlier it was assumed that, aside from depth, all
shrimp samples were drawn from locations which
are dynamically homogeneous; i.e., the behavior of
shrimp populations through time does not vary from
site to site. This is clearly a restrictive and simpli-
fying assumption and is without doubt the major
limitation on the results presented here. Nonethe-
less, it was a necessary simplification for us to
analyze the commercial fishing data upon which this
study was based. Consequently, we view those
results which rely upon this assumption as tentative
and in need for further validation.
Examination of the seasonal trend in the relative
abundance of ovigerous females showed that in
Hawaii over 50% of H. laevigatus females bear eggs
from October to January, with a peak between
August and February. Wilder (1977) found a similar-
ly timed but more narrowly defined breeding season
for H. laevigatus in Guam, where the percentage of
ovigerous females in trap catches reached a max-
imum during December, but was not particularly
high in any other month. Clarke (1972) reported that
H. ensifer in Hawaii also reproduces in the winter.
The breeding season of these shrimps is unusual
among Hawaiian crustaceans and fishes, which
typically reproduce during the spring and summer
and uncommonly during the winter (Watson and
Leis 1974; Lobel 1978; Uchida et al. 1980; Uchida
and Tagami 1984; Walsh 1984).
Our data also indicate that in Hawaii sexual
maturity of female ono shrimp occurs at approx-
imately 40 mm CL, a size similar to that reported
by King (1983) for shrimp from Fiji, Vanuatu, West
Samoa, and Tonga and by Moffitt and Polovina (fn.
5) for samples from the Marianas. Based upon the
estimated parameters of the von Bertalanffy growth
equation derived here, this corresponds to an age
of first maturity of 4 yr. Although we have no data
on the maturation of males, we believe they prob-
ably mature earlier and at smaller size, perhaps at
age 3 when they are 37-38 mm CL. Such a result
is consistent with the findings of Moffitt and Polo-
vina (fn. 5) who found that male H. laevigatus in the
Marianas mature at a smaller size than do females.
Wilder (1977) speculated that both H. ensifer and
H. laevigatus in Guam are protandrous hermaphro-
dites, as did Clarke (1972) for Hawaiian populations
of H. ensifer. However, the results presented in
King and Moffitt (1984) tend to contradict this con-
clusion. These authors studied the morphometry and
sexuality of five deep water pandalids, including//.
laevigatus, in Fiji and the Marianas. Using the
relative length of the appendix masculina expressed
as a proportion of CL, they found no tendency
toward protandrous hermaphroditism. Moreover,
the sex ratio reported in their study was approx-
imately 1:1.
Our results also indicate that for Hawaiian popula-
tions of H. laevigatus, and we speculate for most
tropical pandalids, a sex transition does not occur.
Wenner (1972) has termed the pattern exhibited in
Figure 4 the standard sex ratio pattern, as distin-
guished from one of reversal. Due to the large
numbers of females in small size classes, these data
are generally inconsistent with a protandric herma-
phroditic life history, as has been hypothesized by
previous workers on Heterocarpus spp. (Clarke
923
FISHERY BULLETIN: VOL. 84, NO. 4
1972; Wilder 1977). King and Moffitt (1984) also
argue for dioecy in this species based upon relative
changes in the morphology of the appendix
masculina.
Evidence now exists to suggest that the sex ratio
of if. laevigatus undergoes a seasonal change (Table
4), although the reasons for this are at present
unknown. A biological alteration in population struc-
ture of this order seems unlikely. Rather, the rela-
tively high catch of females during the December-
January period may be due to seasonal changes in
catchability or vulnerability of one or both sexes to
the traps. Alternatively, the spatial dispersion of H.
laevigatus may depend on sex. If males and females
are spatially segregated, the high proportion of
females in the December-January sample may have
been due to small sample size (N = 207).
We have also shown that sex ratio depends strong-
ly on the depth sampled (Table 5), with diminishing
representation of females as depth increases. This
spatial heterogeneity between the sexes may be due
to directed movements. Based on size trends of
females we conclude that they recruit to deeper
water and subsequently migrate to shallower water.
We have no evidence for similar movement of males.
Studies by King (1983) on Pacific Heterocarpus
spp. showed cyclic migrations in these shrimps, sug-
gesting that depth distribution may change season-
ally, with an annual migration up and down the slope
of the sea floor. The data presented in Figure 5 in-
dicate that mature H. laevigatus in Hawaii do
migrate seasonally, demonstrating distinct shifts in
the depth distributions of both sexes during the
reproductive season. Because this result is con-
founded by what may be a location effect, however,
we view them as preliminary and in need of further
confirmation. King (1983) also reported that Hetero-
carpus spp. were found in stomachs of tuna in Fiji,
indicating perhaps some type of vertical migration
in the water column.
King (1985), based on work completed in Fiji, ex-
amined the question of iteroparity and semelparity
in several genera of pandalid shrimp (Plesionika,
Saron, Parapandalus, and Heterocarpus). Based on
the difference between length at sexual maturity
and maximum length, he concluded that shallow-
water species (e.g., H. ensifer) are semelparous. He
states that deepwater Heterocarpus spp. "have an
extended reproductive lifespan, the length of which
may be taken to indicate the number of spawnings."
We conclude, based on the relative size-frequency
distributions of males and females during peak and
postreproductive seasons, that both sexes survive
well after reproducing— evidence in favor of itero-
parity. Although a high mortality of shrimp follow-
ing the breeding season would be evidence consis-
tent with a semelparous life history, it is not a
sufficient result to prove it. This is because each
female, before dying, could have sequential multi-
ple clutches during the October-February ovigerous
period. Nonetheless, good survival oiH. laevigatus
females after carrying eggs (Fig. 6) is indicative of
iteroparous reproduction.
The regression technique of Wetherall et al. (in
press) produced estimates of the ratio of mortality
to growth coefficient of 2.9 and 4.3 for females and
males respectively. Moffitt and Polovina (fn. 5),
using similar methods, estimated Lm = 55.2 mm
CL and ZIK = 2.5 for combined male and female
samples of H. laevigatus from essentially unfished
stocks in Guam and the Marianas. Ralston (1986)
also reported that the ZIK ratio of an unexploited
population of H. laevigatus at Alamagan in the
Marianas was about 2.0. The differences between
estimates may therefore relate to differences in
levels of exploitation. Moreover, the higher mortal-
ity rate of male shrimp when compared with females
(1.51 versus 0.73 yr_1) may explain the somewhat
biased sex ratio in favor of females.
ACKNOWLEDGMENTS
We acknowledge the help of the fishing vessels
Easy Rider, Easy Rider Too, and Mokihana. Special
thanks go to Jack Klein of the Mokihana crew for
his collection of material. Also, we thank Robert
Richlynski and Patricia M. Van Nuis for their
technical help during the collection of data.
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1972. Exploration for deep benthic fish and crustacean
resources in Hawaii. Univ. Hawaii, Hawaii Inst. Mar. Biol.
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BMDP.
1977. BMDP Biomedical Computer Programs, P-Series.
Univ. Calif. Press, Los Ang., 880 p.
Department of Land and Natural Resources.
1979. Hawaii fisheries development plan. Department of
Land and Natural Resources, State of Hawaii, 297 p.
Gallucci, V. F., and T. J. Quinn II.
1979. Reparameterizing, fitting, and testing a simple growth
model. Trans. Am. Fish. Soc. 108:14-25.
Gooding, R. M.
1984. Trapping surveys for the deepwater caridean shrimps,
Heterocarpus laevigatus and H. ensifer, in the Northwestern
Hawaiian Islands. Mar. Fish. Rev. 46(2): 18-26.
Gunderson, D. R., P. Callahan, and B. Goiney.
1980. Maturation and fecundity of four species of Sebastes.
Mar. Fish. Rev. 42(3-4):74-79.
924
DAILEY and RALSTON: BIOLOGICAL DEVELOPMENT OF HETEROCARPUS LAEVIGATUS
King, M. G.
1983. The ecology of deepwater caridean shrimps (Crustacea:
Decapoda: Caridea) near tropical Pacific Islands with par-
ticular emphasis on the relationship of life history patterns
to depth. Ph.D. Thesis, Univ. South Pacific, Suva, Fiji, 258
P-
King, M. G., and A. J. Butler.
1985. Relationship of life-history patterns to depth in deep-
water caridean shrimps (Crustacea: Natantia). Mar. Biol.
(Berl.) 86:129-138.
King, M. G., and R. B. Moffitt.
1984. The sexuality of tropical deepwater shrimps (Decapoda:
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Lobel, P. S.
1978. Diel, lunar, and seasonal periodicity in the reproduc-
tive behavior of the pomacanthid fish, Centropyge potteri,
and some other reef fishes in Hawaii. Pac. Sci. 32:193-207.
OlSHl, F.
1983. Pacific Tuna Development Foundation - State of Hawaii
shrimp industry development project. State Hawaii, Dep.
Land Nat. Resour., Div. Aquat. Resour., 22 p.
Pauly, D.
1982. Studying single-species dynamics in a tropical multi-
species context. In D. Pauly and G. I. Murphy (editors),
Theory and management of tropical fisheries. ICLARM and
CSIRO, Manila, 360 p.
Richer, W. E.
1973. Linear regressions in fishery research. J. Fish. Res.
Board Can. 30:409-434.
Struhsaker, P., and D. C. Aasted.
1974. Deepwater shrimp trapping in the Hawaiian Islands.
Mar. Fish. Rev. 36(10):24-30.
Uchida, R. N., and D. T. Tagami.
1984. Biology, distribution, population structure, and pre-
exploitation abundance of spiny lobster, Panulirus mar-
ginatus (Quoy and Gaimard), in the Northwestern Hawaiian
Islands. In R. W. Grigg and K. T. Tanoue (editors), Pro-
ceedings of the Symposium on Resource Investigations in
the Northwestern Hawaiian Islands, Vol. 1, April 24-25,
1980, University of Hawaii, Honolulu, Hawaii, p. 157-198.
UNIHI-SEAGRANT-MR-84-01.
Uchida, R. N., J. H. Uchiyama, D. T. Tagami, and P. M. Shiota.
1980. Biology, distribution, and estimates of apparent abun-
dance of the spiny lobster, Panulirus marginatus (Quoy and
Gaimard), in waters of the Northwestern Hawaiian Islands:
Part II. Size distribution, legal to sublegal ratio, sex ratio,
reproductive cycle, and morphometric characteristics. In
R. W. Grigg and R. T. Pfund (editors), Proceedings of the
Symposium on Status of Resource Investigations in the
Northwestern Hawaiian Islands, April 24-25, 1980, Univer-
sity of Hawaii, Honolulu, Hawaii, p. 131-142. UNIHI-
SEAGRANT-MR-80-04.
Walsh, W. J., III.
1984. Aspects of nocturnal shelter, habitat space, and juvenile
recruitment in Hawaiian coral reef fishes. Ph.D. Thesis,
Univ. Hawaii, Honolulu, 475 p.
Watson, W., and J. M. Leis.
1974. Ichthyoplankton of Kaneohe Bay, Hawaii. Univ.
Hawaii Sea Grant Publ. UNIHI-SEAGRANT-TR-01, 178 p.
Wenner, A. M.
1972. Sex ratio as a function of size in marine Crustacea.
Am. Nat. 106-321-350.
WETHERALL, J. A., J. J. POLOVINA, AND S. RALSTON.
In press. Estimating growth and mortality in steady state fish
stocks from length-frequency data. ICLARM/KISR Conf.
Theory and Application of Length-Based Methods for Stock
Assessment.
Wilder, M. N.
1977. Biological aspects and the fisheries potential of two
deepwater shrimps, Heterocarpus ensifer and H. laevigatus
in waters surrounding Guam. M.S. Thesis, Univ. Guam,
Agana, Guam, 79 p.
925
AN INTENSIVE FISHING EXPERIMENT FOR
THE CARIDEAN SHRIMP, HETEROCARPUS LAEVIGATUS, AT
ALAMAGAN ISLAND IN THE MARIANA ARCHIPELAGO
Stephen Ralston1
ABSTRACT
During January 1984 an intensive fishing experiment for the deepwater caridean shrimp, Heterocarpus
laevigatus, was conducted near Alamagan Island in the Mariana Archipelago. Twenty standard shrimp
traps were set daily, producing a significant decline in the average catch rate from 3.33 to 1.82 kg/trap-
night over a 16-day period. This drop was associated with a removal of 776 kg of shrimp from the study
site. Resampling the area 4 months later showed that the catch rate remained depressed. Length-frequency
data demonstrate that the decrease in catch per unit effort was due to a decline in the number of shrimp
caught. An initial population size of 1,714 kg from 312 ha habitat is estimated, corresponding to one
exploitable shrimp per 51 m2. The estimate of catchability (0.001945 trap-night"1) indicates that H.
laevigatus may be easily overfished by trapping.
Intensive fishing experiments can provide the ideal
complement to resource surveys using catch per unit
effort (CPUE) to estimate the relative abundance
of exploitable stock. Whereas values of CPUE are
usually adequate for studying spatial and temporal
variation in resource abundance, often an absolute
estimate of exploitable biomass is required. This is
particularly true of yield assessments. Due to the
relative nature of CPUE statistics, a conversion fac-
tor is necessary to translate catch rates into absolute
units of biomass. This proportionality is termed
catchability, typically a constant parameter (but see
Schnute 1983; Polovina 1986) which can be esti-
mated from the results of intensive fishing ex-
periments (Ricker 1975).
The advantages of intensive fishing over alterna-
tive methods of estimating the catchability coeffi-
cient (q) are several. Foremost is that no history of
either catch or effort data is needed. This character-
istic makes methods of fishing success (Ricker 1975)
or survey-removal (Schnute 1983) particularly at-
tractive for use in assessments involving exploratory
survey data, as well as for studying emerging new
fisheries. A second advantage is that results can be
obtained rapidly. Because fishing is, by definition,
conducted intensively over a short time period and
the necessary computations are quite simple, an
estimate of q is quickly realized.
Southwest Fisheries Center Honolulu Laboratory, National
Marine Fisheries Service, NOAA, 2570 Dole Street, Honolulu, HI
96822-2396.
Although these advantages recommend the ap-
proach, two restrictive assumptions must be made
in analyzing the data. One must assume, in the
absence of information to the contrary, that the
population fished is closed, or equivalently, that
additions exactly balance removals other than those
due to fishing. The basis of this assumption can be
strengthened if the intensive fishing site is located
in a naturally isolated area. For example, Polovina
(1986) performed an intensive fishing experiment
on a small pinnacle 5.5 km in circumference which
was isolated by 75 km of deep water from the near-
est similar habitat. A second assumption is that fish-
ing removals account for all changes in stock
biomass, i.e., natural mortality, growth, and recruit-
ment are negligible during the period of fishing. For
this reason, removals are carried out intensively
over as short a time interval as possible. If both
assumptions hold then q can be estimated directly
by the slope of the linear regression of either CPUE
on cumulative catch (Leslie and Davis 1939) or
log{CPUE} on log{cumulative effort} (DeLury 1947).
Refinements to these two basic methods have been
proposed by Braaten (1969), Crittenden (1983),
Schnute (1983), and Polovina (1986) among others.
Generally, estimators have been found to be most
sensitive to a departure from the assumption of con-
stant catchability. A variety of adjustments have
been used to correct this and other statistical prob-
lems which often occur with real data.
The work reported here is an application of the
intensive fishing method to estimate the catchabil-
Manuscript accepted July 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
927
FISHERY BULLETIN: VOL. 84, NO. 4
ity and population density of a deepwater caridean
shrimp, Heterocarpus laevigatas. This circumglobal
species is found in depths of 400-950 m in subtropical
and tropical latitudes (King 1984). Experimental
trapping surveys have shown it to be abundant at
widespread localities in the central and western
Pacific (King 1983), and a developing commercial
fishery for this species has emerged in the Hawaiian
Islands (Gooding 1984). Interest by Pacific island na-
tions in promoting the harvest of this shrimp is great
(King 1981), providing the impetus for an assess-
ment of the Heterocarpus resource in the Mariana
Archipelago. Additional results of this research
program are reported elsewhere (Moffitt and
Polovina2).
MATERIALS AND METHODS
Intensive fishing for Heterocarpus laevigatus was
conducted in an area 3.5 km off the north end of
Alamagan Island in the western Pacific (lat.
17°39'N, long. 145°50'E). Alamagan is part of the
Commonwealth of the Northern Mariana Islands,
lying 450 km north of Guam (Fig. 1). It is small,
uninhabited, and of recent volcanic origin. While the
ocean bottom slopes steeply away from the island
at an angle of 25° to the east, south, and west, a
broad shelf, approximately 6.5 km2 in area and
lying 600-800 m deep, extends well off the north end
of the island. This shelf was selected as a study site
because 1) good catches of H. laevigatus were pre-
viously obtained in the area, 2) 700 m is an ideal
target depth for trapping this species (Moffitt and
Polovina fn. 2), 3) the relatively uniform bottom
topography would facilitate setting and retrieving
fishing gear, and 4) the area had no known history
of prior exploitation.
Fishing was conducted over a 16-d period, 9-24
January 1984, from the NOAA ship Townsend
Cromwell. Shrimp traps of standard Honolulu Lab-
oratory design were set daily in four strings of five
traps each. All traps were half round in shape (91
x 66 x 46 cm), with a frame constructed of 1.27
cm reinforcing steel, covered with 1.27 x 2.54 cm
mesh hardware cloth (illustrated in figure 3 of
Gooding 1984). Individual traps within a set were
spaced 40 m apart and were baited with three
chopped Pacific mackerel, Scomber japonicus. All
traps were set between 1100 and 1300 h in 600-800
2Moffitt, R. B., and J. J. Polovina. In prep. Distribution and
yield of the deepwater shrimp resource in the Marianas. South-
west Fisheries Center Honolulu Laboratory, National Marine
Fisheries Service, NOAA, 2570 Dole Street, Honolulu, HI
96822-2396.
m and were retrieved the following day between
0800 and 1100 h. In addition, a large (150 x 150
x 150 cm) pyramidal commercial shrimp trap was
sometimes deployed alone.
When fishing gear was recovered, the traps were
individually emptied and the contents sorted,
counted, and weighed to the nearest 0.01 kg by
species lot. On three occasions a random length-
frequency sample of trap-caught H. laevigatus was
saved for later study. All shrimp in these samples
were measured to the nearest 0.1 mm CL (carapace
length) with dial calipers.
To accurately delimit the bottom topography of
the study area, an unregistered reconnaissance
hydrographic survey was conducted over the site on
9 February 1984, with the Townsend Cromwell.
Depth soundings from a Raytheon3 fathometer were
recorded every 3 min over an 8.5-h period as the
vessel ran a predefined cruise track which covered
the entire study area. The position of the vessel was
recorded to the nearest 0.01 min at each sounding.
The Townsend Cromwell returned to the study site
again from 12 to 16 May 1984, to assess the recovery
of the H. laevigatus population in the study area and
to determine the effect of different baiting practices
on CPUE. Four sets of six traps each were set over-
night on each of four occasions. Half these traps con-
tained three chopped Pacific mackerel whereas the
other half (i.e., every other one) contained two whole
Pacific mackerel. The catch was sorted and treated
as discussed previously.
RESULTS
Hydrographic Survey
A total of 164 depth soundings were obtained over
the study site. The data were contoured using the
GCONTOUR procedure of SAS/GRAPH (SAS 1981)
and the resulting chart is presented in Figure 2.
Solid lines represent isobath contours spaced at 200
m depth intervals. Note that the shrimp study site
is a saddle point; concave upwards along the north-
south axis and concave downwards from east-west.
The hydrographic survey revealed a small but steep
pinnacle and a deep canyon immediately adjacent
to the study area.
In the figure the locations of each string of five
standard traps are shown as open circles (n = 60)
whereas single sets of the large pyramid trap are
given as closed circles (n = 8). Fishing effort was
3Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
928
RALSTON: FISHING EXPERIMENT FOR CARIDEAN SHRIMP
Bank C
■°Maug I.
o Asuncion I.
DAgrihan I
P Pagan I.
-20°-
■19*-
-18°-
<?A
amagan I.
BankD
Guguan I.
-17°-
Pathfinder Reef
Arakane Reef
Bank A
°Sarigan I.
^Anatahan I.
38 fm Bank .,
Esmeralda Bank '•-•
» Faral Ion de Med
in il la -
L/Saipan
"VTinian I."
° Aguijan I.
^Rota I.
-I6C
-15°-
-14°-
GUAM
"Cocos I.
^Galvez Banks.
'■■' Santa Rosa Reef
I43e
I44<
I45c
I46e
147° E
■13°-
FlGURE 1.— Map of the Mariana Archipelago.
929
FISHERY BULLETIN: VOL. 84, NO. 4
17°40'
■o
3
o
Z
I7°38'
145-48'
145°50'
East Longitude
145°52'
Figure 2.— Contour map of the Alamagan study site. Isobaths given in meters. Open circles repre-
sent set locations of standard traps (one set is composed of five traps); closed circles show sets
of the pyramid trap. The stipple border encloses the area of greatest fishing intensity. One minute
latitude = 1.85 km.
concentrated in the area enclosed by stipple borders,
where 65% of all sets (44 of 68) occurred. This area
represents 312 horizontal ha of shrimp habitat.
Intensive Fishing Experiment
Although 20 standard shrimp traps were set daily
for 15 consecutive days, 29 traps were lost due to
entanglement on the bottom. This resulted in 271
effective trap-nights of standard fishing effort and
a gear loss rate of 9.7% (Table 1). The loss of shrimp
traps is not believed to have affected the outcome
of the intensive fishing experiment for two reasons:
First, the Pacific mackerel bait was rapidly ex-
hausted in the traps, as evidenced by its condition
after a single night's soak; second, large holes were
usually evident in traps if the fishing gear was suc-
cessfully retrieved after being fouled on the bottom.
The catch of H. laevigatus was quite pure; only
trace amounts of H. longirostris, H. ensifer, and the
eel Synaphobranchus affinis co-occurred in the
traps. The latter species was observed to consume
individual H. laevigatus on occasion, but this had a
negligible impact on overall catch rates of the
shrimp.
A total catch of 663.36 kg of H. laevigatus was
landed from standard traps, yielding an overall
CPUE of 2.45 kg/trap-night (Table 1). In addition,
another 112.77 kg were taken in eight sets of the
pyramid trap for an overall CPUE of 14.10 kg/trap-
night (Table 1). The larger commercial trap out-
performed individual standard Honolulu Laboratory
Table 1 .—Summary of catch and effort statistics of the intensive
fishing experiment for Heterocarpus laevigatus at Alamagan Island,
9-24 January 1984. All catches in kilograms and effort in standard
trap-nights. CPUE includes only standard trap catches.
Standard
Pyramid
Corrected
Date
trap
trap
cumulative
Daily
(mo/d/yr)
catch
catch
catch
effort
CPUE
1/9/84
62.52
31
20
3.13
1/10/84
42.30
37.65
102
18
2.35
1/11/84
64.61
—
175
20
3.23
1/12/84
44.96
23.86
241
17
2.64
1/13/84
85.80
6.72
322
20
4.29
1/14/84
42.90
22.98
401
19
2.26
1/15/84
47.79
—
458
15
3.19
1/16/84
34.27
6.60
503
14
2.45
1/17/84
34.57
3.18
542
19
1.82
1/18/84
34.57
2.41
579
20
1.73
1/19/84
39.01
9.37
622
20
1.95
1/20/84
41.23
—
667
20
2.06
1/21/84
27.10
—
701
20
1.36
1/22/84
28.75
—
729
14
2.05
1/23/84
32.98
—
760
15
2.20
Total
663.36
112.77
271
traps by a ratio of 5.76 to 1. Thus, one set of the
large trap was roughly equivalent to one set of a
string of five standard traps, but the former was
much more variable in its performance. Overall, a
total of 776.13 kg of H. laevigatus were removed
from the study area during the 16-d experiment.
These averaged 28 g each (16 shrimp/lb).
The data presented in Table 1 are arranged to be
fitted by the Leslie model (Ricker 1975). The CPUE
was computed each day based solely on standard
trap catch and effort statistics, although cumulative
930
RALSTON: FISHING EXPERIMENT FOR CARIDEAN SHRIMP
removals included catches from the large commer-
cial trap. As in Ricker (1975), CPUE is regressed
against corrected cumulative catch, defined as the
cumulative catch prior to the start of an interval plus
half the catch taken during the interval (see also von
Geldern 1961).
Standard daily CPUE is plotted against cumula-
tive catch removed in Figure 3. The slope of the
regression is significantly less than zero (one-tailed
test, t = -2.80, df = 13, P = 0.01). Estimates of
slope, intercept, and mean squared error were
-0.001945 trap-night'1, 3.334 kg/trap-night, and
0.3754 (kg/trap-night)2, respectively. Consequently,
the catchability coefficient is estimated to be q =
0.001945 trap-night-1 and the initial population
size prior to the start of fishing to be n = 1,714 kg.
Confidence intervals for these estimates are
P(0.0004 < q < 0.0034) = 0.95 and P(1150 < n <
6005) = 0.95 (Ricker 1975). Notice that the con-
fidence interval for the estimate of initial popula-
tion biomass (n) is asymmetrical about the point
estimate.
Crittenden (1983) and others have warned against
unequal variance in plots of CPUE against cumula-
tive catch. To test for this possibility, the absolute
values of the residuals from Figure 3 were ranked
and the corrected cumulative catches were ranked.
A Spearman rank correlation coefficient was then
calculated, resulting in rs = -0.189, P = 0.50.
From this analysis there is no evidence of hetero-
scedasticity. Further, there is little to suggest curvi-
linearity in Figure 3. A runs test (Tate and Clelland
1957) on the signs of the residuals indicates they are
5.0-1
~ 4.(H
.C
O)
c
a
«J 3. OH
a>
I
LU
3
a
U
2.0-
1.0-
200 400 600
Cumulative Catch - kg
800
Figure 3.— Leslie model applied to Heterocarpus laevigatus at
Alamagan. Each point represents 1 day of fishing. Data from Table
1.
randomly sequenced (P > 0.40). This result supports
the assumption of constant catchability.
At the time the experiment was terminated, 776
kg of shrimp had been removed by trapping. An
estimate of the concomitant catch rate can be cal-
culated from the regression equation of Figure 3.
This estimate of CPUE is 1.82 kg/trap-night. When
the Townsend Cromwell returned to the study site,
4 mo later, the mean catch rate was 1.91 kg/trap-
night (42 effective standard trap-nights of effort,
s = 1.33), this based on a total catch of 80.08 kg
H. laevigatus. The preceding calculations include
only those traps which were baited comparably to
the experimental traps (three chopped Pacific
mackerel). Traps with two whole baits (n = 42)
yielded an average catch rate of 1.39 kg/trap-night
(s = 1.09).
Length-Frequency Distributions
Examination of size-composition data can help
interpret changes in weight CPUE. Declining trap
catch rates could, for example, represent fewer in-
dividuals of the same size. Conversely, a decline in
the average size of individuals caught with no
change in numbers would also result in declining
CPUE.
The three length-frequency distributions of H.
laevigatus sampled during the period of experimen-
tal fishing are presented in Figure 4. For each dis-
tribution the date of capture, depth of capture, sam-
ple size, and mean carapace length are provided.
Although appearing superficially similar, the results
of ANOVA show that significant differences exist
in size composition among the three samples (F =
10.03, df = 2, 343, P < 0.001). These differences,
however, do not explain the decline in CPUE. The
data in the figure show that the mean size of H.
laevigatus actually increased over time, and that the
overall decline in CPUE observed in Figure 2 must
therefore have been due to a decrease in the number
of shrimps caught.
DISCUSSION
Powell (1979) has shown that the shape of the
descending limb of length-frequency distributions
can provide useful information concerning the rela-
tionship between mortality and growth. Specifical-
ly, the ratio of Z (instantaneous total mortality rate)
to K (von Bertalanffy growth coefficient) is defined
in a simple way by the interrelationship of the least
size when fully vulnerable to the gear, the mean size
in the catch of fully recruited individuals, and the
931
FISHERY BULLETIN: VOL. 84, NO. 4
15
10-
5-
15
10-
■
5-
15
1-9-84
695 m
n = 132
X = 37.4
fl/
1-16-84
530 m
n = 103
X = 40.2
N
ru
_DL
^
Carapace Length -mm
Figure 4.— Length-frequency distributions of Heterocarpus
laevigatas taken in shrimp traps.
von Bertalanffy asymptotic size (L^). This is true
if the following conditions hold: 1) the growth of in-
dividuals follows a deterministic von Bertalanffy
growth curve, 2) mortality is constant and uniform
for all ages, and 3) recruitment is constant and con-
tinuous over time (Beverton and Holt 1956).
Results presented in Dailey and Ralston (1986)
provide the basis for estimating the minimum CL
when H. laevigatus becomes fully recruited to the
trap fishery. They provide a regression equation
relating carapace width (CW) to CL. In this study
the smallest mesh dimension of standard shrimp
traps was 1.27 cm. This provides a logical cutoff
point for measurement of least CW for shrimp that
are fully vulnerable to the gear. Based on their func-
tional regression this corresponds to 30 mm CL.
It is evident from the three panels in Figure 4 that
the size distribution of H. laevigatus above 30 mm
CL is characterized by both rising and descending
portions. As shown by Powell (1979) this indicates
a ZIK ratio of less than unity (i.e., instantaneous
mortality rate is less than the growth coefficient).
Alternatively, it is possible that the rising portions
of the length distributions are not representative of
the population sampled, but are instead a reflection
of behavioral interactions among shrimp of differ-
ent sizes. Chittleborough (1974), for example, has
shown that the presence of large individuals of the
decapod crustacean Panulirus cygnus inhibited
smaller conspecifics from entering baited traps,
even though smaller lobsters were vulnerable to the
traps in the absence of large ones. If this kind of
behavioral interaction was also in evidence here, the
effective least size of H. laevigatus when fully
vulnerable to the traps may be as large as 41 mm
CL, the mode of the pooled length-frequency distri-
bution. This would indicate a ZIK ratio of 2.0
because of the linearity of the descending portions
of the size-frequency distributions. Only further
experimentation will resolve this issue.
With respect to the intensive fishing experiment
it is useful to consider whether or not the basic
assumptions of the Leslie model were violated dur-
ing the course of the study. The first of these was
closure of the population. Two factors support the
contention that the study population was effective-
ly isolated and that the effects of immigration and
emigration were negligible. First, the hydrographic
survey showed that the study site comprised a semi-
isolated extension of the main island. Continuity of
prime habitat (600-800 m depth) with the island
proper extended along two narrow corridors to the
southeast and southwest. The shrimp has been taken
as shallow as 400 m and as deep as 950 m in the
Mariana Archipelago, but the 600-800 m depth
range encompasses the preponderance of the
region's shrimp stock (Moffitt and Polovina fn. 2),
although elsewhere (e.g., Fiji, Vanuatu, and Samoa)
the depth distribution apparently extends into some-
what shallower water (King 1984). The second fac-
tor arguing for closure is that the catch rate of H.
laevigatus remained low after a 4-mo hiatus in fish-
ing. If movements or migrations of shrimp were
biologically significant over this time interval, a
larger change in CPUE would be expected. It is
tempting to attribute the small increase in catch rate
(4.9%) to some type of biological recovery, but the
estimate of mean squared error in CPUE from
Figure 3 (0.3754 kg2/trap-night2) indicates that
background variation is too large for the observed
difference to be significant. Regardless, the data
support the assumption that the population is closed.
The second assumption was that growth, natural
mortality, and recruitment are negligible factors in
accounting for changes in CPUE. That the experi-
ment was completed in only 16 d and the popula-
932
RALSTON: FISHING EXPERIMENT FOR CARIDEAN SHRIMP
tion was reduced an estimated 45.3% are persua-
sive elements here. Additionally, the size-frequency
data show no indication of a major alteration in
population structure. As long as the selective prop-
erties of the fishing gear remain unchanged, alter-
ations in the length composition of the catch are not
expected over short time intervals, at least due to
the direct effects of fishing. Further, no recruitment
of small shrimp is evident. That the mean size of H.
laevigatus seemed to increase as the experiment pro-
gressed might support the hypothesis that growth
of the stock was significant. An alternate explana-
tion, however, is that size structure varies with
depth of capture. Results from the Hawaiian Islands
(Gooding 1984; Dailey and Ralston 1986) have now
demonstrated this. The three samples presented in
Figure 4 are confounded by this variable; other
unknown factors may also have affected the shrimp
size-frequency data (e.g., sexual dimorphism, con-
tagious dispersion, sampling error, etc.). In addition,
the estimated growth rate from the data (3.9 mm
CL over 8 d = 0.49 mm/d) is biologically unten-
able.
Other investigators, notably Schnute (1983) and
Crittenden (1983), have cautioned against the effects
of changing catchability and unequal variance on
Leslie model estimates. From the data gathered,
there is little statistical evidence to suggest that
these factors affected parameter estimates and I
therefore assume that 0.001945 trap-night-1 and
1,714 kg are reasonable estimates of standard trap
catchability and virgin population size, respec-
tively.
Given that the virgin biomass of H. laevigatus in
the study area was 1,714 kg, the next question is:
How large an area was intensively fished? From
Figure 2 it is clear that there is no simple answer
to this question. A number of sets were located in
areas peripheral to the main trapping area. Desig-
nating the stipple bordered area as the effective area
fished is arbitrary, but provides a useful starting
point to allow calculation of shrimp densities. This
area was calculated to be 312 ha, corresponding to
a projected density of 5.5 kg of exploitable H. laevi-
gatus per hectare. Since individuals weighed 28 g
each, on average, this is equivalent to 1 exploitable
shrimp/51 m2 of bottom, a remarkably low density.
Furthermore, a catchability coefficient of 0.001945
trap-night-1 indicates that one unit of standard
trap effort can reduce a 312-ha population of shrimp
by about 0.2%. This is certainly a significant impact.
The vulnerability to trapping that this species
demonstrates is cause for attention and careful
resource management.
ACKNOWLEDGMENTS
This paper is the result of the Resource Assess-
ment Investigation of the Mariana Archipelago at
the Southwest Fisheries Center Honolulu Labora-
tory, National Marine Fisheries Service.
I would like to thank the crew of the Townsend
Cromwell for their help in completing this study and
Samuel G. Pooley, Victor A. Honda, Leigh Neil, and
Ahser Edward for their tireless efforts and good
spirits while at sea. This paper benefited greatly
from a review provided by C. D. Knechtel.
LITERATURE CITED
Beverton, R. J. H., and S. J. Holt.
1956. A review of methods for estimating mortality rates in
fish populations, with special reference to source of bias in
catch sampling. Rapp. P.-v. Reun. Cons. Perm. int. Explor.
Mer 140:67-83.
Braaten, D. O.
1969. Robustness of the DeLury population estimator. J.
Fish. Res. Board Can. 26:339-355.
Chittleborough, R. G.
1974. Home range, homing, and dominance in juvenile west-
ern rock lobsters. Aust. J. Mar. Freshwater. Res. 25:
227-234.
Crittenden, R. N.
1983. An evaluation of the Leslie-DeLury method and a
weighted method for estimating the size of a closed popula-
tion. Fish. Res. (Amst.) 2:149-158.
Dailey, M. D., and S. Ralston.
1986. Aspects of the reproductive biology, spatial distribu-
tion, growth, and mortality of the deepwater caridean
shrimp, Heterocarpus laevigatus, in Hawaii. Fish. Bull.,
U.S. 84:915-925.
DeLury, D. B.
1947. On the estimation of biological populations. Bio-
metrics 3:145-167.
Gooding, R. M.
1984. Trapping surveys for the deepwater caridean shrimps,
Heterocarpus laevigatus and H. ensifer, in the Northwestern
Hawaiian Islands. Mar. Fish. Rev. 46(2): 18-26.
King, M. G.
1981. Increasing interest in the tropical Pacific's deepwater
shrimps. Aust. Fish. 40(6):33-41.
1983. The ecology of deepwater caridean shrimps (Crustacea:
Decapoda: Caridea) near tropical Pacific islands with par-
ticular emphasis on the relationship of life history patterns
to depth. Ph.D. Thesis, Univ. South Pacific, Suva, Fiji, 258
P-
1984. The species and depth distribution of deepwater cari-
dean shrimps (Decapoda, Caridea) near some Southwest
Pacific islands. Crustaceana 47:174-191.
Leslie, P. H., and D. H. S. Davis.
1939. An attempt to determine the absolute number of rats
on a given area. J. Anim. Ecol. 8:94-113.
Polovina, J. J.
1986. A variable catchability version of the Leslie model with
application to an intensive fishing experiment on a multi-
species stock. Fish. Bull, U.S. 84:423-428.
933
FISHERY BULLETIN: VOL. 84, NO. 4
Powell, D. G. Schnute, J.
1979. Estimation of mortality and growth parameters from 1983. A new approach to estimating populations by the
the length frequency of a catch. Rapp. P. -v. Reun. Cons. removal method. Can. J. Fish. Aquat. Sci. 40:2153-2169.
int. Explor. Mer 175:167-169. Tate, M. W., and R. C. Clelland.
Ricker, W. E. 1957. Nonparametric and shortcut statistics in the social,
1975. Computation and interpretation of biological statistics biological, and medical sciences. Interstate Printers Publ.,
of fish populations. Fish. Res. Board Can., Bull. 191, Inc., Danville, IL., 171 p.
382 p. Von Geldern, C. E., Jr.
SAS Institute, Inc. 1961. Application of the DeLury method in determining the
1981. SAS/GRAPH user's guide. 1981 ed. SAS Inst., Inc., angler harvest of stocked catchable-sized trout. Trans. Am.
126 p. Fish. Soc. 90:259-263.
934
ICHTHYOPLANKTON IN NERITIC WATERS OF
THE NORTHERN GULF OF MEXICO OFF LOUISIANA:
COMPOSITION, RELATIVE ABUNDANCE, AND SEASONALITY
James G. Ditty1
ABSTRACT
Ichthyoplankton samples were collected monthly between November 1981 and October 1982 in neritic
continental shelf waters off Louisiana. The survey provided the first quantitative data on the abundance
and seasonal occurrence of larval fishes from open coastal waters of this area. At least 48 families of
fishes were represented in samples that included 107 taxa, 54 of which were identified to species. Larval
densities were lowest during the winter and highest during the summer with a mean monthly density
of 208/100 m3. Five families accounted for about 90% of total larvae: Engraulidae, Sciaenidae, Clupeidae,
Carangidae, and Bothidae. The five most abundant taxa overall, in order of decreasing abundance, were
anchovies (Engraulidae); Atlantic croaker, Micropogonias undulatus; Atlantic thread herring, Opistho-
nema oglinum; gulf menhaden, Brevoortia patronus; and Atlantic bumper, Chloroscombrus chrysurus.
These taxa accounted for 82% of all larvae collected. Comparison of ichthyoplankton surveys throughout
the Gulf of Mexico showed that the 10 most abundant families contributed over 90% of total larval abun-
dance in coastal surveys but less than 70% in offshore surveys. Likewise, the five most abundant taxa
contributed over 80% of total larval abundance in all but one of the coastal surveys but less than 40%
in the offshore surveys. These data suggest that compared with offshore waters, there are relatively
fewer dominant taxa among the ichthyoplankton in neritic waters of the Gulf of Mexico.
The northern Gulf has traditionally been one of the
most productive fishery areas in North America
(Gunter 1967), yet seasonality and abundance of
larval fishes from open waters are poorly known.
Previous studies of early life history stages in this
area have mainly been focused either on select taxa
(Turner 1969; Fore 1970, 1971; Christmas and
Waller 1975; Fruge 1977; Ditty 1984; Cowan 1985;
Shaw et al. 1985) or to surveys limited in temporal
and areal coverage (Walker 1978; Ditty and Trues-
dale 1984). Stuck and Perry (1982) surveyed the
ichthyoplankton community adjacent to Mississippi
Sound, while Marley (1983) conducted an egg survey
and Williams (1983) a larval fish survey of lower
Mobile Bay, AL. The most comprehensive studies
of the offshore larval ichthyofauna in the Gulf of
Mexico and adjacent areas were those of Finucane
et al. (1977) from the south Texas outer continen-
tal shelf; Houde et al. (1979) from the eastern Gulf
of Mexico off Florida; Richards (1984) from the
Caribbean Sea; and Powles and Stender (1976) from
the South Atlantic Bight area off the east coast of
the United States. The objective of this paper is to
provide quantitative data on the abundance and
seasonal occurrence of larval fishes from open
Louisiana Department of Wildlife and Fisheries, Seafood Divi-
sion, P.O. Box 15570, Baton Rouge, LA 70895.
coastal waters of the northern Gulf of Mexico off
Louisiana.
MATERIALS AND METHODS
Plankton samples were collected monthly between
November 1981 and October 1982 (except March
1982) in neritic continental shelf waters off Louisi-
ana. Samples were collected at six stations in a 3.2
km2 area located about 12.9 km south-southwest of
Caminada Pass, in depths of 10-12 m (Fig. 1). Col-
lections were made with a 60 cm paired-net, open-
ing and closing bongo-type BNF-1 sampler2, each
net was of 0.363 mm Nitex3 mesh. Nets were
lowered to depth, opened, and towed simultaneous-
ly, in series, at discrete depths (surface, middepth,
and near-bottom) for about 3 min, at a ship speed
of approximately 1.5 kn; all samples were collected
during the day. A General Oceanics (Model 2030)
flowmeter was placed in the mouth of each net to
estimate volume filtered. Samples were preserved
in seawater with buffered Formalin and returned
to the laboratory for sorting. Fish larvae were
removed from each net and identified to the lowest
Manuscript accepted July 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
2Tareq and Co., 8460 S.W. 68th Street, Miami, FL 33143.
3Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
935
FISHERY BULLETIN: VOL. 84, NO. 4
94°00W
93 00 W
92°00W
I
9100 W
i
90°00W
I
89 OOW
— J—
31°00N
30 OON-
29 OON-
GULF OF MEXICO
Figure 1.— Location of study area.
possible taxon, and standard length was measured
with an ocular micrometer; all specimens were sub-
sequently archived in 70% ethanol. Hydrographic
profiles of the water column were taken at approx-
imately 1-1.5 m intervals with a Martek Mark VI
water quality monitor, except during January, Feb-
ruary, and September 1982 when the Martek unit
was inoperable. During these 3 mo, water temper-
atures and salinities were measured with a Beckman
RS-5 inductive salinometer near surface, middepth,
and bottom. Estimates of monthly mean larval den-
sities were calculated by dividing total larvae by
total volume filtered at each depth and integrated
over depth. Densities are expressed as number/ 100
m3. Seasonal designations were based primarily on
mean surface water temperatures during the year:
<20°C (Winter: December-February); 20°-25°C
(Spring: April-May); >25°C (Summer: June- August);
and rapidly declining surface water temperatures
(Fall: September-November).
Additional data on larval occurrence and season-
ality only were compiled from surface-towed meter
net (0.363 mm mesh) collections at stations sampled
between January 1981 and December 1982. These
data consisted of four nearshore stations located
adjacent to the bongo stations and were sampled
monthly. Two additional groups of stations, one of
four and the other of five stations, were located
about 24 km south of the nearshore stations in
depths of about 30 m. Each group of offshore sta-
tions was sampled quarterly but on consecutive
months during 1981; thereafter, monthly samples
were collected only at the four station group. These
seasonality data are not discussed but are included
in the Appendix Table.
Ancillary occurrence and seasonality data on lar-
val bothids, scombrids, and sciaenids collected off
Louisiana during the spring and early summer of
1982 were compiled from surface-towed 0.5 m ring
net (0.505 mm mesh), 60 cm bongo net (0.333 mm
mesh), and surface-towed 1 x 2 m neuston net
(0.946 mm mesh) samples (SEAMAP 1983). Bongo
tows were oblique and from the surface to 200 m
or within 5 m of the bottom at shallower depths.
Seasonality data for these taxa were compiled only
from stations located between long. 88°30'W and
93°30'W and shoreward of lat. 27°00'N and, al-
though not discussed, are also included in the
Appendix Table. Additional station and cruise data
are provided in Richards et al. (1984).
936
DITTY: ICHTHYOPLANKTON IN NERITIC WATERS
RESULTS
Taxonomic Problems
Larvae of many fishes in the northern Gulf of
Mexico are poorly known and taxonomic problems
are common, even in some of the most abundant
taxa. No attempt was made to identify blennies,
gobies, myctophids, synodontids, or cynoglossids to
species because of the paucity of literature on lar-
val development for these taxa. Little is also known
about the taxonomy and morphological development
of engraulid larvae. At least five species of engrau-
lids are known to occur as adults in the north-central
Gulf: Anchoa mitchilli, A. hepsetus, A. lyolepis, A.
cubana, Anchoviella perfasciata (Modde and Ross
1981), and possibly Engraulis eurystole (Hastings
1977). Anchoa mitchilli, A. hepsetus, and A. lyolepis
probably account for most of the engraulid larvae
collected. Larvae of A. hepsetus and A. mitchilli in
the Chesapeake Bay Region can be distinguished
from each other primarily on placement of dorsal
and anal fins (Manseuti and Hardy 1967), but this
character is insufficient to separate reliably the addi-
tional species of anchovy that may occur in this area.
Separation of menhaden larvae is also difficult.
Three species of menhaden are known to occur as
adults in this area: Brevoortia smithi (Chandeleur
Sound, LA, eastward), B. patronus (Tampa Bay, FL,
westward to Veracruz, Mexico) and B. gunteri
(Mississippi Sound, MS, westward) (Christmas and
Gunter 1960; Springer and Woodburn 1960; Dahl-
berg 1970; Turner 1971). Published descriptions are
available for laboratory-reared larvae of B. smithi
(Houde and Swanson 1975) and B. patronus (Hettler
1984) only. Brevoortia gunteri have never been
described nor positively identified from the north-
ern Gulf. Although the congeners have spawning
seasons that reportedly overlap, the center of
spawning of B. patronus is apparently off Louisiana
between the Mississippi and Atchafalaya River
Deltas (Turner 1969; Fore 1970; Christmas and
Waller 1975). Since Brevoortia larvae collected dur-
ing this study appear similar to that described as
B. patronus (Hettler 1984) and because I have recog-
nized in subsequent samples (at sizes >7 mm SL) a
second morph that could be B. gunteri, all larvae
were considered B. patronus.
Published descriptions of sciaenid larvae are in-
adequate to reliably distinguish between small
larvae of the species of Menticirrhus (M. ameri-
canus, M. littoralis, and M. saxatilis) or between
small Cynoscion arenarius and C. nothus. Two types
of C. arenarius larvae were recognized primarily on
the absence (Type A) or presence (Type B) of pig-
ment in the dorsal midline immediately above the
enlarged melanophore located in the ventral mid-
line about midway along the anal fin base. Additional
data on the separation of these types are provided
in Cowan (1985). Small carangid larvae (<5 mm SL)
of certain taxa are also difficult to identify and were
referred to a morphological type when a generic or
specific epithet could not be assigned. The taxonomy
and/or larval development of some of the other
monthly dominants (e.g., Lepophidium spp., Ophi-
dion spp., Auxis spp., and Ariomma sp.) are poorly
understood.
Hydrography
Water temperatures between November 1981 and
October 1982 ranged from 16°C in January and Feb-
ruary to 31° C in June and were below 20 °C from
December through February and above 25 °C from
May through October. There was little thermal
stratification except during the summer, with
stratification most pronounced in June (Fig. 2A).
Salinity stratification was most pronounced from
February through August, with little stratification
from September through January. Salinities were
lowest near the surface, increased with depth, and
ranged from <20%o near the surface in February
to 32%o in December; salinities near the bottom
ranged from 31%o in September to 36%o in the
spring and early summer. Salinities near the sur-
face steadily decreased from April through July and
increased thereafter, whereas those near the bot-
tom were comparatively more stable throughout the
study period (Fig. 2B). In February, there was a
distinct salinity gradient within the upper 6 m of the
water column that ranged from 18°/oo at the sur-
face to 30°/oo near middepth. In June, two distinct
water masses were present with a halocline near
middepth. Salinities of these two water masses dif-
fered by about 10%o with the less saline waters
above middepth (Fig. 2B). Further information on
water temperature and salinity variability and the
physical processes that affect the hydrography of
the study area are provided in Wiseman et al. (1982).
Seasonal Composition and Abundance
At least 48 families of fishes were represented in
bongo net samples that included 107 taxa, 54 of
which were identified to species. About 36,500 lar-
vae were collected, with <5% (primarily damaged
or yolk-sac larvae) unidentifiable to family. The
majority of larvae collected were <5 mm SL except
937
FISHERY BULLETIN: VOL. 84, NO. 4
N
M
N
M J
J A
Figure 2.— Profiles of water temperature and salinity (November 1981-October 1982) at a representative station from the study area
located in neritic waters of the northern Gulf of Mexico off Louisiana. A. Water temperature, B. Salinity. X indicates sampling depths.
Collection dates were scaled by Julian calendar.
larvae of clupeiform fishes; these were usually <10
mm SL.
Generally, seasonal larval densities followed water
temperatures (T) and were lowest during winter (X
= 51/100 m3 at T <20°C), increased during the
spring (X = 207/100_m3 at T <25°C), peaked
during the summer (X = 394/100 m3 at T near
30°C), and declined during the fall (X = 179/100
m3 at rapidly declining T). Approximately 6% of all
fish larvae were collected during the winter and
47.5% during the summer. Larval densities were
lowest in December and highest in June, with a
mean monthly density of 208/100 m3 (Fig. 3). Over-
all, December had the fewest taxa (13) and Septem-
ber the most (37). Five families accounted for about
90% of total larvae: Engraulidae, Sciaenidae,
Clupeidae, Carangidae, and Bothidae. The five most
abundant taxa overall, in order of decreasing abun-
dance, were anchovies (Engraulidae); Atlantic
croaker, Micropogonias undulatus; Atlantic thread
herring, Opisthonema oglinum; gulf menhaden,
Brevoortia patronus; and Atlantic bumper, Chloro-
scombrus chrysurus. These taxa accounted for about
82% of all larvae taken. Thirty-eight taxa occurred
in sufficient numbers that they were within the 10
most abundant taxa collected in at least one month.
Densities of these taxa are presented in Table 1.
Anchovies accounted for about 49% of all larvae
938
DITTY: ICHTHYOPLANKTON IN NERITIC WATERS
and were collected throughout the year, but were
most abundant in June and least abundant in
November (Table 1). Anchovies accounted for 65%
of all larvae taken during the spring and 69% dur-
ing the summer, but declined to about 6% of all lar-
vae collected during the fall and winter, respectively;
anchovies were the second most abundant taxon col-
lected during the winter and were fourth during the
fall. Most anchovy larvae were collected near the
surface and middepths; only 11% were collected
near the bottom. A few flat anchovy, Anchoviella
perfasciata, postlarvae were collected in February
only.
Atlantic croaker accounted for 66% of all sciaenid
larvae and were most abundant in November (Table
1). This species accounted for 58% of all larvae taken
during the fall and for 14% of larvae overall. Most
Atlantic croaker (65%) were collected near middepth
with only 1% collected near the surface. Two types
of sand seatrout, Cynoscion arenarins, were recog-
nized with Type A collected from April to September
and Type B from April to October. Of all sand
seatrout larvae taken, 60% were Type A and 40%
Type B, with Type A the second and Type B the
third most abundant of all sciaenid larvae. Density
of Type A exceeded that of Type B until September
o
o
2
uj
Q
<
>
M A
MONTH
Figure 3.— Density of ichthyoplankton (no./lOO m3) by month,
from neritic Gulf of Mexico waters off Louisiana, November 1981-
October 1982.
and October when Type B were more abundant
(Table 1). Most Type A (66%) and Type B (56%) lar-
vae were collected near the bottom with <5% of
Type A and of Type B larvae, respectively, collected
near the surface. Larvae of red drum, Sciaenops
ocellatus, were taken during the fall only and were
most abundant in September, whereas Menticirrhus
spp. were collected in all months except December
and January and were most abundant in October
(Table 1). Larval densities of other less abundant
sciaenids that included black drum, Pogonias cromis;
banded drum, Larimus fasciatus; spot, Leiostomus
xanthurus; silver perch, Bairdiella chrysoura; and
silver seatrout, Cynoscion nothus, never exceeded
1/100 m3. Densities of star drum, Stellifer lance-
olatus, and spotted seatrout, C. nebulosus, were
<2/100 m3 for any month.
Larvae of both the scaled sardine, Harengula
jaguana, and Atlantic thread herring were collected
from April to October, whereas gulf menhaden were
collected from October to February and round her-
ring, Etrumeus teres, only in January and February.
No larvae of Spanish sardine, Sardinella sp., were
identified. Densities of Atlantic thread herring were
greatest in June, scaled sardine in July, and gulf
menhaden in January. Densities of Atlantic thread
herring accounted for about 58% of all clupeid larvae
and for 9% of larvae overall; gulf menhaden
accounted for 34% of all clupeids and for 5% of lar-
vae overall. Scaled sardine accounted for 8% of all
clupeid larvae. Atlantic thread herring was the sec-
ond most abundant taxon collected in each season
except winter, and accounted for 88% of all clupeid
larvae collected between April and October; gulf
menhaden accounted for 73% of all winter larvae.
Over 99% of Atlantic thread herring and 80% of
scaled sardine were collected when surface water
temperatures were above 25°C; 90% of gulf men-
haden were taken at water temperatures below
20°C. Most scaled sardine (79%) larvae were taken
near the surface and only 2% near the bottom. Men-
haden larvae were abundant at all depths with 37%
collected near the surface and 24% near the bottom.
Atlantic thread herring were most abundant near
middepth (62%) and least abundant near the surface
(6%).
Larvae of Atlantic bumper were collected from
June to October but were most abundant in July.
This species accounted for about 5% of all larvae
and was the third most abundant taxon collected
during both the summer and fall months. Atlantic
bumper accounted for about 94% of all carangid lar-
vae with most bumper (94%) collected when surface
water temperatures averaged 30°C. Atlantic
939
FISHERY BULLETIN: VOL. 84, NO. 4
Table 1 .—Densities (no./1 00 m3) of abundant taxa from neritic waters of the northern Gulf of Mexico off Louisiana,
November 1981 -October 19821.
Taxa
Nov.
Dec.
Jan.
Feb.
Apr.
May
June
July
Aug.
Sept.
Oct.
Engraulidae
0.8
4.0
1.6
2.9
193.8
74.3
598.1
213.4
3.0
27.6
3.3
Brevoortia patronus
7.3
2.7
67.1
41.0
0.8
1.4
Etrumeus teres
—
—
0.4
0.2
—
—
—
—
—
—
—
Opisthonema oglinum
—
—
—
—
0.3
52.1
71.9
2.3
16.6
62.5
(2)
Harengula jaguana
—
—
—
—
5.7
0.2
—
11.9
9.5
0.2
(2)
Synodontidae
(2)
—
(2)
0.6
—
0.3
—
—
—
—
—
Myctophidae
(2)
—
1.0
7.2
0.4
Bregmaceros canton
0.4
(2)
—
0.1
0.3
0.5
—
—
—
—
0.1
Lepophidium spp.
0.9
Ophidion spp.
0.6
Membras martinica
—
—
—
(2)
1.0
(2)
Carangidae Type A
—
—
—
—
—
1.5
—
—
—
—
—
Chloroscombrus chrysurus
7.8
48.3
13.5
39.2
6.7
Oligoplites saurus
1.3
2.8
—
—
—
Trachurus lathami
— ;
—
—
0.4
—
—
—
—
—
—
—
Orthopristis chrysoptera
—
—
—
(2)
1.0
—
—
—
—
—
—
Archosargus probatocephalus
—
—
—
—
2.9
—
—
—
—
—
—
Lagodon rhomboides
(2)
—
0.3
0.4
Cynoscion arenarius (Type A)
—
—
—
—
22.5
6.3
7.2
17.2
10.3
1.9
—
Cynoscion arenarius (Type B)
—
—
—
—
10.6
0.8
6.7
11.1
10.2
5.7
1.5
Leiostomus xanthurus
0.8
0.5
0.1
0.2
Menticirrhus spp.
(2)
—
—
(2)
1.2
0.4
1.4
2.5
0.1
2.0
5.2
Micropogonias undulatus
182.8
2.8
—
2.2
126.4
Sciaenops ocellatus
12.8
6.3
Stellifer lanceolatus
—
—
—
—
1.4
0.1
1.6
0.3
0.3
0.3
0.2
Chaetodipterus faber
(2)
0.6
5.5
0.1
1.3
—
Mugil cephalus
—
—
0.4
(2)
—
—
—
—
—
—
—
Blennidae
0.3
1.6
0.6
(2)
2.8
9.0
1.2
2.0
0.2
0.9
0.1
Gobiidae
0.4
1.0
—
0.4
0.6
0.8
0.2
0.2
—
0.2
0.4
Auxis spp.
—
—
—
—
0.2
1.0
—
—
—
0.5
0.1
Scomberomorus maculatus
—
—
—
—
0.5
0.1
1.7
5.5
4.8
1.5
—
Ariomma sp.
—
—
0.7
—
—
—
—
—
—
—
—
Peprilus burti
1.4
0.1
0.5
0.9
0.1
0.2
0.1
—
—
—
0.5
Peprilus paru
0.4
0.6
0.5
0.6
4.4
(2)
Etropus crossotus
0.4
—
—
—
—
9.0
9.4
1.9
(2)
0.7
0.5
Citharichthys spilopterus
0.4
(2)
0.4
0.6
0.1
—
—
(2)
—
—
—
Symphurus spp.
0.5
0.1
—
—
0.1
1.5
2.8
1.4
0.1
0.5
0.2
Myrophis punctatus
(2)
0.1
0.1
0.2
Wo data for March 1982.
2Density <0. 1/100 m3.
bumper were most abundant near middepth (60%)
and least abundant near the bottom (9%). Other
abundant carangids included leatherjacket, Oligo-
plites saurus; rough scad, Trachurus lathami; and
carangid Type A larvae. All carangid Type A lar-
vae were <4 mm SL and appear similar to that
described as the round scad, Decapterus punctatus,
by Aprieto (1974).
Larvae of gulf butterfish, Peprilus burti, occurred
from October to June and harvestfish, P. paru, from
May to October (Table 1). Most gulf butterfish (85%)
larvae were collected when surface water tempera-
tures were <25°C whereas all harvestfish were col-
lected when surface water temperatures were above
25°C. Spanish mackerel, Scomberomorus macula-
tus, larvae occurred from April to September but
were most abundant in July; most (96%) were col-
lected when surface water temperatures exceeded
25°C. Most Spanish mackerel (74%) larvae were col-
lected near middepth; only 5% were collected near
the bottom. King mackerel, 5. cavalla, larvae were
collected only in September and at a density
<0.5/100 m3.
Many taxa occurred in relatively low abundance,
and although not included in Table 1, provided addi-
tional data on seasonality. These data are presented
in the Appendix Table. Only taxa with larvae <10
mm SL for a given month (except anguilliform lepto-
cephali or sygnathids) were included in the Appen-
dix Table, except where noted.
DISCUSSION
Data on peak seasonal occurrence of many of the
abundant taxa from the present study agree with
those of other coastal surveys from the north-central
Gulf of Mexico off Mississippi (Stuck and Perry
1982) and off Alabama (Williams 1983). During
1982, greatest densities of larval menhaden off
central Louisiana (the present study) occurred in
940
DITTY: ICHTHYOPLANKTON IN NERITIC WATERS
January-February and off western Louisiana (Shaw
et al. 1985) in February-March. Stuck and Perry
(1982) found larval menhaden most abundant be-
tween January and March adjacent to Mississippi
Sound. These data agree with past studies (Fore
1970; Christmas and Waller 1981) from this area
that reported high densities of menhaden eggs
between December and February. All three of the
north-central Gulf studies (Stuck and Perry 1982;
Williams 1983; and the present study) reported
greatest densities of Atlantic croaker during Octo-
ber and November; densities of sand seatrout were
greatest in April, with a second smaller peak in den-
sity during either July or August. Both Atlantic
bumper and Spanish mackerel were most abundant
from July to September in each of these three
studies. Stuck and Perry and the present study also
found the greatest density of red drum in Septem-
ber; Williams did not sample in September. In the
present study, Atlantic thread herring were most
abundant in June, with a second peak in September;
scaled sardine were most abundant during July and
August. Few scaled sardine and Atlantic thread her-
ring larvae were collected by Williams; no Atlantic
thread herring and few scaled sardine were collected
by Stuck and Perry. All three of these north-central
Gulf studies also reported a bimodal peak in abun-
dance of engraulids but differed slightly in month
of peak density. Stuck and Perry, and Williams
found greatest densities in April, with a second
smaller peak in August. The smaller of the two
peaks in abundance of engraulids occurred in April,
with the greatest density in June in the present
study (Table 1).
Comparison of dominant families and taxa col-
lected overall in the present study with those of
other ichthyoplankton surveys throughout the Gulf
of Mexico are presented in Tables 2 and 3. Lower
bay/coastal surveys were those conducted primarily
inside the 10 m depth contour, except for Hoese
(1965), who had a single transect of six stations out
to 50 m. Offshore surveys were those conducted
mainly in waters deeper than 10 m but shoreward
of the edge of the continental shelf. Although not
all the data listed in Tables 2 and 3 are directly com-
parable because of differences in gear type, mesh
size, or tow, these studies provide general informa-
tion on larval composition and abundance.
Most of the surveys from coastal waters (Hoese
1965; Blanchet 1979; Williams 1983; Collins and
Finucane 1984; and the present study) found that
engraulids dominated the summer ichthyoplankton,
whereas Stuck and Perry (1982) reported engraulids
second to Atlantic bumper in abundance. However,
Stuck and Perry may have undersampled small
engraulid and clupeid larvae because of the large
mesh (1.050 mm) of their nets. Menhaden dominated
the winter ichthyoplankton in all of the aforemen-
tioned coastal surveys, except Collins and Finucane
(1984). These authors found that pigfish, Orthopris-
tis chrysoptera, larvae were the most abundant taxa
during the winter in waters off the Everglades of
south Florida. All of these surveys also consistent-
ly placed engraulids and sciaenids at or near the top
in total larval abundance. Overall, clupeids were
relatively more abundant off south Florida (Collins
and Finucane 1984) than in the other coastal
surveys, except Hoese (1965), who sampled only the
Table 2.— Comparison of the five most abundant families collected overall from neritic waters off Louisiana with other ichthyoplankton
surveys throughout the Gulf of Mexico.
Engraulidae
Sciaenidae
Clupe
idae
Carangidae
Bothidae
Gear type, mesh size,
depth of tow,
Study
Rank
%
Rank
%
Rank
°/o
Rank
°/o
Rank
%
Location
and region1
Present study
1
49.0
2
19.0
3
16.0
4
5.5
5
1.5
Coastal
1,6,9,10,11,15
Hoese 1965
2
42.0
3
7.0
1
45.0
—
0.5
—
0.5
Coastal
2,4,9,14
Stuck and Perry
2
19.7
3
18.2
6
3.4
1
38.8
4
5.6
Coastal
3,8,9,11,15
1982
Williams 1983
1
69.3
2
14.5
3
4.5
4
2.8
—
0.5
Lower Mobile
Bay/Coastal
3,7,9,11,15
Blanchet 1979
1
75.8
2
4.9
8
1.9
7
2.2
<0.1
Lower
Apalachicola
Bay/Coastal
2,6,7,9,16
Collins and
2
22.5
4
6.9
1
24.1
5
6.1
—
<0.1
Coastal
2,7,9,12,18
Finucane 1984*
Finucane et al. 19793
5
6.2
—
<0.1
3
8.1
8
3.7
6
6.1
Offshore
1,7,13,14
Houde et al. 1979
12
2.0
30
0.3
1
20.5
6
3.9
3
6.4
Offshore
1,2,7,12,17
'1 60 cm bongo
7 0.505 mm
13 double-obliq
ue
2inshore data only
2 1 m
8 1 .050 mm
14 west-central
31977
bongo
net data only
3 1 x 0.5 m rectangu
lar
9 surface
15 north-centra
I
4 0.086 mm
10 middepth
16 north-east
5 0.333 mm
11 bottom
17 east-central
6 0.363 mm
12 oblique
18 south-east
941
Table 3.-
FISHERY BULLETIN: VOL. 84, NO. 4
-Comparison of five most abundant taxa from neritic waters off Louisiana with ichthyoplankton surveys
throughout the Gulf of Mexico.
Stuck
Collins
and
and
Finucane
Houde
Present
Hoese
Perry
Williams
Blanchet
Finucane
et al.
et al.
study
1965
1982
1983
1979
19841
19792
1979
Taxa
%
%
%
%
%
%
%
%
Engraulidae
49.0
19.7
69.0
75.8
22.5
7.1
Micropogonias undulatus
14.0
5.8
Opisthonema oglinum
9.0
4.5
7.9
Brevoortia patronus
5.0
15.6
4.3
Chloroscombrus chrysurus
5.0
38.4
2.8
1.8
4.8
Harengula jaguana
29.1
Anchoa hepsetus
24.0
Anchoa mitchilli
17.7
Menticirrhus spp.
2.6
Cynoscion arenarius
12.0
8.2
Citharichthys-Etropus complex
5.6
Symphurus spp.
3.8
Atherinidae
3.9
Gobiesox strumosus
3.2
Gobiosoma spp.
2.7
Microgobius spp.
9.1
Orthopristis chrysoptera
4.8
Gobiidae
15.8
15.1
Bregmaceros atlanticus
7.1
Saurida spp.
6.1
Syacium spp.
4.1
Sardinella anchovia
8.6
Decapterus punctatus
3.1
Diplectrum formosum
2.8
1 1nshore data only.
21977 bongo net data only.
surface waters of his offshore transect (Table
2).
Offshore, Houde et al. (1979) found that clupeids
(Spanish sardine and Atlantic thread herring),
gobiids, and bothids (mostly dusky flounder, Sya-
cium papillosum) dominated summer ichthyoplank-
ton in the eastern Gulf of Mexico off Florida, where-
as clupeids (round herring and Spanish sardine),
bothids (mostly gray flounder, Etropus rimosus),
and bregmacerotids dominated the winter. In the
western Gulf of Mexico off the south Texas coast,
Finucane et al. (1979) reported that, during 1977,
clupeids (mostly scaled sardine) and bothids (most-
ly Syacium spp.) dominated the summer and breg-
macerotids and clupeids (menhaden) the winter
ichthyoplankton. In the northern Gulf of Mexico off
Louisiana, Ditty and Truesdale (1984) found that
engraulids and carangids (mostly Atlantic bumper)
dominated the summer (July 1976), whereas larvae
of clupeids (mostly gulf menhaden) and gobiids
dominated the winter (January-February 1976). The
most abundant families collected overall off Florida
were clupeids and gobiids (35.6% of all larvae), and
off south Texas were gobiids and synodontids
(26.7% of all larvae). The kinds of larvae (gobiids,
bothids, clupeids, and bregmacerotids) that domi-
nated these two offshore surveys were similar, but
with clupeids and bothids relatively more abundant
off Florida than Texas; engraulids were relatively
more abundant off south Texas than off Florida
(Table 2). Ditty and Truesdale (1984) found clupeids
and engraulids most abundant overall (67.7% of all
larvae), but their surveys were too limited temporal-
ly and in areal coverage for adequate comparison
to the other two offshore surveys.
The 10 most abundant families accounted for
66.6% of all larvae collected off Florida (Houde et
al. 1979) and for 68.6% off south Texas (Finucane
et al. 1979). In contrast, the top 10 families in each
of the coastal surveys contributed over 90% of all
larvae collected. Likewise, the five most abundant
taxa contributed over 80% of all larvae collected in
all but one (Collins and Finucane 1984) of the coastal
surveys but <40% in the two offshore surveys (Table
3).
In conclusion, there was general agreement
among all three coastal surveys from the north-
central Gulf of Mexico on peak seasonal occurrence
of many of the abundant taxa and on the dominant
families in overall larval abundance. Comparison of
other coastal and offshore ichthyoplankton surveys
throughout the Gulf of Mexico with the present
study suggests that, when compared with offshore
waters, there are relatively fewer dominant taxa
942
DITTY: ICHTHYOPLANKTON IN NERITIC WATERS
among the ichthyoplankton in neritic waters of the
Gulf of Mexico.
ACKNOWLEDGMENTS
This study represents a portion of an ongoing
multiyear synoptic environmental assessment of the
Louisiana Offshore Oil Port (LOOP, Inc.) and related
facilities conducted by the Louisiana Department of
Wildlife and Fisheries. I would like to thank Robert
Ganczak and R. Harry Blanchet for their support
and advice; Carlos Garces for statistical guidance;
Jill Onega for typing the various drafts of the manu-
script; Ron Gouguet for computer programming
expertise, collection of hydrographic data, and
generating the hydrographic profile plots; and to
acknowledge Frank M. Truesdale, R. Harry Blan-
chet, and the other reviewers for their valuable com-
ments and suggestions for manuscript improve-
ment. Thanks to the captain and crew of the LOOP
Vigilance, to LOOP Inc., and to the Louisiana
Department of Wildlife and Fisheries for additional
support. Thanks also to the Southeast Area Monitor-
ing and Assessment Program (SEAMAP) for pro-
viding data on the bothids, sciaenids, and scombrids
collected off Louisiana during 1982 and to William
J. Richards and Tom Potthoff for identifying the
SEAMAP scombrids.
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943
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944
DITTY: ICHTHYOPLANKTON IN NERITIC WATERS
Appendix Table.— Seasonality of larval fishes in the northern Gulf of Mexico off Louisiana, January 1981 -December 1982.
Taxa Jan. Feb. Mar. Apr. May June July Aug. Sept. Oct. Nov. Dec.
Neoconger mucronatus ....
Muraenidae
Gymnothorax sp.
Hoplunnis sp.
Congridae ....
Ophichthidae .... .... ....
Bascanichthys bascanium
Myrophis punctatus
Ophichthus gomesii .... ....
Pseudomyrophis 'D' ....
Brevoortia patronus
Etrumeus teres
Harengula jaguana
Opisthonema oglinum
Sardinella sp. ....
Engraulidae
Anchoviella perfasciata^ ....
Gonostomatidae ....
Cyclothone sp. ....
Vinciquerria nimbaria ....
Synodontidae .... ....
Paralepidae ....
Lestidiops affinis
Myctophidae
Centrobranchus nigriocellatus ....
Diaphus sp.
Diogenichthys atlanticus ....
Hygophum sp. ....
Lampanyctus sp. ....
Gobiesox strumosus
Ceratiodei .... ....
Antennariidae .... ....
Gigantactinidae
Bregmaceros cantori
Bregmaceros atlanticus
Urophycis spp.
Ophidiidae .... ....
Brotula barbata
Lepophidium spp.
Ophidion spp.
Ophidion welshilgrayi .... ....
Ophidion selenops .... ....
Exocoetidae .... .... ....
Hyporhamphus unifasciatus
Atnerinidae .... .... ....
Membras martinica
Holocentrus sp. ....
Macrorhamphosus scolopax
Syngnathus spp. .... ....
Serranidae
Anthinae .... ....
Hemanthias leptus ....
Grammistinae ....
Rypticus maculatus ....
Serraninae ....
Serraniculus pumilio ....
Pomatomus saltatrix ....
Carangidae Type A2 ....
Carangidae Type B2 .... .... ....
Carangidae Type C2
Carangidae Type D2 ....
Chloroscombrus chrysurus
Oligoplites saurus
Selene sp.
Trachurus lathami
Coryphaena equiselis ....
Lutjanus sp.
Gerreidae ....
Orthopristis chrysoptera . . . . ....
Archosargus probatocephalus
945
FISHERY BULLETIN: VOL. 84, NO. 4
Appendix Table.— Continued.
Taxa Jan. Feb. Mar. Apr. May June July Aug. Sept. Oct. Nov. Dec.
Lagodon rhomboides
Bairdiella chrysoura
Cynoscion arenarius Type A
C. arenarius Type B
C. nebulosus
C. nothus
Larimus fasciatus
Leiostomus xanthurus
Menticirrhus spp.
Micropogonias undulatus
Pogonias cromis
Sciaenops ocellatus
Stellifer lanceolatus
Mullidae
Chaetodipterus faber
Labridae
Scaridae
Mugil cephalus •
Mugil curema
Sphyraena spp.
Blennidae
Callionymus pauciradiatus
Gobiidae
Gobionellus hastatus
Microdesmus spp.
Diplospinus multistriatus
Trichiurus lepturus
Auxis sp.
Euthynnus alletteratus
E. pelamis
Scomber japonicus
Scomberomorus cavalla
S. maculatus
Thunnus albacares
T. atlanticus
T. thynnus
Ariomma sp.
Cubiceps pauciradiatus
Nomeus gronovii
Peprilus burti
P. paru
Scorpaena spp.
Prionotus spp.
Dactylopterus volitans
Bothus sp.
Citharichthys sp.
Citharichthys sp. Type A
Citharichthys sp. Type B
Citharichthys sp. Type C
C. cornutus
C. gymnorhinus
C. spilopterus
Cyclopsetta sp.
Engyophrys senta
Etropus crossotus
Monolene sessilicauda
Paralichthys sp.
Syacium sp.
S. gunteri
S. papillosum
Trichopsetta ventralis
Achirus lineatus
Trinectes maculatus
Symphurus spp.
Monacanthus setifer
Sphoeroides spp.
'Juveniles.
2Morph Type A may represent Decapterus lEIagatis; Type B - Selar crumenopthalamus; Type C - Seriola spp.; Type D - Caranx spp.
946
STOMACH CONTENTS AND FOOD CONSUMPTION ESTIMATES OF
PACIFIC HAKE, MERLUCCIUS PRODUCTUS1
Eric A. Rexstad2 and Ellen K. Pikitch3
ABSTRACT
Analysis of 466 stomachs of Pacific hake, Merluccius productus, collected during August 1983 off the
coasts of Washington and Oregon indicates euphausiids comprise the most important food resource in
terms of percent by weight, numbers, and frequency of occurrence for the species at that time of year.
The importance of fish in the Pacific hake diet increases with the size of the hake, constituting 87% of
the diet by weight in the largest individuals. Weak evidence of a nocturnal feeding pattern was observed.
This indistinct nocturnal feeding pattern could have been caused by poor food availability due to El Nino.
Estimates of food consumption by Pacific hake indicate that this species may have a substantial impact
on some commercially valuable species such as pink shrimp, Pandalus jordani, even though pink shrimp
is a fairly minor component of the diet. A statistically significant negative relationship between Pacific
hake catch-per-unit-effort (CPUE) and pink shrimp CPUE off the west coast of the United States, using
a lag of 2 years, was found.
Pacific hake, Merluccius productus, constitute an
important component of the California Current
ecosystem off the west coast of North America.
It is estimated that a standing stock of approx-
imately 1.5 million metric tons (t) exists off the
Pacific coast between central California and Van-
couver Island (Bailey et al. 1982). This biomass
represents a substantial prey base for a variety of
fish in the ecosystem: great white sharks, Car-
charodon carcharias; soupfin sharks, Galeorhinus
zyopterus; Pacific electric ray, Torpedo californica;
bonito, Sarda chiliensis; albacore, Thunnus
alalunga; bluefin tuna, Thunnus thynnus; rock-
fishes, Sebastes spp.; sablefish, Anoplopoma fimbria;
lingcod, Ophiodon elongatus; dogfish, Squalus acan-
thias; and arrowtooth flounder, Atheresthes stomias
(Bailey et al. 1982). Pacific hake also constitute a
major prey item for a number of marine mammals,
including the California sea lion, Zalophus califor-
nianus; northern sea lion, Eumetopias jubatus;
northern fur seal, Callorhinus ur sinus; saddleback
dolphin, Delphinus delphis; Pacific whiteside
dolphin, Lagenorhynchus obliquidens; and northern
right whale dolphin, Lissodelphis borealis (Fiscus
1979).
'Technical paper No. 7718, Oregon Agricultural Experimental
Station.
department of Fisheries and Wildlife, Hatfield Marine Science
Center, Oregon State University, Newport, OR 97365; present
address: Colorado Cooperative Fish and Wildlife Research Unit,
Department of Fishery and Wildlife Biology, Colorado State
University, Ft. Collins, CO 80523.
department of Fisheries and Wildlife, Hatfield Marine Science
Center, Oregon State University, Newport, OR 97365.
Pacific hake also have an important impact on
species below them in the food chain. Best (1963)
described Pacific hake as opportunistic feeders.
Their diet includes numerous species of Crustacea,
particularly euphausiids, several genera of shrimp,
crab megalopae, and a variety of fish including
Pacific herring, Clupea harengus pallasi; rockfish;
sablefish; and flatfish (Livingston 1983). Pacific hake
may compete for food resources with a host of other
species that feed on the abundant euphausiid
resource (Tyler and Pearcy 1975; Karpov and
Cailliet 1978; Brodeur and Pearcy 1984), including
commercially prized salmonids (Peterson et al.
1982).
At the top of the trophic structure is the commer-
cial fishing fleet, comprised mainly of foreign joint-
venture fishing boats that have harvested, on
average, 127,000 t of Pacific hake per year since
1966 (R. C. Francis4).
Pacific hake migrate seasonally along the west
coast of North America (Swartzman et al. 1983) and
spawn in winter in the warm waters off southern
California and the Baja peninsula. During the spring
and summer, the adults migrate as far north as Van-
couver Island to feed. The Pacific hake tend to
stratify along the coast by size, with the largest in-
dividuals traveling farthest from the spawning areas
and smaller juveniles remaining off the coast of
California. In autumn, the adults return to the south-
ern spawning areas (Bailey et al. 1982).
4R. C. Francis, Fisheries Research Institute, University of Wash-
ington, Seattle, WA 98195, pers. commun. May 1985.
Manuscript accepted July 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
947
FISHERY BULLETIN: VOL. 84, NO. 4
The pink shrimp, Pandalus jordani, fishery off
Oregon was one of the most economically viable fish-
eries during the late 1970s with landings in excess
of 26,000 t in 1978. Subsequent to that time, pink
shrimp landings have declined, with slightly over
2,000 t being landed in 1984 (Saelens and Zirges
1985). The purpose of this study was to describe the
dietary habits of the Pacific hake and, in particular,
to determine whether predation by Pacific hake on
pink shrimp could explain some of the fluctuations
seen in pink shrimp landings.
MATERIALS AND METHODS
In August and September 1983, during the Na-
tional Marine Fisheries Service (NMFS) West Coast
Groundfish Survey, Pacific hake stomachs were
sampled from 41 hauls taken during daylight hours
between Coos Bay, OR, and Grays Harbor, WA (Fig.
1). Tows were of 0.5-h duration using a Nor'eastern5
high-opening bottom trawl equipped with roller gear
which has an approximate horizontal opening of 13.4
m and vertical opening of 8.8 m. Further details of
the sampling regime can be found in Gunderson and
Sample (1980) and Weinberg et al. (1984). Between
5 and 15 individuals of each sex from a 5 cm size
class (30-34 cm, 35-39 cm, 40-44 cm, 45-49 cm, 50-54
cm, 55 + cm) were sampled from each haul where
practical. A total of 466 stomachs were extracted
at sea and placed in cheesecloth bags. Stomachs with
evidence of regurgitated contents were not included
in the sample. Stomachs were preserved in a 10:1
solution of seawater to Formalin.
Stomach Content Analysis
In the laboratory, stomachs were transferred to
ethyl alcohol and examined under a dissecting micro-
scope. Stomach fullness and degree of digestion
were visually estimated and given a qualitative
rating (0-4 from empty to distended, and from un-
recognizable to recently consumed). Contents were
identified to the lowest taxon and enumerated. Wet
weight of each taxon was also determined.
Diet composition was characterized by percent of
total number of food items (%N), percent of total
diet by weight (%VF), and frequency of occurrence
in nonempty stomachs (FO). An index of relative im-
portance (IRI) was then derived from these values
IRI = FO (%N + %W) (Pinkas et al. 1971).
The data were further stratified by sex, time of
125
124'
5Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Figure 1.— Stations where Pacific hake stomachs were taken dur-
ing 1983 NMFS West Coast Groundfish Survey; 100 and 200 m
isobaths are also shown.
948
REXSTAD and PIKITCH: FOOD CONSUMPTION OF PACIFIC HAKE
collection (morning, afternoon, and evening), depth
of capture (0-100 m, 100-200 m, >200 m), and size.
Chi-square tests of homogeneity (Ostle and Mensing
1975) were performed on the frequency of occur-
rence data for each prey species in these categories.
Consumption Estimates
Using the size-specific prey consumption informa-
tion derived from this study, Pacific hake popula-
tion abundance estimates from the 1983 NMFS
survey (Weinberg et al. 1984; Francis fn. 4) and
bioenergetics estimates from Francis (1983), trophic
calculations were performed to estimate ecosystem-
level impacts of prey consumption by Pacific hake
in the Columbia INPFC (International North Pacific
Fisheries Commission) statistical area in 1983.
Biomass estimates were derived from two distinct
surveys. The bottom trawl survey estimated the ben-
thic component of the population. Details of these
estimates can be found in Weinberg et al. (1984).
The pelagic component of the population was esti-
mated by hydroacoustic methods. Size composition
of the pelagic segment of the population was esti-
mated from companion midwater trawls conducted
from the hydroacoustic vessel. Biomass estimates
for each of the five size classes sampled were deter-
mined from estimated numbers in each centimeter
size interval and length-weight regressions (Fran-
cis fn. 4).
Using a mean body weight for each size class, the
percent of total body weight consumed daily was
calculated based on the equations of Francis (1983).
This total biomass consumption was then broken
down into the constituent prey categories found in
the stomachs of fish sampled using the percent of
the diet by weight. These calculations were repeated
for each of the five classes, and both the pelagic and
benthic components of the population, to derive daily
consumption estimates.
Residence times provided by Francis (1983) for
each age class within each statistical area were con-
verted to residence time by size class to account for
the migratory behavior of Pacific hake. This pro-
vided consumption rate estimates summed over the
length of time Pacific hake are found in the Colum-
bia statistical area. An example of the calculations
used to estimate total consumption of each prey item
category is shown in Table 1.
Pacific Hake-Pink Shrimp Interaction
The relationship between the abundance of Pacific
hake and pink shrimp was examined via regression
Table 1.— Calculations used to compute total consumption of
Thysanoessa spinifera. Column E1 = A x B/100 x C/1 00. Column
E2 = E1 x D. Biomass is combined benthic and pelagic com-
ponents of the population, BWD is percent body weight consumed
per day, W is percent of the diet by weight composed of T. spini-
fera, and Days is number of days each size class resides in the
Columbia INPFC Area. Note total biomass differs from value given
in text due to biomass of population <35 cm in length.
(A)
(B)
(C)
(D)
(E1)
(E2)
Size
Consumption
class
Biomass
Daily
Seasonal
(cm)
(1,000 t)
%BWD
%W
Days
(1,000 t)
35-39
331.252
1.10
14.7
80
0.540
42.85
40-44
69.126
0.98
9.4
69
0.060
4.20
45-49
21.272
0.84
17.2
45
0.030
1.38
50-54
17.640
0.65
14.9
42
0.020
0.72
55 +
8.936
0.40
6.4
41
0.002
0.09
Total
448.226
0.652
49.24
analysis. Data from Francis et al. (unpubl. data) on
Pacific hake catches in U.S. waters from 1967 to
1982 were converted to catch per unit effort (CPUE)
based on the number of days of effort of foreign
stern-trawling factory ships (BMRTs). Pounds per
hour of pink shrimp taken in the equivalent of single-
rigged shrimp trawls (SRE) in California, Washing-
ton, and Oregon from 1968 to 1984 (Saelens and
Zirges 1985) were used as the dependent variable
in regression analyses.
Two regressions were performed. The first used
hake CPUE in year i to predict shrimp CPUE in
year i, while the second involved a 2-yr lag (i.e.,
Pacific hake CPUE in year i versus shrimp CPUE
in year i + 2).
RESULTS
Stomach Content Analysis
A breakdown of the stomach contents by size class
of Pacific hake is presented in Table 2. Euphausiids
dominate the diet of small hake while decapods and
fish become increasingly important as Pacific hake
increase in size. Considering percent of the diet by
weight, the importance of euphausiids monotonically
decreases from 100 to 7.9% with increasing predator
size. Likewise, the importance of fish rises from 0
to 87.1% with increasing predator size. Pink shrimp
comprise only a minor portion of the diet, the largest
percentage being 4.9% for the largest size class.
Commercially important herring comprise nearly
one-third of the diet of the larger size classes.
A previously unreported prey item, the ghost
shrimp, Callianassa sp., appeared in the diet of the
Pacific hake sampled in this study. These burrow-
949
FISHERY BULLETIN: VOL. 84, NO. 4
Table 2.— Summary of stomach contents of Merluccius productus collected during the 1983 NMFS Pacific Coast Groundfish Survey.
T = <0.1%.
30-34 cm
35-39 cm
40-44 cm
45-49 cm
50-54 cm
>55 cm
Prey category
FO1 %N2 %W3 FO %N %W FO %N %W FO %N %W FO %N %W FO %N %W
Euphausiacea
Thysanoessa spinifera — — — 14.9 15.0 14.7 27.5 10.6 9.4 32.5 79.6 17.2 52.4 65.1 14.9 61.9 62.3 6.4
Euphausia pacifica 25.0 16.7 17.1 56.4 73.7 72.7 68.1 78.5 70.8 10.4 9.0 2.2 19.5 18.7 3.9 33.3 23.4 1.3
Unidentified 100.0 83.3 82.9 33.0 10.4 6.2 33.3 10.3 10.7 31.2 9.2 2.5 35.4 12.4 1.9 19.0 9.0 0.2
Decapoda
Pandalus jordani — — — 1.1 T 0.2 — — — 1.3 0.1 0.1 — — — 19.0 2.3 4.9
Sergestes similis — — — 2.1 0.7 2.9 5.8 0.3 2.5 — — — — — — — — —
Pasiphaea pacifica — — — — — — 1.5 T 2.0 — — — — — — 14.3 1.5 0.4
Crangon sp. — — — — — — — — — 2.6 0.1 0.2 4.9 1.1 12.0 — — —
Callianassa sp. ___ ______ 11.7 o.7 13.4 8.5 1.1 14.5 — — —
Osteichthyes
Engraulis mordax — — — — — — — — — 1.3 0.1 1.5 2.4 0.3 2.7 — — —
Clupea harengus — — — — — — 2.9 0.1 3.8 3.9 0.2 34.7 3.7 0.2 28.4 — — —
Thaleichthys pacificus — — — — — — 1.4 T 0.6 9.1 0.4 23.0 1.2 0.1 T — — —
Osmeridae — — — — — — — — — 1.3 0.1 T 1.2 0.1 2.8 — — —
Gadidae — — — ———— — — 1.3 0.1 1.2 2.4 0.2 2.4 4.8 0.2 83.6
Pleuronectidae — — — — — — — — — 1.3 0.2 0.1 2.4 0.2 14.5 9.5 0.6 3.4
Agonidae ___ ___ ___ ___ 1.2 0.1 0.4 — — —
Myctophidae ___ 0.8 T 1.5 — — —— — —— — —— — _
Unidentified — — — 5.3 0.2 1.8 5.8 0.2 0.3 9.1 0.4 3.6 7.3 0.5 1.8 14.3 0.6 0.1
Number of stomachs
(empty) 11(7) 120(26) 97(28) 118(41) 93(11) 27(6)
Number of prey items 6 2,006 2,029 1,921 1,206 478
Weight of stomach
contents (g) 0.4 77.0 78.0 376.5 319.3 293.0
1 Frequency of occurrence in non-empty stomachs.
2Percent of diet by number of items.
3Percent of diet by weight of stomach contents.
ing animals were found in stomachs of Pacific hake
taken at towing stations between 8.3 and 15.6 km
(4.5 and 8.5 mi) offshore but not in immediate prox-
imity to estuaries where ghost shrimp are most
often found.
Chi-square tests (Table 3) illustrate the patterns
in prey consumption by various stratifications of the
data. There was little statistical difference in
stomach contents of males compared with females.
The analysis of prey categories by depth is essen-
tially an inshore-offshore comparison as isobaths run
roughly parallel to the coastline in the study area.
Statistically significant differences were found in
depth of capture for both species of euphausiids
found in this study. Thysanoessa spinifera was more
important in the diet of fish taken close to shore
whereas Euphausia pacifica was important for fish
taken futher offshore. Eulachon, Thaleichthys pacif-
icus, was found in stomachs more often in shallow
waters than at depth. These animals, being anad-
romous, are often found in bays and estuaries, i.e.,
close to shore.
A significant difference exists in the presence of
the two species of euphausiids in stomachs collected
at different times of the day. The data collected in
this study show that T. spinifera were seldom found
in stomachs collected after 1600 h while E. pacifica
Table 3.— Chi-square analysis of difference in stomach content
by prey category and various factors.
Factor
Sex
Depth
Time
Size
Prey category
df = 1
df = 2
df = 2
df = 4
Thysanoessa
spinifera
2.48
15.65***
23.67***
36.69***
Euphausia pacifica
1.42
17.45***
6.23*
76.90***
Pandalus jordani
0.48
1.02
3.53
39.60***
Sergestes similis
0.02
28.07***
0.12
9.86*
Pasiphaea pacifica
0.80
17.47***
3.92
34.39***
Crangon sp.
0.02
6.40*
3.07
8.27
Callianassa sp.
0.05
3.69
9.14*
20.30***
Engraulis mordax
0.46
0.68
3.87
3.99
Clupea harengus
0.76
3.95
10.14**
4.30
Thaleichthys
pacificus
0.72
9.35**
4.14
16.71**
Osmeridae
2.24
1.44
2.49
2.33
Gadidae
0.01
0.16
2.20
5.44
Pleuronectidae
4.55*
1.45
2.21
12.49*
' = P<, 0.05,
= P*S 0.01, *** =
P< 0.001.
were often found in stomachs collected during that
time (Fig. 2a).
To further examine the diel feeding pattern of
Pacific hake, the percent of all stomachs in each of
two fullness categories (<25% full; > 75% full) was
calculated by time of day. A three-point moving
average was computed for each fullness category,
and the resulting averages plotted (Fig. 3). There
950
REXSTAD and PIKITCH: FOOD CONSUMPTION OF PACIFIC HAKE
CD
O
c
05
O
Q.
E
"cd
DC
X
CD
~o
c
S>
Prey Consumption by Time of Day
-
70 1
60
CD
50 ■
05
■4— «
L.
O
Q_
40 ■
E
"CD
30 ■
DC
X
CD
"D
20 -
_C
10 ■
>>
0
A Thysanoessaspinifera
B Euphausia pacifica
C Pandalus Jordan i
D Sergestessp.
E Pasiphaea pacifica
F C rang on sp.
G Callianassasp.
H Engraulis mordax
I Clupeaharengus
J Thaleichthys pacificus
K Osmeridae
L Gadidae
M Pleuronectidae
800-1200
1200-1600
1600-2000
jj_*
t^TU i-l- Ixl - fca
A B C D E F G
— . n S.
1
Prey Category
Prey Consumption by Size Class of Predator
100 -
2
80 -
60 -
40 -
20 ~ff
.
- j
n .L
I
A Thysanoessaspinifera
B Euphausia pacifica
C Pandalus jordani
D Sergestessp.
E Pasiphaea pacifica
F Crangonsp.
G Callianassasp.
H Engraulis mordax
I Clupeaharengus
J Thaleichthys pacificus
K Osmeridae
L Gacf/c/ae
M Pleuronectidae
35-39cm
40 -44cm
45 -49cm
50 -54cm
55 + cm
jfl *_[]_
■ I - ji
K L M
JI
A B
D E F G H I
Prey Category
K L M
Figure 2.— Index of relative importance for major prey categories by a) time of collection and b) size of Pacific hake. Square
root transformation used for scaling purposes.
951
FISHERY BULLETIN: VOL. 84, NO. 4
100*
Percent Stomachs Mostly Full/Empty
75*
c
V
o
1_
V
0-
50* -
25*
0*
Stomochs less than 25* full
54
40
80
31
30
25
59
50
15
34
— i 1 1 1 1 1 —
10 11 12 13 14 15
Time (hours)
16
17
18
19
Figure 3.— Diel pattern of stomach contents of Pacific hake as demonstrated by percent
of stomachs <25% full (upper curve) and >75% full (lower curve). Three-point moving
average used to smooth the curves. Sample sizes shown above x-axis.
is a weak indication that these fish exhibit a pattern
of feeding more heavily at night than during the day.
For a predator feeding nocturnally, the expected
pattern of this curve would be low percentages of
empty stomachs early and late in the day, and high
percentages of empty stomachs at midday. No tows
were made between the hours of 2000 and 0700 thus
direct evidence of nocturnal feeding was not avail-
able.
Comparison of stomach contents by size class
showed the greatest amount of variation (Table 3,
Fig. 2b) because of the shift in diet composition from
euphausiids in early life stages to fishes in later
stages.
The estimated consumption by Pacific hake in the
Columbia statistical area over all prey categories is
4,651 t/d (Table 4). The amount of euphausiids con-
sumed (over 4 kt/d), exceeds that of all other prey
categories combined, but several commercially
valuable species are also consumed in significant
quantities. Consumption of pink shrimp is estimated
at over 9.2 t/d, and almost 120 t/d of herring are
consumed. Residence time for each size class of
Pacific hake was derived from data presented by
Francis (1983) (size class 1: 80 d; size class 2: 69 d;
size class 3: 45 d; size class 4: 42 d; and size class
5: 41 d) to extrapolate estimates of annual prey con-
sumption from the daily consumption rate in the
Columbia area. The annual consumption of pink
shrimp, based on these data, is estimated at 659.3 1.
Pacific Hake-Pink Shrimp Interaction
The regression of Pacific hake CPUE versus pink
shrimp CPUE resulted in a nonsignificant correla-
tion (r2 = 0.114, df = 15, P = 0.185). However,
the regression performed with a 2-yr lag (hake
CPUE in year i versus shrimp CPUE in year i +
2) showed a significant negative correlation between
the variables (r2 = 0.418, df = 15, P = 0.005).
Note that the significance of the latter analysis
stems largely from data obtained in recent years
(Fig. 4).
DISCUSSION
One of the most striking patterns found in the data
is the distinct change in diet composition that Pacific
952
REXSTAD and PIKITCH: FOOD CONSUMPTION OF PACIFIC HAKE
Table 4.— Diet composition by size class on a daily basis (t) and on seasonal basis (kt). Values based on biomass tor the Columbia
INPFC area estimated from bottom trawl survey (Weinberg et al. 1984) and hydroacoustic survey (Francis, see text fn. 4). T - <0.1
t/d or 0.05 kt seasonally.
Size 1
Size 2
Si
ze 3
Size 4
Size 5
Totals
Prey category
Daily
Season
Daily
Season
Daily
Season
Daily
Season
Daily
Season
Daily
Season
Euphausiacea
Thysanoessa spinifera
535.1
42.5
64.0
4.4
30.6
1.4
17.2
0.7
2.3
.0.1
649.2
49.1
Euphausia pacifica
2,646.4
210.4
481.8
33.2
3.9
0.2
4.5
0.2
0.5
T
3,137.1
244.0
Unid. euphausiid
225.7
17.9
72.8
5.0
4.5
0.2
2.2
0.1
0.1
T
305.2
23.3
Total euphausiid
3,407.3
270.9
618.6
42.7
39.0
1.7
23.9
1.0
2.8
0.1
4,091.6
316.4
Decapoda
Pandalus jordani
7.3
0.6
0.0
0.0
0.2
T
0.0
0.0
1.8
0.1
9.2
0.7
Sergestes sp.
105.6
8.4
17.0
1.2
0.0
0.0
0.0
0.0
0.0
0.0
122.6
9.6
Pasiphaea pacifica
0.0
0.0
13.6
0.9
0.0
0.0
0.0
0.0
0.1
T
13.8
1.0
Crangon sp.
0.0
0.0
0.0
0.0
0.4
T
13.8
0.6
0.0
0.0
14.2
0.6
Callianassa sp.
0.0
0.0
0.0
0.0
23.9
1.1
16.7
0.7
0.0
0.0
40.6
1.8
Osteichthyes
Engraulis mordax
0.0
0.0
0.0
0.0
2.7
0.1
3.1
0.1
0.0
0.0
5.8
0.2
Clupea harengus
0.0
0.0
25.9
1.8
61.8
2.8
32.8
1.4
0.0
0.0
120.5
5.9
Thaleichthys pacificus
0.0
0.0
4.1
0.3
41.0
1.8
0.1
T
0.0
0.0
45.1
2.1
Osmeridae
0.0
0.0
0.0
0.0
0.4
T
3.2
0.1
0.0
0.0
3.6
0.2
Gadidae
0.0
0.0
0.0
0.0
2.1
0.1
2.8
0.1
30.2
1.2
35.1
1.4
Pleuronectidae
0.0
0.0
0.0
0.0
0.2
T
16.7
0.7
1.2
0.1
18.1
0.8
Agonidae
0.0
0.0
0.0
0.0
0.0
0.0
0.5
T
0.0
0.0
0.5
T
Myctophidae
54.6
4.3
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
54.6
4.3
Unid. fish
65.5
5.2
2.0
0.1
6.4
0.3
2.1
0.1
T
T
76.1
5.7
Grand total
3,640.2
289.4
681.2
47.0
178.0
8.0
115.7
4.8
36.2
1.5
4,651.4
350.7
Shrimp CPUE (year i+2), Hake CPUE (year i)
800
700
600
in
500
UJ
z>
0.
o
400
a.
E
If)
300 -
200 -
100
D 75-77
68-70
D
D
66-68
70-72
a
D 73-75
-
D
71-73
76-78
a
67-69
D
69-71
□
□
72-74
74-76
a
-
77-79
□
i
i , . ...
,_, 80-82
79-81 u
81-83
-, P-
78-80
D
82-84
□
r 1
12 16 20 24
Hake CPUE (t/BMRT day)
28
32
36
Figure 4.— Pink shrimp CPUE in year i + 2 (y-ax\s) plotted against Pacific hake CPUE
in year i (z-axis). Regression expression is y = 1029 - 23.23x (r2 = 0.418). Numbers
on the plot represent the years of the CPUE data.
953
FISHERY BULLETIN: VOL. 84, NO. 4
hake undergo as they increase in size. Thysanoessa
spinifera appears to be more important to larger
hake whereas Euphausia pacifica is more important
to smaller individuals. Pink shrimp and glass shrimp,
Pasiphaea pacifica, were consumed almost exclu-
sively by fish >55 cm. Eulachon and pleuronectids
were also predominantly consumed by larger hake.
Cannibalism was also observed among larger
individuals.
Diel Feeding Pattern
A number of previous researchers have postulated
that species in the genus Merluccius exhibit a diel
feeding pattern (Outram and Haegele 1972; Bow-
man and Bowman 1980). Alton and Nelson (1970)
as well as Livingston (1983) described Pacific hake
as nocturnal predators that migrate vertically to
feed near the surface during hours of darkness and
dive to deeper water during daylight hours. Brin-
ton (1967) and Alton and Blackburn (1972) showed
that this same vertical migration pattern exists for
the two species of euphausiids found in this study.
If the Pacific hake follow the euphausiids on their
vertical diel migration, the expectation is that the
relative proportion of both species of euphausiids
in the diet should not vary significantly by time of
day. As reported above, our findings conflict with
this expectation.
To further examine this apparent deviation, we
considered potentially confounding factors; such as
differences in the distributions of the euphausiid
species and various size classes of Pacific hake. Brin-
ton (1962) reported that T. spinifera is a neritic
species and E. pacifica is a more oceanic species.
Analysis of length-frequency data from the cruise
during which this study was conducted shows that
Pacific hake of different size classes segregate by
depth. Pacific hake <40 cm in length made up 37%
of the catch in <100 m of water, but these same size
classes comprised 62% of the catch taken in MOO
m of water. Hence, the smaller individuals were
found in greater abundance in the habitat associated
with E. pacifica.
This phenomenon of smaller fish occurring in
deeper water and consequently consuming greater
quantities of E. pacifica explains the apparent dif-
ference in importance of the two species of euphau-
siids by time of day (Fig. 2a). Only 7% of the non-
empty stomachs taken before 1200 h were from fish
<40 cm in length whereas of the fish sampled after
1600 h, 34% were <40 cm in length. Thus, we regard
the observed differences in consumption of T. spini-
fera and increasing importance of E. pacifica by
time of day as spurious, confounded by the differ-
ences in the diets and distributions of various size
classes of Pacific hake.
This study coincided with the strong presence of
El Nino in 1983 which may have altered the nor-
mal migration pattern of Pacific hake and conse-
quently the residence time estimates, and may also
have affected the abundance of the prey base.
Hence, there may be some error in the consump-
tion estimates presented herein. Miller et al. (1984)
noted a decline in the relative abundance of T.
spinifera off the Oregon coast during 1983 in com-
parison with other years. Thus, feeding to satiation
during evening hours may have been impossible;
consequently, feeding occurred whenever euphau-
siids were encountered. Additional circumstantial
evidence of aberrant feeding behavior of Pacific
hake in 1983 is their severely depressed growth
(Francis and Hollowed 1985). Food resources may
only have been sufficient for maintenance metabo-
lism with little energy remaining for growth. These
observations may explain why the diel feeding pat-
tern observed was weak.
Trophic Interaction
The seasonal migration pattern and consequent
latitudinal stratification of Pacific hake stocks by
size class makes it difficult to compare food habit
studies conducted at different times of the year and
at different locations on the Pacific coast. Nonethe-
less, examining only the role of pink shrimp in the
diet, we find first mention of Pacific hake preying
on this species by Gotshall (1969a, b). Analyzing
Pacific hake stomachs collected off California be-
tween 1966 and 1969, Gotshall found high incidences
(54% frequency of occurrence) of pink shrimp dur-
ing late summer and early fall, particularly in Pacific
hake collected over shrimp beds. The study was an
attempt to use Pacific hake as biological samplers
to estimate pink shrimp abundance, focusing sam-
pling effort on known pink shrimp beds, and, as
such, the sampling design was quite different from
other studies.
Outram and Haegele (1972) reported that 3% of
the Pacific hake stomachs collected off the coast of
British Columbia contained pink shrimp. Pink
shrimp were found in 5.7% of the Pacific hake
stomachs collected during the summers of 1965 and
1966 of f Washington and Oregon (Alton and Nelson
1970). Livingston and Alton (1982) found that pan-
dalid shrimp constituted 0.3% by weight of the con-
tents of the 1,430 stomachs of Pacific hake taken
off the coasts of Washington and Oregon during the
954
REXSTAD and PIKITCH: FOOD CONSUMPTION OF PACIFIC HAKE
summer of 1967. From 204 stomachs collected dur-
ing the 1980 NMFS West Coast Groundfish Survey
off the coasts from Oregon to Vancouver Island,
Livingston (1983) found pink shrimp constituted
0.7% by weight of the Pacific hake diet. Pink shrimp
occurred in 1.7% of the Pacific hake stomachs col-
lected in the study described in this paper. Thus,
with the exception of Gotshall's work, studies of the
food habits of Pacific hake have shown pink shrimp
generally comprise well under 10% of the Pacific
hake diet, and thus do not appear to be an impor-
tant food source for hake. However, due to the large
biomass of Pacific hake in the North Pacific, it is
possible that Pacific hake may represent a signifi-
cant source of mortality even for those species, in-
cluding pink shrimp, that are not significant com-
ponents of the Pacific hake diet (Francis 1983).
The estimated consumption of 659.3 t/season of
pink shrimp compares with a commercial catch of
2,197 1 of pink shrimp landed in Oregon during 1984
by 59 vessels (Saelens and Zirges 1985). It is con-
ceivable that the magnitude of Pacific hake preda-
tion on pink shrimp may increase in the near future.
Small Pacific hake, preying mainly on euphausiids,
constituted the bulk of the consumers in this study.
The strong 1980 year class of Pacific hake, seen as
the 35-39 cm size class in these 1983 data, will have
substantially greater impact on commercially valu-
able species upon reaching larger sizes when these
valuable species comprise a larger fraction of the
diet.
Francis (1983) inferred, from catch statistics of
Pacific hake and pink shrimp, that increased catches
of Pacific hake since the inception of the foreign and
subsequent joint- venture fisheries may have con-
tributed to the dramatic increase in the landings of
pink shrimp during the late 1970s. The causal
mechanism inferred is the release of predation
pressure on the pink shrimp population as a result
of decreased Pacific hake abundance due to fishing.
This "surplus" in the pink shrimp population was
harvested by the increasingly vigorous shrimp
fishery.
This contention is disputed by Livingston and
Bailey (1985). Their analysis focuses on pink shrimp
CPUE during two time periods: 1952-65 during
which Pacific hake were unexploited and 1966-77
during which a substantial joint-venture fishery
occurred. They found no appreciable change in aver-
age pink shrimp CPUE between the two periods.
Extending their analysis to include the most recent
catch statistics, we also fail to find the existence of
a significant difference between the periods 1957-65
and 1966-84 (t = 1.05, 26 df, P = 0.303).
However, if pink shrimp have constituted a fair-
ly constant proportion of the Pacific hake diet over
time, as suggested by this and previous Pacific hake
food habit studies, then there may indeed be a rela-
tionship between the release of predator pressure
by the Pacific hake and increased catches of pink
shrimp. The regression-correlation analysis pre-
sented above has an advantage over the average
pink shrimp CPUE analysis because it incorporates
information about both hake and shrimp abun-
dances. The regression-correlation results provide
weak statistical support to Francis' contention that
there is a relationship between Pacific hake and pink
shrimp population dynamics. However, further ob-
servations are needed to obtain greater confidence
in this relationship. In particular, it will be interest-
ing to note that the impact of the strong 1980 year
class Pacific hake on pink shrimp catches in the near
future.
CONCLUSION
Pacific hake occupy a unique trophic position,
serving not only as predators but also as prey for
a variety of species carrying valuations other than
those of an economic nature (endangered species
and species managed under the Marine Mammal
Protection Act). Euphausiids constitute the primary
source of food for Pacific hake in the North Pacific.
However, as Pacific hake mature, euphausiids
decrease in importance and fish take on greater im-
portance. Owing to the vast quantity of hake bio-
mass living in the North Pacific, it has been shown
that Pacific hake may consume large quantities of
several commercially valuable species, even though
these species comprise a fairly small percentage of
the diet. It has also been demonstrated that a
statistically significant relationship exists between
CPUE of Pacific hake and pink shrimp. Additional
years of data are required to have a clearer under-
standing of this relationship.
ACKNOWLEDGMENTS
Bill Barss and Mark Saelens of the Oregon
Department of Fish and Wildlife (ODFW) assisted
in the collection of the Pacific hake stomachs at sea
and with the identification of decapods. Leslie Lutz
of ODFW helped with the laboratory analysis and
Rick Brodeur, Chris Wilson, and Bruce Mundy of
Oregon State University aided in the identification
of fish remains. Rick Brodeur also gave suggestions
on statistical analysis. Helpful comments were pro-
vided by Mac Zirges, Mark Saelens, Robert Fran-
955
FISHERY BULLETIN: VOL. 84, NO. 4
cis, Rick Brodeur, Chuck Harding, Barb Knopf,
Chris Wilson, David Erickson, and two anonymous
reviewers. Robert Francis, Northwest and Alaska
Fisheries Center, NMFS, provided data on histori-
cal Pacific hake catch data and hydroacoustic survey
estimates. This publication is the result, in part, of
research sponsored by NOAA, Office of Sea Grant,
Department of Commerce, under contract No.
NA81AA-D-00086 (Project No. R/OFP-20), and by
the Oregon Department of Fish and Wildlife.
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siids, Thysanoessa spinifera Holmes and Euphausia pacifica
Hansen in coastal waters of Washington. Calif. Fish Game
58:179-190.
Alton, M. S., and M. 0. Nelson.
1970. Food of Pacific hake, Merluccius productus, in Wash-
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Bailey, K. M., R. C. Francis, and P. R. Stevens.
1982. The life history and fishery of Pacific whiting, Merluc-
cius productus. Calif. Coop. Oceanic Fish. Invest. Rep. 23:
81-98.
Best, E. A.
1963. Contribution to the biology of the Pacific hake, Merluc-
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Bowman, R. E., and E. W. Bowman.
1980. Diurnal variation in the feeding intensity and catch-
ability of silver hake {Merluccius bilinearis). Can. J. Fish.
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Brinton, E.
1962. The distribution of Pacific euphausiids. Bull. Scripps
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1967. Vertical migration and avoidance capability of euphau-
siids in the California Current. Limnol. Oceanogr. 12:
451-483.
Brodeur, R. D., and W. G. Pearcy.
1984. Food habits and dietary overlap of some shelf rock-
fishes (genus Sebastes) from the northeastern Pacific Ocean.
Fish. Bull., U.S. 82:269-293.
Fiscus, C. H.
1979. Interactions of marine mammals and Pacific hake.
Mar. Fish. Rev. 41(10):l-9.
Francis, R. C.
1983. Population and trophic dynamics of Pacific hake
(Merluccius productus). Can. J. Fish. Aquat. Sci. 40:1925-
1943.
Francis, R. C, and A. Hollowed.
1985. Status of the Pacific hake resource and recommenda-
tions for management in 1985. Status of stocks document
to Pacific Fisheries Management Council, Portland, OR.
Gotshall, D. W.
1969a. Stomach contents of Pacific hake and arrowtooth
flounder from northern California. Calif. Fish Game 55:
75-82.
1969b. The use of predator food habits in estimating relative
abundance of the ocean shrimp, Pandalus jordani Rathbun.
FAO Fish. Rep. 57, p. 667-685.
GUNDERSON, D. R., AND T. M. SAMPLE.
1980. Distribution and abundance of rockfish off Washington,
Oregon, and California during 1977. Mar. Fish. Rev. 42
(3-4):2-16.
Karpov, K. A., and G. M. Cailliet.
1978. Feeding dynamics of Loligo opalescens. In C. W.
Recksiek and H. W. Frey (editors), Biological, oceanograph-
ic, and acoustic aspects of the market squid, Loligo opales-
cens Berry, p. 45-65. Calif. Dep. Fish Game, Fish Bull.
169.
Livingston, P. A.
1983. Food habits of Pacific whiting, Merluccius productus,
off the west coast of North America, 1967 and 1980. Fish.
Bull. U.S. 81:629-636.
Livingston, P. A., and M. S. Alton.
1982. Stomach contents of Pacific whiting off Washington
and Oregon, April-July 1967. U.S. Dep. Commer., NOAA
Tech. Memo, NMFS F/NWC-32.
Livingston, P. A., and K. M. Bailey.
1985. Trophic role of the pacific Whiting, Merluccius pro-
ductus. Mar. Fish. Rev. 47(2):16-22.
Miller, C. B., H. P. Batchelder, R. D. Brodeur, and W. G.
Pearcy.
1984. Response to the zooplankton and ichthyoplankton off
Oregon to the El Nino event of 1983. In W. S. Wooster and
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eastern subarctic Pacific Ocean, p. 185-187. Wash. Sea
Grant Prog., Univ. Wash., Seattle.
Ostle, B., and R. W. Mensing.
1975. Statistics in research. 3d ed. Iowa State Univ. Press,
Ames, 596 p.
OUTRAM, D. N., AND C. HAEGELE.
1972. Food of Pacific hake (Merluccius productus) on an off-
shore bank southwest of Vancouver Island, British Colum-
bia. J. Fish. Res. Board Can. 29:1792-1795.
Peterson, W. T., R. D. Brodeur, and W. G. Pearcy.
1982. Food habits of juvenile salmon in the Oregon coastal
zone, June 1979. Fish. Bull., U.S. 80:841-851.
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.
Saelens, M. R., and M. H. Zirges.
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Wildl. Inf. Rep. 85-6.
Swartzman, G. L., W. M. Getz, R. C. Francis, R. T. Haar, and
K. Rose.
1983. A management analysis of Pacific whiting (Merluccius
productus) fishery using an age-structured stochastic recruit-
ment model. Can. J. Fish. Aquat. Sci. 40(4):524-539.
Tyler, H. R., Jr., and W. G. Pearcy.
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Weinberg, K. L., M. E. Wilkins, and T. A. Dark.
1984. The 1983 Pacific west coast bottom trawl survey of
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956
DIET OF NORTHERN FUR SEALS, CALLORHINUS URSINUS,
OFF WESTERN NORTH AMERICA
Michael A. Perez1 and Michael A. Bigg2
ABSTRACT
Data recorded from the stomach contents of 18,404 northern fur seals, Callorhinus ursinus, mostly
females aged >3 years collected off western North America during 1958-74, were analyzed to determine
the relative importance of each prey species by region, subregion, and month. When weighted for energy
content, the primary food species were small schooling fishes. Between western Alaska and California
from December to August the most significant prey species were northern anchovy, Engraulis mordax
(20%); Pacific herring, Clupea harengus pallasi (19%); capelin, Mallotus villosus (8%); Pacific sand lance,
Ammodytes hexapterus (8%); Pacific whiting, Merluccius productus (7%); salmon, Oncorhynchus spp.
(6%); Pacific saury, Cololabis saira (4%); and rockfishes, Sebastes spp. (4%). Other food species eaten
in this area consisted of a wide variety of squids (17%) and other fishes (7%). In the eastern Bering Sea
the main prey species from June to October were juvenile walleye pollock, Theragra chalcogramma (35%);
capelin (16%); Pacific herring (11%); and squids, Berryteuthis magister and Gonatopsis borealis, which
comprise most (30%) of the remaining diet of northern fur seals in this region. In all areas off western
North America, fishes were the main food species of these pinnipeds in neritic waters, while squids were
the most important prey in oceanic waters. Typically three prey species comprised 80% of their diet
in any one area, although the composition of the diet varied in type and importance by region and month.
The northern fur seal, Callorhinus ursinus, is found
in the Bering Sea, Sea of Okhotsk, and throughout
the North Pacific Ocean, north of approximately lat.
32 °N off western North America and lat. 36 °N off
Asia (Baker et al. 1970; Fiscus 1978). Although its
pelagic distribution is extensive, the main concen-
trations lie over the continental shelf. There are
three main stocks of this species. The largest stock
breeds on the Pribilof Islands in the eastern Bering
Sea and migrates primarily to coastal waters be-
tween the Gulf of Alaska and California. The other
two stocks breed on the Commander Islands in the
western Bering Sea and on Robben Island off north-
ern Japan. Both stocks migrate primarily along the
Asian coast. To determine the diet of the Pribilof
Islands population, the United States and Canada,
under the auspices of the North Pacific Fur Seal
Commission, conducted annual pelagic studies dur-
ing 1958-74 to collect stomach contents and other
biological information.
The results of research on the diet of northern fur
seals by the United States and Canada during
1958-74 have been presented in many annual and
2-6 yr summaries submitted by each country to the
North Pacific Fur Seal Commission. Kajimura (1984)
cited most of these reports. Spalding (1964), Stroud
et al. (1981), and Kajimura (1985) also published
reports on diet collected since 1958. Studies on the
food habits of the northern fur seal prior to 1958
include Lucas (1899), Clemens and Wilby (1933),
Clemens et al. (1936), Schultz and Rafn (1936), May
(1937), Wilke and Kenyon (1952, 1954, 1957), Taylor
et al. (1955), and Kenyon (1956).
Investigations to date have reported that north-
ern fur seals eat a wide variety of fishes and squids.
However, the relative importance of each prey
species has remained uncertain because substantial
differences often existed between values of relative
importance derived by volumetric measure and
those derived by frequency of occurrence. For ex-
ample, squids were important (averaging 39%) in
the diet using frequency of occurrence but not
significant (15%) using volume (Bigg and Fawcett
1985; Perez and Bigg3). The long-suspected reason
for this difference was that squid beaks accumulated
Northwest and Alaska Fisheries Center, National Marine Mam-
mal Laboratory, National Marine Fisheries Service, NOAA, 7600
Sand Point Way N.E., Seattle, WA 98115.
department of Fisheries and Oceans, Pacific Biological Station,
Nanaimo, British Columbia V9R 5K6, Canada.
3Perez, M. A., and M. A. Bigg. 1980. Interim report on the
feeding habits of the northern fur seal in the eastern North Pacific
Ocean and eastern Bering Sea. In H. Kajimura, R. H. Lander,
M. A. Perez, A. E. York, and M. A. Bigg, Further analysis of
pelagic fur seal data collected by the United States and Canada
during 1958-74, Part 2, p. 4-172. Unpubl. rep. Northwest and
Alaska Fisheries Center, National Marine Mammal Laboratory,
National Marine Fisheries Service, NOAA, 7600 Sand Point Way
N.E., Seattle, WA 98115.
Manuscript accepted July 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
957
FISHERY BULLETIN: VOL. 84, NO. 4
in stomachs of seals thereby inflating the importance
of squid (Scheffer 1950; Spalding 1964; Bigg and
Fawcett 1985). Recent experimental studies con-
firmed that squid beaks accumulate in fur seal
stomachs (Bigg and Fawcett 1985).
To date, no reports have been published on the
diet of northern fur seals that take this bias into ac-
count. However, Bigg and Perez (1985) suggested
a method, called modified volume, which reduces the
bias and also accounts for differences in digestion
rates between fish and squid. In this method,
evidence of diet based on trace remains, such as
squid beaks and fish bones, is omitted in the
analyses, and a combination of the frequency of oc-
currence and volumetric methods is used to estab-
lish the relative importance of individual prey
species.
We use the modified volume method in this report
to analyze data from the stomach contents collected
by the United States and Canada during 1958-74.
We will describe the annual diet of northern fur seals
in the eastern North Pacific and eastern Bering Sea
by region and subregion. We also incorporate the
energy content of important prey species to deter-
mine whether this might affect relative importance,
a procedure not tried previously with this seal.
METHODS
Lander (1980) and Kajimura (1984, 1985) de-
scribed the methods used to take northern fur seals
at sea during 1958-74 and to identify- and measure
the prey items found in their stomachs by volume
and frequency of occurrence. A total of 18,404
stomachs were collected of which 7,373 contained
food and an additional 3,326 had only trace remains.
Perez and Bigg (fn. 3) summarized the data on
volume and frequency of occurrence for all species
of northern fur seal prey by month and region.
Perez and Bigg4 and Bigg and Perez (1985) gave
a detailed discussion of the procedure used to cal-
culate modified volume values. First, prey species
represented in any stomach only by trace amounts
(<10 cc) were omitted. Second, the proportions of
total fish and total squid in the diet by subregion,
region, and month were then determined by non-
trace frequency of occurrence. Third, the ratio of
each species within only the fish category and within
only the squid category was determined by volume.
The taxonomic groupings recorded in the original
data which overlapped each other were either pooled
with higher taxa or were proportionally divided
among component species depending upon which
level of taxa had the most data. This prevented food
groupings from being partially compared against
themselves. Next, the volumetric ratios for in-
dividual fish and squid species were adjusted to sum,
respectively, to the total proportion of fish and squid
in the diet. Finally, all values were readjusted to
total 100%.
The relative importance of prey species has been
presented in this report in two ways: 1) modified
volume values for each region by month, and for
each subregion with data from all months pooled;
and 2) modified volume values for each region based
on combined months data which were weighted for
Table 1 .—Estimated energy values (wet mass) for important north-
ern fur seal prey. C = bomb calorimetry combustion value; P =
proximate analysis value1; muscle = edible portion only of raw
material; whole = raw material from entire specimen.
Energy
Analysis
value
and
Prey
(kcal/g)
tissue
Reference
American shad
2.08
P, muscle
Sidwell (1981)
Pacific herring
2.17
P, whole
Sidwell (1981);
Bigg et al. (1978)
Northern anchovy
1.79
P, whole
Sidwell (1981)
Salmonids
2.01
P, muscle
Sidwell (1981)
Capelin
1.31
C, whole
Miller2
Eulachon
1.41
P, muscle
Stansby (1976)
Deep-sea smelts
0.76
P, whole
Childress and Nygaard
(1973)
Myctophiform
1.58
P, whole
Childress and Nygaard
fishes
(1973)3
Pacific saury
2.20
P, muscle
Sidwell (1981)
Jacksmelt
1.24
P, muscle
Watt and Merrill (1963)
Pacific cod
1.00
P, muscle
Sidwell (1981)
Pacific whiting
1.17
P, whole
Sidwell (1981)
Walleye pollock
1.41
C, whole
Miller2
Threespine
stickleback
1.15
C, whole
Wootton (1976)
Jack mackerel
1.24
P, whole
Sidwell (1981)
Rockfishes
1.17
P, muscle
Sidwell et al. (1974)
Sablefish
2.17
P, muscle
Sidwell (1981)
Atka mackerel
1.58
P, muscle
Kizevetter (1971)
Pacific sand lance
1.22
P, muscle
Sidwell (1981)
Flounders
1.20
P, muscle
Sidwell (1981)4
Market squid
1.15
P, muscle
Sidwell (1981)
Onychoteuthid
squids
1.29
Perez5
Gonatid squids
1.27
Perez5
4Perez, M. A., and M. A. Bigg. 1981. Modified volume: a two-
step frequency-volume method for ranking food types found in
stomachs of northern fur seals. Unpubl. rep., 25 p. Northwest
and Alaska Fisheries Center, National Marine Mammal Labora-
tory, National Marine Fisheries Service, NOAA, 7600 Sand Point
Way N.E., Seattle, WA 98115.
'Values were calculated with the following energy factors derived from Watt
and Merrill (1963): 9.50, 5.65 and 4.00 kcal/g respectively for fat, protein and
carbohydrate.
2Miller, L. K. 1978. Energetics of the northern fur seal in relation to
climate and food resources of the Bering Sea. U.S. Mar. Mammal Comm.
Rep. MMC-75/08, 27 p.
3Myctophidae and Paralepididae.
4Pleuronectidae.
5Perez, M. A., Natl. Mar. Mammal Lab., Northwest and Alaska Fish. Cent.,
Natl. Mar. Fish. Serv., NOAA, 7600 Sand Point Way N.E., Seattle, WA 981 15,
unpubl. data, 1984.
958
PEREZ and BIGG: DIET OF NORTHERN FUR SEALS
the energy value of prey. Data from all years of
collection were pooled. We assumed that the impor-
tance of a prey species to northern fur seals de-
pended, at least in part, on its energy content. Table
1 lists the estimated caloric values for prey species
consumed most often. These estimates are provi-
sional because little is known about changes in
energy content within each species by season.
Energy values for squids tend to be lower than those
for fishes, although large variability exists among
fish species.
No attempt was made to describe diet by age, sex,
and reproductive condition. In our sample, 88% of
the northern fur seals were females aged >3 yr, of
which 53% were pregnant and 29% were nonpreg-
nant. Thus, the diet described is primarily that
for pregnant and nonpregnant females aged >3
yr.
The eastern North Pacific Ocean and eastern Ber-
ing Sea were divided into 7 regions and 21 sub-
regions (Fig. 1). The boundaries for the seven
regions were those which have been traditionally
EASTERN BERING SEA
SEALASKA
BEROFF
^V^
62° N
.- y (
UNIMAK
WESTERN ALASKA
GULF OF ALASKA
HECATE
WASHOFF
WASHINGTON
•BCIMLETS
WESTVAN .
PEROUSE
OREGON
WASHNO
CALIFORNIA
NORTH PACIFIC OCEAN
NCALOFF
CCALOFF
SCALOFF
CCALIN
SCALIN
\
52°
42°
32°
175° W
155°
135°
115°
Figure 1.— Seven regions (denoted by darker lines) and 21 subregions used in the northern fur seal analyses: 1) California comprised
of subregions SCALIN (southern California, inshore), SCALOFF (southern California, offshore), CCALIN (central California, inshore),
CCALOFF (central California, offshore), NCALIN (northern California, inshore), and NCALOFF (northern California, offshore); 2)
Oregon which includes half of subregion WASHNO (southern Washington and northern Oregon, inshore); 3) Washington which includes
subregions PEROUSE (area west of Juan de Fuca Strait from Barkley Sound to Cape Flattery, including La Perouse Bank and Swift-
sure Bank; inshore), WASHOFF (Washington, offshore), and half of WASHNO; 4) British Columbia which includes subregions BCINLETS
(inside passages and inlets of B.C., inshore), WESTVAN (area west of Vancouver Island and Queen Charlotte Strait, inshore), HECATE
(Hecate Strait area, inshore), and BCOFF (British Columbia, offshore); 5) the Gulf of Alaska which includes subregions SEALASKA
(southeast Alaska, inshore), NOGULF (northern Gulf of Alaska, including Fairweather Bank; inshore), KODIAK (area around Kodiak
Island, including Portlock Bank and Albatross Bank; inshore), and CENGULF (oceanic region of the Gulf of Alaska, offshore); 6) western
Alaska which includes part of subregion UNIMAK (Unimak Pass area); and 7) the eastern Bering Sea comprised of subregions BERIN
(Bering Sea shelf, inshore) and BEROFF (Bering Sea basin, offshore), and also includes subregions PRIBILOF (area around the Pribilof
Islands) and most of UNIMAK. Subregions in which >50% of the area is <100 fathoms are noted as inshore; the remainder are noted
as offshore.
959
FISHERY BULLETIN: VOL. 84, NO. 4
used in analyses of pelagic data for northern fur
seals. The subregions were selected to compare diet
between inshore (neritic) and offshore (oceanic)
areas and to indicate diet in certain localities where
collection effort was relatively high. Inshore areas
were defined as those generally occurring on the
continental shelf (depths up to 100 fathoms) and off-
shore areas as those beyond the continental shelf.
RESULTS
The cruise tracks (Fig. 2) taken by research
vessels of the United States and Canada for the col-
lection of northern fur seals during 1958-74 indicate
the relative distribution of research effort. Most col-
lections were made in the coastal areas between
California and British Columbia, off Kodiak Island,
and in the eastern Bering Sea between Unimak Pass
and the Pribilof Islands. Few specimens were taken
more than 160 km from shore.
Diet by Region and Month
An examination of the number of prey species that
made up the diet indicates that at least nine species
may be consumed within any one subregion. How-
ever, typically only three prey species made up about
80% of the diet (Fig. 3). Thus, relatively few species
of food are of primary importance in any one local-
ity. As will be made clear in the following regional
and subregional accounts, the primary food species
can change among localities.
Our interpretation of Figures 4-11 which follow
requires clarification. These figures show modified
volume values only for those individual species that
we felt were important and that had sufficient
sample sizes to be reliable. Thus, we arbitrarily pre-
sented only those species that were of >5% in im-
portance for samples with at least 20 stomachs con-
taining food. Species of less importance were pooled
either as miscellaneous fishes or squids. Also, be-
62° N
175° W 155° 135° 115°
Figure 2.— Cruise tracks of northern fur seal research vessels from the United States and Canada during 1958-74.
960
PEREZ and BIGG: DIET OF NORTHERN FUR SEALS
4 6
Number of prey species
10
Figure 3.^The cumulative percentage distribution of the number
of prey species eaten in the total diet of northern fur seals taken
during 1958-74. Data for each of the 21 subregions are plotted,
although only the average relationship is graphed.
cause the prey consumed by month within sub-
regions were not presented here, we take these data
from Perez and Bigg5 in our interpretation of sub-
regional data.
California
Northern anchovy, Engraulis mordax, was the
most important food eaten by the northern fur seals
off California (Fig. 4A) whether its energy content
was considered or not. However, it was more im-
portant when its caloric value was taken into ac-
count. Northern anchovy was eaten mainly during
January to March in inshore and offshore waters of
central and southern California (Fig. 4B, C). Pacific
whiting, Merluccius productus, was second in im-
portance (Fig. 4A) and was preyed upon in all areas
of California, although primarily during April and
May (Fig. 4B, C). Market squid, Loligo opalescens,
was eaten from January to June, but only in neritic
locations (Fig. 4B, C). Onychoteuthid squids (Ony-
choteuthidae) were eaten offshore and were the
more important squid species consumed in the south-
ern areas off California (Fig. 4C). Other prey types
were of relatively minor importance, although some
were locally significant, such as Pacific saury, Colo-
labis saira, mainly in oceanic areas off northern and
central California (Fig. 4 A, B, C).
6Perez, M. A., and M. A. Bigg. 1981. An assessment of the
feeding habits of the northern fur seal in the eastern North Pacific
Ocean and eastern Bering Sea. Unpubl. draft rep., 146 p. North-
west and Alaska Fisheries Center, National Marine Mammal
Laboratory, National Marine Fisheries Service, NOAA, 7600 Sand
Point Way N.E., Seattle, WA 98115.
100
NCALIN
NCAL0FF
CCALIN
CCAL0FF
SCALIN
SCAL0FF
116
53
1105
353
78
106
Figure 4.— Composition (percent) of diet of northern fur seals by
prey species off California during 1958-74 (A) for pooled January-
June samples (N = 1,811), using modified volume (dark bars) and
energy-adjusted modified volume; (B) by month using modified
volume; and (C) by subregion with pooled January-June samples
using modified volume. A dark line separates squid and fish
categories in the latter two figures. Key: ANC = northern an-
chovy; GON = gonatid squids; JAC = jack mackerel; JCK =
jacksmelt; MAR = market squid; MF = miscellaneous fish species;
MS = miscellaneous squid species; MYC = myctophiform fishes;
ONY = onychoteuthid squids; OP = other prey; SBL = sablefish;
SRY = Pacific saury; WHI = Pacific whiting.
961
FISHERY BULLETIN: VOL. 84, NO. 4
Oregon
Only 69 northern fur seals with food in their
stomachs were collected in Oregon between Janu-
ary and May during 1958-74, with 58 of these taken
during April. Thus, diet could not be determined by
month or by inshore and offshore areas. As in
California, the main food was northern anchovy
(Fig. 5). Other important prey were market squid,
onychoteuthid squids, Pacific whiting, and rock-
fishes (Sebastes spp.).
Washington
Pacific herring, Clupea harengus pallasi, was the
most important food for northern fur seals off
Washington, particularly when energy content was
considered (Fig. 6A). It was only slightly more sig-
nificant than rockfishes, salmonids (Salmonidae,
primarily Oncorhynchus spp.), and northern anchovy
when caloric values were not incorporated. Pacific
herring was eaten from December to June but only
SRY WHI
Prey species
Figure 5.— Composition (percent) of diet of northern fur seals by
prey species off Oregon during 1958-74 for pooled January- June
samples (N = 69), using modified volume (dark bars) and energy-
adjusted modified volume. Key: ANC = northern anchovy; MAR
= market squid; ONY = onychoteuthid squids; OP = other prey;
ROC = rockfishes; SRY = Pacific saury; WHI = Pacific whiting.
MAR ONY GON SHA HER ANC SAL CAP EUL ROC SBL OP
Prey species
B
100
8 50
D
J
F
M
A
M
J
42
179
152
343
757
425
20
N
WASHNO PEROUSE WASHOFF
746 961 234
Figure 6.— Composition (percent) of diet of north-
ern fur seals by prey species off Washington dur-
ing 1958-74 (A) for pooled December-June samples
(N = 1,918), using modified volume (dark bars) and
energy-adjusted modified volume; (B) by month
using modified volume; and (C) by subregion with
pooled December-June samples using modified
volume. A dark line separates squid and fish
categories in the latter two figures. Key: ANC =
northern anchovy; CAP = capelin; EUL = eula-
chon; GON = gonatid squids; HER = Pacific her-
ring; MAR = market squid; MF = miscellaneous
fish species; MS = miscellaneous squid species;
ONY = onychoteuthid squids; OP = other prey;
ROC = rockfishes; SAL = salmonids; SBL =
sablefish; SHA = American shad; WHI = Pacific
whiting.
962
PEREZ and BIGG: DIET OF NORTHERN FUR SEALS
in neritic areas (Fig. 6B, C). Rockfishes, salmonids,
and northern anchovy were also consumed by seals
during this time, both inshore and offshore. North-
ern anchovy was primarily important in the south-
ern area of the region (Fig. 6C). The main food in
oceanic waters consisted of two families of squids,
Onychoteuthidae and Gonatidae (Fig. 6C). Market
squid was the primary squid species preyed upon in
neritic areas.
British Columbia
As in Washington, Pacific herring was the prim-
ary food of the northern fur seals from February
to June in most inshore areas, particularly when
energy content was taken into account (Fig. 7 A, B,
C). It was mainly consumed by northern fur seals
off the west coast of Vancouver Island and in Hecate
Strait. In coastal inlets, market squid was impor-
tant, but not significantly for the region as a whole.
The diet of northern fur seals in oceanic waters dur-
ing May and June was almost exclusively onycho-
teuthid squids and salmonids (Fig. 7B, C). Other
prey species were relatively insignificant (Fig. 7A).
However, because the coastline of British Colum-
bia is complex, and sample sizes were small, addi-
tional local differences in diet may exist in inshore
areas (Fig. 7C).
MAR
HER SAL
Prey species
B
100
£ 50 -
N
WESTVAN BCINLETS HECATE BCOFF
140 41 79 78
Figure 7.— Composition (percent) of diet of northern fur seals by prey species off British Columbia during 1958-74 (A) for pooled January-
June samples (N = 354), using modified volume (dark bars) and energy-adjusted modified volume; (B) by month using modified volume;
and (C) by subregion with pooled January-June samples using modified volume. A dark line separates squid and fish categories in the
latter two figures. Key: COD = Pacific cod; EUL = eulachon; GAD = gadid fishes; GON = gonatid squids; HER = Pacific herring;
MAR = market squid; MF = miscellaneous fish species; ONY = onychoteuthid squids; OP = other prey; POL = walleye pollock; ROC
= rockfishes; SAL = salmonids; SBL = sablefish; US = unidentified squid; WHI = Pacific whiting.
963
FISHERY BULLETIN: VOL. 84, NO. 4
Gulf of Alaska
Based on all samples collected in the Gulf of
Alaska, the main diet of northern fur seals was
Pacific herring when energy content was con-
sidered, but Pacific sand lance, Ammodytes hexap-
terus, was most important when caloric values were
not considered (Fig. 8A). However, there were
subregional differences in diet. Off southeastern
Alaska, collections were made in Sitka Sound dur-
ing February and March where the diet was almost
exclusively Pacific herring (Fig. 8B, C). In the north-
ernmost area of the region the diet consisted chief-
ly of capelin, Mallotus villosus, but also to a lesser
degree of both walleye pollock, Theragra chalco-
gramma, and Pacific sand lance (Fig. 8C). Off
Kodiak Island during April to July, the diet was
mainly Pacific sand lance and capelin (Fig. 8B, C).
Gonatid squids (Gonatidae) were the primary foods
of northern fur seals in oceanic waters of this region
from April to June. Rockfishes and salmonids were
also eaten by northern fur seals in offshore and
northern inshore areas of the region (Fig. 8C).
Western Alaska
Of the 309 stomachs with food collected in this
region from May to October 1958-74, 239 were
taken during June, with most of these collected
south of Unimak Pass. The main foods of the north-
ern fur seals were Pacific sand lance and capelin,
as off Kodiak Island, with the energy content of each
having little effect on their relative importance (Fig.
9). Other important prey were Atka mackerel,
Pleurogrammus monopterygius, salmonids, walleye
pollock, and the squid Berryteuthis magister. Sable-
fish, Anoplopoma fimbria, and Pacific herring were
also eaten by northern fur seals south of Unimak
Pass during summer months.
GON
HER
CAP .POL
Prey species
SND OP
B
100
75 -
S 50
Figure 8.— Composition (percent) of diet of northern
fur seals by prey species in the Gulf of Alaska during
1958-74 (A) for pooled February-July samples (N =
1,163), using modified volume (dark bars) and energy-
adjusted modified volume; (B) by month using modified
volume; and (C) by subregion with pooled February-
July samples using modified volume. Key: CAP =
capelin; GON = gonatid squids; HER = Pacific her-
ring; MF = miscellaneous fish species; MS =
miscellaneous squid species; OP = other prey; POL =
walleye pollock; ROC = rockfishes; SAL = salmonids;
SND = Pacific sand lance; US = unidentified squid.
100'
75-
50
25-
HER
• • • •
'.SND*.
■ ■ ■_■_•_■.
*p6l>:
HER
CAP
Mv/;i*y^
CAP
SND
F
M
A
M
J
J
SEALASKA
NOGULF
KODIAK
CENGULF
N
32
196
203
452
260
20
N
242
115
733
73
964
PEREZ and BIGG: DIET OF NORTHERN FUR SEALS
30,-
BER
SAL
CAP POL ATK
Prey species
SND
OP
Figure 9.— Composition (percent) of diet of northern fur seals by prey
species in western Alaska during 1958-74 for pooled May-October samples
(N = 309), using modified volume (dark bars) and energy-adjusted modified
volume. Key: ATK = Atka mackerel; BER = Berryteuthis magister;
CAP = capelin; OP = other prey; POL = walleye pollock; SAL =
salmonids; SND = Pacific sand lance.
Eastern North Pacific
Northern anchovy (20%) and Pacific herring (19%)
were the main species eaten by the northern fur
seals in the eastern North Pacific when data from
all regions and months were pooled (Fig. 10). These
prey were the most important whether energy con-
tent was considered or not, although importance in-
creased when the caloric values were included.
Salmonids (6%), capelin (8%), Pacific whiting (7%),
walleye pollock (2%), Pacific sand lance (8%), and
rockfishes (4%) were also commonly eaten. The re-
maining diet was made up of a wide variety of squids
(mainly market squid, 6%; onychoteuthid squids,
6%; and gonatid squids, 5%) and other fishes (mainly
Pacific saury, 4%; sablefish, 2%; and Atka mackerel,
2%). Squids were the primary food species in oceanic
waters between California and the Gulf of Alaska,
and fishes were the main prey in the neritic areas.
Although not eaten in large amounts, salmonids and
rockfishes were the main fishes consumed in oceanic
areas between Washington and the Gulf of Alaska
(Figs. 6C, 7C, 8C).
O
■D > n.
£ > °
*o-=
Ox
Z O
uiZ
I cc
o»
<o
c
Q.
u S
V) 0
■o —
z S
u.
S1*
is
CC
UJ
I
5 UJ
-J Q.
f*
O
<3
^O
Sin
— UJ
u. _|
2<
a. S
CC Q.
Figure 10.— Composition (percent) of diet of northern fur seals by prey species in
the eastern North Pacific (excluding the Bering Sea) during 1958-74 using modified
volume (dark bars) and energy-adjusted modified volume. Data from all months and
years were pooled (N = 5,624).
965
FISHERY BULLETIN: VOL. 84, NO. 4
Eastern Bering Sea
Walleye pollock was the most important food for
northern fur seals in the eastern Bering Sea, par-
ticularly around the Pribilof Islands and in other in-
shore waters during July to September (Fig. 11 A,
B, C). Capelin was the main food near Unimak Pass
during June to October. The squids, Berryteuthis
magister and Gonatopsis borealis, were the primary
prey species of fur seals in the oceanic areas (Fig.
11C). Deep-sea smelts (Bathylagidae) were eaten off-
shore, mainly in association with squid. The relative
importance of each prey species was not markedly
affected by the energy content adjustments (Fig.
11A).
Effect of Energy Value of Prey
In general, the ranking of prey species in the diet
of northern fur seals was similar when using either
modified volume or modified volume weighted for
the energy content of prey. However, caloric values
affected relative importance in regions where high
energy foods (e.g., Pacific herring, northern an-
chovy, salmonids), or where low energy foods (e.g.,
market squid, Pacific whiting) were commonly
eaten. In such cases, the adjustment shifted impor-
tance of a prey species in the same direction as the
relative value of their caloric content compared with
other prey in the diet. A species with high energy
content increased in importance, but this caused
others to decrease because the relative values of
prey species in the diet all totaled 100%.
DISCUSSION
The results of earlier investigations on the diet
of northern fur seals indicated that basically the
UNIMAK PRIBILOF BERIN BEROFF
N 543 308 1017 732
Figure 11.— Composition (percent) of diet of northern fur seals
by prey species in the eastern Bering Sea during 1958-74 (A) for
pooled June-October samples (N = 1,749), using modified volume
(dark bars) and energy-adjusted modified volume; (B) by month
using modified volume; and (C) by subregion, with pooled June-
October samples using modified volume. A dark line separates
squid and fish categories in the latter two figures. Key: ATK =
Atka mackerel; BER = Berryteuthis magister; CAP = capelin;
DEE = deep-sea smelts; GTP = Gonatopsis borealis; HER =
Pacific herring; MF = miscellaneous fish species; OP = other prey;
POL = walleye pollock.
966
PEREZ and BIGG: DIET OF NORTHERN FUR SEALS
same species of prey were important by region and
month as reported in the current study. This was
true for the numerous annual and intermittent sum-
mary reports prepared by the United States and
Canada for the North Pacific Fur Seal Commission
during 1958-74. However, they are not reviewed
here because they typically described diet for a par-
ticular year or 2-6 yr period and were based on
subsets of the samples that we used. In other
studies, Stroud et al. (1981) and Kajimura (1984,
1985) mentioned, although did not demonstrate, that
squids were the main food species in offshore areas,
whereas fishes were the most important inshore.
This observation was confirmed in our findings. The
phenomenon appears to exist throughout the feed-
ing range of northern fur seals off western North
America.
Also, as found in our study, Taylor et al. (1955)
and Kajimura (1985) reported that the main food for
the northern fur seal off California was northern an-
chovy. Similarly, Clemens and Wilby (1933),
Clemens et al. (1936), Schultz and Rafn (1936), May
(1937), Wilke and Kenyon (1952), Spalding (1964),
and Kajimura (1985) all indicated that Pacific her-
ring was the primary prey between Washington and
southeastern Alaska. Taylor et al. (1955) and Kaji-
mura (1985) found that capelin was prominent in the
diet off Kodiak Island; and Lucas (1899), Wilke and
Kenyon (1952), and Kajimura (1985) found that
walleye pollock was the most significant species in
the eastern Bering Sea; and Wilke and Kenyon
(1957) reported that capelin was important to north-
ern fur seals near Unimak Pass.
However, there were some differences between
the results of earlier research and the current analy-
sis. Taylor et al. (1955) stated that 1) jacksmelt,
Atherinopsis calif orniensis, was second in impor-
tance for northern fur seals off California rather
than insignificant as we reported; 2) salmon was the
main food off Oregon rather than a minor diet item;
3) walleye pollock was more important than Pacific
herring off Washington; and 4) Pacific sand lance
was rarely foraged off Kodiak Island rather than
eaten almost as frequently as capelin. Kenyon (1956)
found Pacific sandfish, Trichodon trichodon, to be
the most commonly consumed food of seals which
were taken on rookeries of the Pribilof Islands,
whereas the current study found that it was rarely
eaten. Most of these differences probably resulted
from small sample sizes of earlier studies or dis-
similar measures of importance. Also, some differ-
ences in diet will result from interannual variability
in prey abundance and movement patterns owing
to environmental conditions or other factors.
Factors other than just the relative importance
by region and month must be taken into account
when determining the significance of each prey
species to the seal. Robbins (1983) stated that the
nutritional value of food should also be considered.
For example, food species with high caloric values
will be more important than those with low caloric
values because the amount of food required for
metabolic functions depends to some extent upon
the energy content of that food. However, high
energy foods are more valuable only when they are
not more difficult to capture and do not contain
more indigestible or toxic substances than lower
energy content species. These detrimental factors
do not appear to be involved when considering the
most important foods eaten by northern fur seals
in the eastern North Pacific Ocean. Northern an-
chovy and Pacific herring were already the most im-
portant prey species even without accounting for
their energy content. But because they also had rela-
tively high energy values, their importance in-
creased in the seal's diet. Thus, relative importance
with an adjustment for energy content appears to
be a better measure of diet than when energy con-
tent is not incorporated.
Another factor to consider is the proportion of the
year that the northern fur seal population spends
in each locality. Each prey species in the total an-
nual diet should be weighted by the importance of
each subregion and region where the prey is eaten.
This weighting requires understanding the route
and timing of migration, and the changes in local
seasonal abundance of northern fur seals. The
general pattern of migration for the Pribilof Islands
stock is well known (Baker et al. 1970; Fiscus 1978;
Bigg 19826). Essentially all population components,
except most 1-2 yr-olds, are thought to occur in the
eastern Bering Sea during June-July to October
where they pup, mate, nurse, and rest on the Pribilof
Islands. Most 1-2 yr-olds remain in the North Pacific
Ocean during this time. The stock leaves the east-
ern Bering Sea in November-December and travels
mainly to the coastal areas between southeastern
Alaska and California, with the largest number ap-
parently going to California by January. Most males
remain in Alaskan waters, and seals aged 1-2 yr re-
main offshore. The return migration starts in March-
April with most seals arriving in the northern Gulf
of Alaska by May. However, while this general pat-
6Bigg, M. A. 1982. Migration of northern fur seals in the
eastern North Pacific and eastern Bering Sea: an analysis using
effort and population composition data. Unpubl. rep., 77 p. De-
partment of Fisheries and Oceans, Pacific Biological Station,
Nanaimo, British Columbia V9R 5K6, Canada.
967
FISHERY BULLETIN: VOL. 84, NO. 4
tern of migration is known, no estimates have been
made of the seasonal abundance of seals by region,
and thus total diet cannot be weighted by the sig-
nificance of each locality.
Nonetheless, we are of the opinion that the lack
of estimates of local abundance of northern fur seals
may not be a major bias in our descriptions of diet
for the large coastal regions of the eastern North
Pacific (Fig. 10) and the eastern Bering Sea (Fig.
11). We reason that the sampling effort in the east-
ern North Pacific was extensive from December to
June, as indicated by the size of samples collected
by month and region (Figs. 4-9; see also Figure 2),
and may have largely reflected the seasonal changes
in relative abundance of seals during their coastal
migration. For the eastern Bering Sea, essentially
all samples were taken during July-October, which
was the time most seals resided there.
The most general conclusion to be made about the
diet of coastal northern fur seals is that it consists
primarily of small schooling fish. Previous studies
have made the point that the diet consists of small
schooling fish and squid (Spalding 1964; Kajimura
1985; others). However, our findings suggest that
squid are no more important in the overall diet to
the seal than are the larger sized fish. In the coastal
regions of the eastern North Pacific the northern
fur seal's diet consists of 60% small schooling fish,
23% other fish, and 17% squid. When northern fur
seals arrive off the coast of southeastern Alaska to
California during winter, they feed on northern an-
chovy, Pacific herring, capelin, and Pacific saury.
When most northern fur seals arrive along the coast
of the Gulf of Alaska in spring, they eat capelin and
Pacific sand lance. These are fish <30 cm in length
(Table 2). Typically they are eaten whole whereas
larger fish are first broken into small pieces (Spald-
ing 1964). Walleye pollock is the primary food in the
eastern Bering Sea. It is a large fish as an adult
(Smith 1981), and these fish school. However, north-
ern fur seals feed mainly upon the juvenile stages,
i.e., <20 cm (McAlister and Perez7). Thus, the diet
in this region consists up to 64% small schooling fish,
6% other fish, and 30% squid.
On the Asian coast the diet of northern fur seals
also includes small schooling fishes such as mycto-
phiform fishes (lanternfishes), Pacific saury, Pacific
sand lance, and the Japanese anchovy, Engraulis
Table 2. — Summary of the size range and general habitat of north-
ern fur seal prey.1 A = anadromous; BC = British Columbia;
BER = eastern Bering Sea; CAL = California; GULF = Gulf of
Alaska; I = inshore; NS = near surface; O = offshore; ORE =
Oregon; S = schooling fish; WASH = Washington; WEST =
western Alaska.
Size range (cm)
of specimens
Average
in fur seal
adult
stomachs
size
(sample size in
Prey
(cm)
parentheses)2
General habitat
Pacific herring
<20-30
10-25 (11,>27)
Pelagic (l,S)
Northern anchovy
<18
9-18 (7,27)
Pelagic (l-O.S)
Salmonids3
<80
15-41 (22,>26)
Pelagic (l-0,A)
Capelin
22
7-14 (7,64)
Pelagic (l,S)
Eulachon
23-30
12-21 (3,11)
Pelagic (l,S,A)
Deep-sea smelts
2-18
8-12(6,986)
Pelagic (0,S)
Myctophiform
fishes
13-20
—
Pelagic (0,S)
Pacific saury
10-32
25 (1 ,4)
Pelagic (0,S)
Pacific whiting
66-76
15(1,2)
Pelagic and
semidemersal
(l-O.S)
Walleye pollock
<90
4-40 (71,1721)
Pelagic and
semidemersal
(l-O.S)
Rockfishes
30-53
11-31 (6,>19)
Demersal (l-0,S)
Sablefish
57-60
20-31 (3,>3)
Pelagic and
semidemersal
(l-O.S)
Atka mackerel
<120
15-23 (5,>5)
Pelagic and
semidemersal
(l,S)
Pacific
sand lance
20
—
Demersal (l,S)
Market squid
14-17
7-15 (6,43)
Pelagic (I)
Onychoteuthid
squids4
10-37
14-22 (3,>3)
Pelagic (l-O)
Gonatid squid
12-32
5-24 (10,>59)
Pelagic (l-O)
7McAlister, W. B., and M. A. Perez. 1977. Ecosystem
dynamics— birds and marine mammals. Part 1: preliminary esti-
mates of pinniped-finfish relationships in the Bering Sea (final
report). In Environmental assessment of the Alaskan continen-
tal shelf, Annual Report 12, p. 342-371. U.S. Department of Com-
merce, Environmental Research Laboratory, Boulder, CO.
'Data on average lengths of prey and ecology were compiled from Aki-
mushkin (1 963), Bakkala et al. (1 981 ), Baxter (1 967), Baxter and Duffy (1 974),
Carl (1964), Childress and Nygaard (1973), Childress et al. (1980), Fields
(1965), Fitch (1974), Fitch and Lavenberg (1968, 1971, 1975), Hart (1973),
lnada(1981), Miller and Lea (1976), Naitoetal. (1977), Niggol (1982), Pearcy
(1965), Pearcy et al. (1979), Smith (1981), Taka et al. (1980), and Wespestad
and Barton (1981).
2Total length for fish and dorsal mantle length for squid. The first number
in parentheses is the number of fur seal stomachs examined, and the second
number in parentheses is the number of prey specimens measured. These
data were derived from an analysis of the original unpublished 1 958-74 data.
3Maximum size of salmonids found at sea. Adults in freshwater are larger
(to 147 cm) depending upon species.
4Does not include size range of Moroteuthis (<140 cm) which has been taken
by northern fur seals, but rarely off North America.
japonicus, in addition to walleye pollock and squid
(Taylor et al. 1955; Lander and Kajimura 1980). Of
interest is the fact that in recent years the Japanese
sardine, Sardinops melanosticta, has become more
important in the diet of northern fur seals off Asia
(Yoshida et al.89; Yoshida and Baba1011). This sar-
dine was depleted during the 1930's and 1940's and
8Yoshida, K., N. Okumoto, and N. Baba. 1979. Japanese
pelagic investigation on fur seals, 1978. Far Seas Fish. Res. Lab.,
Shimizu, Jpn., Fur Seal Resour. Sect., Contrib. No. 41-9, 66 p.
968
PEREZ and BIGG: DIET OF NORTHERN FUR SEALS
recovered only recently (Kondo 1980). The northern
fur seal appears to have reacted to this recovery by
eating more sardines. A similar change in diet may
have taken place off California during the past 50
years. The Pacific sardine, Sardinops sagax, was
once the most abundant small, schooling fish off
California, whereas now northern anchovy is (Mur-
phy 1966; Smith 1972; Mais 1974). The Pacific sar-
dine population was drastically reduced during the
1940's mainly because of fishing pressure and has
remained at a relatively low level since, while the
northern anchovy increased in abundance during the
1950's and the 1960's (Vrooman and Smith 1971;
Hart 1973; Wolf and Smith 1985). The Pacific sar-
dine may undergo long-term periodic fluctuations
in population size (Thompson 1921), and it may now
once again be increasing in biomass (Wolf and Smith
1985). Northern fur seals have not eaten Pacific sar-
dine in recent years, but perhaps they fed on this
species prior to the 1940's. The seal may have
changed its diet from largely Pacific sardine to
northern anchovy. Unfortunately, the stomach con-
tents of only two northern fur seals were collected
from California prior to the 1950's (Scheffer 1950).
Clemens and Wilby (1933) gave the only evidence
that sardines were once consumed by these seals in
the eastern North Pacific Ocean. They found that
sardines were commonly eaten during 1931 off
southwestern Vancouver Island.
An interesting speculation regarding the signifi-
cance of small schooling fish to northern fur seals
is the relationship between diet and the migration
route of the seal. Small schooling fish could be im-
portant just because they are abundant and lie along
the coastal migration path of northern fur seals. Ka-
jimura (1985) argued for this possibility. He sug-
gested that the migration pattern of northern fur
seals is genetically established and that the seal
feeds opportunistically upon whatever prey species
are most abundant in its path. He believes that,
although food is not a major factor in determing the
migration route of northern fur seals, the move-
ments of prey species can still alter the local distribu-
tion of fur seals. An alternative possibility is that
the seals learn the location of the main foods and
then selects its migration route to include them.
9Yoshida, K., N. Okumoto, and N. Baba. 1981. Japanese
pelagic investigation on fur seals, 1979-1980. Far Seas Fish. Res.
Lab., Shimizu, Jpn., Fur Seal Resour. Sect., Contrib. No. 41-10,
150 p.
10Yoshida, K., and N. Baba. 1983. Japanese pelagic investiga-
tion on fur seals, 1981-1982. Far Seas Fish. Res. Lab., Shimizu,
Jpn., Fur Seal Resour. Sect, Contrib. No. 41-11, 118 p.
"Yoshida, K., and N. Baba. 1984. Japanese pelagic investiga-
tion on fur seals, 1983. Far Seas Fish. Res. Lab., Shimizu, Jpn.,
Fur Seal Resour. Sect., Contrib. No. 41-12, 67 p.
Baker (1978) argued for this alternative. He pro-
posed that, while some inherited factors may be in-
volved in migration, northern fur seals could main-
ly search the North Pacific Ocean for the most
preferred or abundant food, and thereafter estab-
lish the migration route. Such being the case,
perhaps inexperience explains why 1-2 yr-old seals
are rarely seen inshore feeding with older seals.
Also, perhaps squid is not a preferred or sufficiently
available food for northern fur seals offshore,
because most seals older than 1-2 yr feed inshore
on fish. However, at this stage, not enough is known
about the factors that control migration of the north-
ern fur seal to establish which alternative is true.
As Kajimura (1985) has pointed out, factors other
than diet are no doubt involved as indicated by the
fact that males do not migrate as far south as
females.
ACKNOWLEDGMENTS
The following people assisted us with the prepara-
tion of data for analysis, and with the construction
of tables and figures presented in unpublished pre-
liminary reports of this study: Julia Bosma, Patricia
Bouthillette, Laurie Briggs, Carl Brooks, David
Crystal, Ian Fawcett, Gary Fidler, Job Groot, Carol
Hastings, Marta Hladyschevsky, Kerry Hobbs,
Gerald Hornof, Marilyn Marshall, Elizabeth
Mooney, R. Perez, Kenneth Pierce, and Marsha
Schad.
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971
INSTAR IDENTIFICATION AND LIFE HISTORY ASPECTS OF
JUVENILE DEEPWATER SPIDER CRABS,
CHIONOECETES TANNERI RATHBUN
Patricia A. Tester1 and Andrew G. Carey, Jr.2
ABSTRACT
For the deepwater spider crab, Chionoecetes tanneri, seven instars from first crab stage (3.8 mm carapace
width (CW)) to instar VII (26.8 mm CW) are identified from size-frequency histograms. The average
growth per molt for the first seven instars is 39% and the time from egg to instar VII is estimated to
be 20 months.
Measurements of chela length, abdomen width and carapace width were used to define two growth
phases for C. tanneri and to determine size at maturity for males (142.7 mm CW) and females (102.3
mm CW). The unequal sex ratio of adults (29% males) and presence of chitinoclastic lesions on 76% of
the adult females as compared with only 29% of the adult males suggest that adult females are anecdysic.
In this study of material collected off the southern Oregon coast, the mean adult carapace widths
for males and females is very close to the sizes reported for adult males and females (148.9 and 102.5
mm CW respectively) from the northern Oregon coast. The similarity in size extends to the material
collected from near the type location (Gulf of the Farallons) where instars VI and VII are 19.4 and 27.3
mm CW compared with 19.8 and 26.7 mm CW for the same instars from the southern Oregon coast.
The biotic stability at depths of maximum abundance (500-775 m) contributes to this uniformity.
The spider (or tanner) crab, Chionoecetes tanneri
Rathbun, is similar in size and morphology to the
better known and commercially harvested species
C. bairdi and C. opilio. Unlike C. bairdi and C. opilio
which are typically encountered in shallow waters
and are not reported deeper than 400 m in the
eastern Pacific, C. tanneri is a deep-water species
which ranges to 1,925 m and has its maximum abun-
dance at 500-775 m (Pereyra 1972).
Although C. tanneri is not likely to be fished
commercially because of its deep-water habitat and
certain aspects of its biology, Somerton (1981) sug-
gested that fluctuating supplies of Alaskan crab
species might promote more economical methods for
fishing in deep water. Red crab, Geryon quin-
quedens, taken from depths of 257-1,000 m between
Georges Bank and Cape Hatteras are landed com-
mercially in limited numbers on the eastern sea-
board (Lux et al. 1982; U.S. National Marine
Fisheries Service Fisheries Statistics 1985).
In part, because of its deep-water habitat, certain
life history aspects of C. tanneri are not well known.
Pereyra (1966, 1968) determined size at maturity
1 College of Oceanography, Oregon State University, Corvallis
OR 97331; present address: Southeast Fisheries Center Beaufort
Laboratory, National Marine Fisheries Service, NOAA, Beaufort,
NC 28516-9722.
2College of Oceanography, Oregon State University, Corvallis
OR 97331.
and described the seasonal distribution of adult and
late juvenile crabs. Egg development follows a year-
ly cycle with release of matured eggs and ovulation
of new eggs during the winter (Pereyra 1966). After
hatching, the total larval (pelagic) phase (prezoea,
zoea I, II and megalopa) is estimated to be 80 d
(Lough 1974). Samples collected mainly from a
series of cruises off the Oregon coast from 1972 to
1975 have provided us with C. tanneri specimens
from the first crab stage to adult. These specimens
have made it possible to identify a series of early
instars and to determine juvenile growth rates; they
also provided life history information on size at
maturity and adult and juvenile sex ratios for
comparison with earlier work. In addition, observa-
tions of the carapace condition of adults helped to
substantiate the anecdysic condition of adult
females.
METHODS
Sampling
Samples of C. tanneri were collected off the con-
tinental shelf and slope areas adjacent to Coos Bay,
OR (lat. 42°25'N, long. 124°50'W) in depths rang-
ing from 300 to 1,200 m during 10 cruises between
April 1973 and March 1975. A total of 1,625 crabs
Manuscript accepted February 1986.
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
973
FISHERY BULLETIN: VOL. 84, NO. 4
of both sexes ranging in size from 10 to 165 mm
carapace width (CW) were captured using two types
of trawl gear: a 9 m semi-baloon Gulf of Mexico
shrimp trawl and a 3 m beam trawl (Carey and
Heyamoto 1972). The stretched dimension of the
mesh for both trawl nets was 38 mm (1.5-in), and
the cod ends were lined with 12.7 mm (0.5-in) mesh.
In addition 47 of the smallest crabs (3-10 mm CW)
were found in the gut contents of sable fish, Ano-
plopoma fimbria, and Dover sole, Microstomias
pacificus, caught in these trawls. The Smithsonian
Institution provided another 306 juvenile tanner
crabs taken near the type location for C. tanneri
west of the Farallon Islands (lat. 37°30'N, long.
122°59'W) (Rathbun 1925) at 500-783 m.
Size at Maturity
The size at maturity for both male and female C.
tanneri was based on allometric measurements.
Allometry compares the difference in the propor-
tions of specific body parts with changes in absolute
size of a major body axis (Gould 1966). In Brachyura
the allometric growth of secondary sex characters
is well documented (Tessier 1960; Hartnoll 1969).
In the genus Chionoecetes it takes the form of dif-
ferential enlargement of the abdomen and modifica-
tion of pleopods in females whereas the size and
shape of the chelae are modified in the males
(Watson 1970; Brown and Powell 1972).
Carapace width for both male and female crabs
was measured at its widest part (mesobranchial
region) exclusive of spines (Fig. 1A). The male
carapace width was compared with the length of the
chelar propodus (CPL) which is measured from the
joint between the carpus to the tip of the fixed finger
of the propodus (Fig. IB), whereas the female
carapace width was compared with the width of the
abdomen (AW) which is measured at its widest part
(fifth segment) (Fig. 1C). Males with worn or broken
chelipeds were not used. All measurements were
made to the nearest 0.01 mm using precision dial
calipers, and numbers were rounded to the first
decimal for plotting. Plots of the measurements of
CW vs. CPL and CW vs. AW were used to identify
size at maturity for males and females.
Size-Frequency Histograms,
Growth, and Sex Ratio
Measurements of the carapace width were taken
from the 1,978 crabs available. Size-frequency histo-
grams were constructed and seven juvenile instars
were identified from dominant modes. Adult C. tan-
FlGURE 1.— Body dimensions of Chionoecetes tanneri measured for
size-frequency and allometric analyses. (A) Carapace width (o* and
9) measured at its widest part across the mesobranchial region
and exclusive of spines. (B) Chelar propodus length (cr) measured
from the joint between the carpus and the tip of the fixed finger
of the propodus. (C) Abdomen width (9) measured at its widest
part, across the fifth segment.
neri are sexually dimorphic with respect to body size
(Pereyra 1972). Since we did not know at which molt
this size dimorphism was first evident, the data for
males and females was shaded differently in the size-
frequency histogram. The juvenile sex ratio was
974
TESTER and CAREY: INSTAR IDENTIFICATION OF SPIDER CRABS
calculated for each instar, and when it was clear
from the equal sex ratio that juvenile males and
females were not dimorphic, the percent increase
in carapace width per molt was computed as
Percent increase in CW (mm) =
Postmolt CW (mm) - Premolt CW (mm)
Premolt CW (mm)
x 100
In one series of size-frequency histograms from
samples collected in June, July, and August 1974
and January and March 1975, the progression of
modes (representative of instars of the small
juveniles from fish gut contents) was used to
estimate growth rate. The next larger instar (CW
= 10 mm) was the first to be consistently sampled
by the trawl gear. Starting with the 10 mm CW in-
star from April 1973, growth of juvenile tanner
crabs was followed through August, October, and
November 1973 and March 1974.
Carapace Condition
Detailed observations were made of the carapace
on each specimen and included hardness, amount
of attached fauna, and general condition. Darkened
and softened or weakened areas on the carapaces
were similar to those caused by chitinoclastic bac-
teria (Sindermann 1970) and were thought to be
associated with age. Adult female C. tanneri were
especially subject to carapace deterioration.
RESULTS AND DISCUSSION
Since a high degree of correlation between gonad
maturity and external morphology has been shown
for the genus Chionoecetes (Brown and Powell 1972;
Donaldson et al. 1981), a plot of carapace width and
chela length (Fig. 2) was used to define adult males.
Specimens with chelae longer than 85 mm (corre-
sponding to carapace width >118 mm) were as-
sumed to be sexually mature males. Those females
E
E
D)
C
CD
CO
D
T5
O
a
o
05
CD
.C
O
140
130
120
110
100
90
80
70
60
50
40
30
20
10
0
N=760
.**■"'
0 10 20 30 40 50 60 70 80 90 100 1 10 120 130 140 150 160 170 180
Carapace Width (mm)
Figure 2.— Relationship between carapace width and chelar propodus length for juvenile and adult male Chionoecetes
tanneri.
975
FISHERY BULLETIN: VOL. 84, NO. 4
with abdomen widths > 50 mm (corresponding to
carapace widths >85 mm) form a well-defined group
(Fig. 3) of adults. The mean carapace width for adult
male and female crabs in this study was 142.7 and
102.3 mm respectively and was compared with the
mean carapace widths of 148.9 and 102.5 mm for
females given by Pereyra (1972) for adult C. tan-
neri collected south of the Columbia River mouth.
Brown and Powell (1972) reported a similar corre-
spondence in adult carapace widths for C. bairdi
collected from locations in Alaska. The large varia-
tion in size of mature male C. bairdi in the eastern
Bering Sea was clearly related at the clinal varia-
tion temperature (Somerton 1981).
Seven modes representing juvenile instars are evi-
dent from the size-frequency histograms (Fig. 4).
The mean carapace widths for each juvenile instar
were calculated and subsequently the increase in
CW per molt was computed (Table 1). The average
increase at each molt for instars I-VII is 39% and
there is no difference in growth increment of juve-
nile males and females In a laboratory study using
C. opilio, Miller and Watson (1976) reported that
growth per molt for immature females was signifi-
cantly greater than for immature males. But the
findings of Hilsinger et al. (1975) agree with ours.
They found no difference in growth rate for juvenile
male and female C. bairdi and reported a constant
growth rate of 27% for juvenile females. The change
in the slope of the regression lines of the log-log plots
of the allometric measurements of C. tanneri (Fig.
5) indicated a change in the rate of growth only at
sexual maturity. Chionoecetes tanneri, like C. opilio
(Watson 1970), showed two growth phases, one for
juveniles and one for adults.
If C. tanneri eggs hatch predominantly in winter
(January-March) and the total larval life is 80 d, the
recruitment of the smallest crab stage (CW = 4) to
the population in June- July is in agreement with our
findings. Instars can be followed from 4 mm CW
(instar I) in June and July 1974, to 5.5 cm CW (in-
star II) in August 1974, to 7.5 mm CW (instar III)
in January 1975 (Fig. 6). The smallest specimens
sampled by the trawls were about 10 mm CW, and
there were relatively large numbers of these instar
IV specimens in April 1973 which molted to instar
V by August and to instar VI in October 1973 (Fig.
7). No growth of these instar VI crabs is evident
from the November 1973 or March 1974 data. We
estimate approximately 20 mo from egg hatching
to instar VII (CW = 26.8 mm) (Fig. 8).
Observations on general carapace condition and
abundance of epifauna indicate that adult male C.
tanneri do molt frequently enough to maintain their
E
E
T3
CD
E
o
<
70i
60
50
2 40
30
20
10
N=851
♦ ♦ ♦
.♦♦%
♦♦
♦**♦
«♦♦
10 20 30 40 50 60 70 80 90 100 110 120 130
Carapace Width (mm)
Figure 3.— Relationship between carapace width and abdomen width for juvenile and adult female Chionoecetes tanneri.
976
TESTER and CAREY: INSTAR IDENTIFICATION OF SPIDER CRABS
155
c
c
en
W
0)
CD
u
0)
o
c
g
O
d)
.O
e
3
Carapace Width (mm)
Figure 4.— Size-frequency histograms representing all specimens of Chionoecetes tanneri collected off the Oregon coast 1973-75 and
from the Gulf of the Farallons. Instars I-VII are indicated. Males are shown in solid color.
carapaces relatively free of epifauna and lesions
caused by bacterial infections (Baross et al. 1978).
Of the 290 adult female specimens examined, 87%
showed exoskeleton lesions and these adult females
also had the highest diversity and abundance of epi-
fauna on their exoskeletons. Only 29% of the 124
adult males observed showed the effect of chitino-
clastic bacterial infection. No lesions or epifauna
were found on any of the 1,447 juveniles examined.
In contrast to the findings of Hartnoll (1969) who
worked with shallow-water spider crabs, observa-
tions of the carapace condition of adult male and
female C. tanneri suggests adult males continue to
molt after maturity while adult females are anec-
dysic, a finding consistent with Watson's (1970) data
for C. vpilio. The unequal adult sex ratio (29% males,
Table 1) is also an indication that males may be sub-
jected to the differential mortality of continued
molting.
The agreement of mean CW for adults collected
off the Oregon coast in the study and that of
Pereyra's (1966) work has an interesting corollary
in the material collected from near the Farallon
Islands. The mean carapace width of instars VI and
VII for C. tanneri collected west of the Farallon
Islands is 19.4 and 27.3 mm respectively. The cara-
pace widths for the same instars collected from
Oregon is 19.8 and 26.7 mm. Childress and Price
(1978) credited the constant increase in size between
each pair of instars in the deep-living, midwater
977
FISHERY BULLETIN: VOL. 84, NO. 4
Figure 5.— Growth phases for juvenile and adult
Chionoecetes tanneri. CPL = Chelar propodus length
(mm); CW = Carapace width (mm); AW = Abdomen width
(mm).
200
E
E
•g
c
<u
E
o
£ 50
*6
c
0)
v>
3
•o
o
Q.
o
sz
O
40
30
20-
10
Adult
CPL = 1.21 CW - 57.16
r2.91
Adult
AW * 0.54 CW - 3.07 jfj
2
Juvenile
CPL = 0.56 CW - 3.37 X /
/
2 X *
r .97 X /
/
/
/
/
* Juvenile 0
/ T
AW = 0.46 CW - 3.33
/ ,2.99
20
— i 1 1 —
30 40 50
100
150
Carapace width mm
c
c
(D
(1)
O
Q)
O
C
g
o
a>
E
3
Z
4-
2-
0
4
2
0
4
2
-i r
November 1973
N = 1
i — I — r-^| 1 r
June 1974
N=10
-i 1 ra*T
i — r
July 1974
N=4
-i 1 1 1
N August 1974
y '■■*
-i r
January 1975
N=14 \
in
T 1 1 1 "■ "f""\>
March 1975
N=3
-i r
2
"1 1 i 1 — "7—
6 8 10
Table 1 . — Percent increase in mean carapace width and sex ratio
(males %) for successive instars of Chionoecetes tanneri.
Increase in
carapace width
(%)
48.4
35.8
31.7
43.0
36.5
36.6
N
Males
(0/0)
Carapace width
(mm)
Instar
Mean
s2
I
16
53
3.80
0.25
II
19
—
5.64
0.62
III
18
53
7.66
0.53
IV
175
49
10.09
0.57
V
281
49
14.43
0.68
VI
499
50
19.69
1.18
VII
268
53
26.83
3.40
Adults
411
29
Carapace Width (mm)
Figure 6.— Size- frequency histograms representing early juveniles
with carapace widths < 9 mm. These samples were collected from
stomachs of benthic fish. The dashed line represents the progres-
sion of instars through time with first crab stage in June to instar
II in August and instar III in January.
978
TESTER and CAREY: INSTAR IDENTIFICATION OF SPIDER CRABS
Cruise 1
April 1973
N=93
Figure 7.— Size-frequency histograms representing
juveniles with carapace widths 10-50 mm wide. The
dashed line represents progression of instars through
time with instar IV in April, instar V in August and
instar VI in October through March.
c
c
(0
•4-+
CO
CO
o
<0
o
c
o
!E
O
.Q
E
3
Cruise 3
October 1973
N=143
Cruise 4
November 1973
N= 102
Carapace Width (mm)
E
E
»-*
X
h-
Q
30 -r
25
20-
15
LU
o
<
tt 10-
<
o
megalopoa
«S9»
n — i — i — i — i — i — i — i — i — i — i — | — i — i — i — i — r
January January
TIME (month)
T 1 1 — I 1 — J
January
Figure 8.— Growth rate of Chionoecetes tanneri from egg to seventh instar is estimated to be
at least 20 mo. Dotted lines indicate standard deviation.
979
FISHERY BULLETIN: VOL. 84, NO. 4
mysid, Gnathophausis ingens, to the physical and
biotic stability of this species' environment. Various
environmental factors can alter both the dimensions
and the number of molts in many species of crus-
taceans. At depths of maximum abundance (500-775
m) of C. tanneri, the annual water ranges from 2.3°
to 5.6°C and certainly this uniform environment
contributes to the consistency of instar size and size
at maturity.
ACKNOWLEDGMENTS
We appreciate the assistance of Brian Oliver.
Howard Horton and David Colby reviewed this
manuscript and their time and efforts have greatly
contributed to it. Robert S. Carney was responsible
for the loan of Chionoecetes tanneri from the Smith-
sonian Institution. This research was funded by
NOAA (maintained by the U.S. Department of Com-
merce) Sea Grant Institution Grant Nos. NOAA
04-3-158-1 and NOAA 04-5-158-2. Data analysis was
facilitated by a grant from the Oregon State Uni-
versity Computer Center.
LITERATURE CITED
Baross, J. A., P. A. Tester, and R. Y. Morita.
1978. Incidence, microscopy, and etiology of exoskeleton
lesions in the tanner crab, Chionoecetes tanneri. J. Fish.
Res. Board Can. 35:1141-1149.
Brown, R. B., and G. C. Powell.
1972. Size at maturity in the male Alaskan tanner crab, Chio-
noecetes bairdi, as determined by chela allometry, reproduc-
tive tract weights, and size of precopulatory males. J. Fish.
Res. Board Can. 29:423-427.
Carey, A. G., and H. Heyamoto.
1972. Techniques and equipment for sampling benthic organ-
isms. In A. T. Pruter and D. L. Alverson (editors), Colum-
bia River estuary and adjacent ocean waters: Bioenviron-
mental studies, p. 378-412. Univ. Wash. Press, Seattle.
Childress, J. J., and M. H. Price.
1978. Growth rate of the bathypelagic crustacean Gnatho-
phausia ingens (Mysidacea: Lophogastridae). I. Dimen-
sional growth and population structure. Mar. Biol. (Berl.)
50:47-62.
Donaldson, W. E., R. T. Cooney, and J. R. Hilsinger.
1981. Growth, age and size at maturity of tanner crab, Chio-
noecetes bairdi M. J. Rathbun, in the northern Gulf of Alaska
(Decapoda, Brachyura). Crustaceana 40:286-302.
Gould, S. J.
1966. Allometry and size in ontogeny and phylogeny. Biol.
Rev. 41:587-640.
Hartnoll, R. G.
1969. Mating in the Brachyura. Crustaceana 16:161-181.
Hilsinger, J. R., W. E. Donaldson, and R. T. Cooney.
1975. The Alaskan snow crab, Chionoecetes bairdi, size and
growth. Univ. Alaska Sea Grant Rep. No. 75-12, Inst. Mar.
Sci., 75-6 p.
Lough, R. G.
1974. Dynamics of crab larvae (Anomura, Brachyura) off the
central Oregon coast, 1969-1971. Ph.D. Thesis, Oregon
State Univ., Corvallis, 299 p.
Lux, F. E., A. R. Ganz, and W. F. Rathjen.
1982. Marking studies on the red crab (Geryon quinquedens)
Smith off southern New England. J. Shellfish. Res. 2:71-
80.
Miller, R. J., and J. Watson.
1976. Growth per molt and limb regeneration in the spider
crab, Chionoecetes opilio. J. Fish. Res. Board Can. 33:
1644-1649.
Pereyra, W. T.
1966. The bathymetric and seasonal distribution, and repro-
duction of adult tanner crabs, Chionoecetes tanneri Rathbun
(Brachyura: Majidae), off the northern Oregon coast. Deep-
Sea Res. 13:1185-1205.
1968. Distribution of juvenile tanner crabs (Chionoecetes tan-
neri) Rathbun, life history model, and fisheries management.
Proc. Natl. Shellfish. Assoc. 58:66-70.
1972. Bathymetric and seasonal abundance and general
ecology of the tanner crab, Chionoecetes tanneri Rathbun
(Brachyura: Majidae) off the northern Oregon coast. In
A. T. Pruter and D. L. Alverson (editors), Columbia River
estuary and adjacent ocean waters: Bioenvironmental
studies, p. 538-582. Univ. Wash. Press, Seattle.
Rathbun, M. J.
1925. The spider crabs of America. Bull. U.S. Natl. Mus.
129, 613 p.
SlNDERMANN, C. J.
1970. Principal diseases of marine fish and shellfish. Acad.
Press, N.Y., 369 p.
SOMERTON, D. A.
1981 . Regional variation in the size of maturity of two species
of tanner crab (Chionoecetes bairdi and C. opilio) in the
eastern Bering Sea, and its use in defining management
subareas. Can. J. Fish. Aquat. Sci. 38:163-174.
Tessier, G.
1960. Relative growth. In T. Waterman (editor), The phys-
iology of Crustacea, Vol. 1, p. 537-560. Acad. Press, N.Y.
U.S. National Marine Fisheries Service.
1985. Fisheries of the United States, 1984. U.S. Natl. Mar.
Fish. Serv., Curr. Fish. Stat. 8360, 121 p.
Watson, J.
1970. Maturity, mating, and egg laying in the spider crab,
Chionoecetes opilio. J. Fish. Res. Board Can. 27:1607-1616.
980
NOTES
COMPARISON OF CATCHES IN 4.3 M
AND 12.2 M SHRIMP TRAWLS IN
THE GULF OF MEXICO
Shrimp trawls used to assess shrimp and fish popula-
tions in the southern United States have varied in
length, width, and basic design, making comparisons
of results among studies difficult. Fishery manage-
ment plans by State and Federal agencies emphasize
the need for data that can be reliably compared.
Techniques and equipment necessary to measure
trawl performance so that data collected with dif-
ferent trawls can be compared is costly and time
consuming (Watson 1976; Loesch et al. 1976;
Wathne 1977; Kjelson and Johnson 1978). Recent
emphasis has been placed on standardizing gear and
sampling methods (Watson and Bane 1985) and
determining the effects on catch and mean length
of organisms for different tow durations, mesh sizes,
trawl widths, and towing vessels (Clark 1963; Chit-
tenden and Van Engle 1972; Green and Benefield
1982; Matthews 1982; Cody and Fuls 1985). How-
ever, sample sizes generally have been small and
only selected species have been analyzed.
The present study evaluates small trawls as popu-
lation sampling devices for penaeid shrimp and other
organisms in the Gulf of Mexico. The objective of
this study was to compare the catch rates and mean
lengths of organisms caught with 4.3 m and 12.2 m
trawls pulled during day and night.
Materials and Methods
The study area was the Gulf of Mexico off Texas
between the Colorado River and Port Mansfield in
depths from 7 m to 24 m (Fig. 1). Sample sites were
established in 1° latitude by 1° longitude grids
within the study area. Twenty randomly selected
sites were sampled monthly from November 1982-
February 1983. Samples were equally and random-
ly distributed between day and night.
At each site two trawls were towed simultaneous-
ly for 15 min at approximately 3 kn from the Texas
Parks and Wildlife Department (TPWD) RV
Western Gulf, a double-rigged 21.9 m steel-hull
shrimp trawler. The 4.3 m trawl (small net) was
spread by wooden trawl doors 0.4 m high and 0.8
m long and the 12.2 m wide trawl (large net) was
spread by wooden trawl doors 0.9 m high and 2.1
m long. Both nets had 5.1 cm stretched mesh web-
bing in the body, 4.4 cm mesh in the bag, and were
equipped with tickler chains.
Trawl catches weighing <10 kg were processed
by identifying and counting all organisms in the
catch. For larger catches a 10 kg subsample was ran-
domly selected from the total catch, and the total
number for each species was estimated by dividing
subsample counts by the proportion of subsample
weight to total weight. Total lengths were measured
on no more than 50 individuals of each Penaeus
shrimp species and no more than 20 individuals of
all other species. The arithmetic mean for length
data was calculated for each species in each sample.
The relationship between number caught (or mean
length) in the two trawls was tested for linear, mul-
tiplicative and exponential models, and log and
square root transformations (Sokal and Rohlf 1981).
No significant improvement was found over a linear
regression with no transformation. Mean length
regressions were developed for species with 10 or
more pairs of mean length data (>2 measurements)
in each size of trawl (Fig. 2). Catch regressions were
developed for those species that were present in at
least 20 samples in the large net and were repre-
sented by at least 5 samples with >20 individuals
in the small net. This insured a sufficiently wide
distribution to yield meaningful results (Fig. 3).
Differences (P < 0.01) between day and night
regressions for each species were evaluated using
analysis of co variance (Snedecor and Cochran 1980).
Results
Small trawls can be used to obtain trend data on
mean lengths of species caught in offshore waters.
Relationships exist between the catch in the 4.3 m
trawl vs. the catch in the 12.2 m trawl. No signifi-
cant differences were found in the day-night regres-
sions of mean length for any species tested. There
was no difference in the day-night catch vs. catch
relationship for total organisms or Penaeus setiferus
but one did exist for Trachypenaeus sp. and Squilla
empusa.
Mean lengths in the two trawls were directly cor-
related for all species that met criteria for regres-
sion analysis (Table 1). The regressions of the mean
length of fish caught in one net vs. the other for day
and night were not significantly different for any
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
981
Figure 1.— Gulf of Mexico sampling area off the Texas coast for 4.3 m and 12.2 m trawls towed simultaneously during
November 1982-February 1983.
982
of the species tested (Table 2). The combined regres-
sions had significant positive correlations (0.51-0.89)
explaining 26-79% of the variation.
Catch per tow in the two trawls was positively cor-
related. Correlation coefficients (0.48-0.93) were
significant for all species meeting the criteria for
analysis (Table 3). The percent of variation explained
(r2) varied from 23 to 86%.
There were no significant differences in the day-
night catch vs. catch relationships for total organ-
Table 1.— Linear regression results of 4.3 m trawl mean length (X,) versus the 12.2 m trawl length (V,) for selected species.
Species
Time
Range of
Number
/-intercept
Slope
(b)
Correlation
coefficient
S2 Y ■ X
95% confidence
interval of b
Penaeus setiferus
Day
Night
Combined
93-135
94-164
93-164
29
32
61
12.31
16.29
14.48
0.91
0.87
0.89
0.85**
0.93**
0.88**
61.33
22.98
39.86
0.68-1.13
0.74-1.00
0.76-1.01
Stellifer lanceolatus
Day
Night
Combined
44-125
44-115
44-125
11
24
35
26.35
28.32
27.42
0.70
0.67
0.68
0.91**
0.88**
0.89**
88.77
65.60
68.19
0.45-0.95
0.51-0.83
0.56-0.80
Trachypenaeus sp.
Day
Night
Combined
50-78
50-84
50-84
22
36
58
38.03
43.03
41.77
0.47
0.40
0.42
0.61**
0.61**
0.62**
17.55
19.28
18.03
0.18-0.76
0.22-0.58
0.28-0.56
Portunus gibbesii
Day
Night
Combined
30-48
30-55
30-55
14
30
44
26.44
23.81
25.43
0.39
0.41
0.38
0.53*
0.62**
0.56**
11.78
9.70
10.53
-0.01-0.78
0.21-0.61
0.21-0.56
Squilla empusa
Day
Night
Combined
77-104
48-132
48-132
10
31
41
49.37
69.43
65.78
0.46
0.32
0.34
0.62ns
0.51**
0.51**
48.08
86.95
83.87
0.04-0.89
0.11-0.52
0.15-0.53
Cynoscion nothus
Day
Night
Combined
62-110
70-122
62-122
25
21
46
52.02
45.59
46.18
0.42
0.44
0.46
0.63**
0.71**
0.67**
43.87
30.64
42.16
0.20-0.64
0.23-0.65
0.31-0.62
*P< 0.05.
"P<0.01.
Table 2.— Summary of ANCOVA for mean length of selected species.
Calculated
Calculated
Calculated
Fsfor
Fsfor
Fsfor
Species
df
W0:o, = o2
df
H0:p, = p2
df
HQ:ct, = a2
Penaeus setiferus
(27,30)
2.67 ns
(1,57)
0.04 ns
(1,58)
0.07 ns
Stellifer lanceolatus
(9,22)
1.35 ns
(1,31)
0.03 ns
(1,32)
0.04 ns
Trachypenaeus sp.
(34,20)
1.10 ns
(1,54)
0.09 ns
(1,55)
0.00 ns
Portunus gibbesii
(12,28)
1 .22 ns
(1,40)
0.00 ns
(1,41)
2.89 ns
Squilla empusa
(29,8)
1.81 ns
(1,37)
0.15 ns
(1,38)
4.46 ns
Cynoscion nothus
(23,19)
1 .43 ns
(1,42)
0.01 ns
(1,43)
7.12 ns
Table 3.— Linear regression results of 4.3 m trawl catch/tow (X,) versus the 12.2 m trawl catch/tow (V,) for total organisms and
selected species.
Species
Time
Range of
Number
/-intercept
Slope
(b)
Correlation
coefficient
S2YX
95% confidence
interval of b
Total organisms
Day
Night
Combined
16-212
43-210
16-212
40
40
80
352.71
593.65
420.42
5.83
6.04
6.53
0.58**
0.48**
0.55**
143,234.17
310,412.80
237,569.91
3.18-8.47
2.45-9.64
4.31-8.75
Penaeus setiferus
Day
Night
Combined
0-55
0-51
0-55
40
39
79
12.21
-0.87
7.40
5.37
6.96
6.14
0.90**
0.87**
0.88**
1,129.54
2,291.77
1,757.99
4.51-6.23
5.65-8.26
5.38-6.90
Squilla empusa
Day
Night
0-28
0-37
40
39
6.03
-5.58
4.50
6.81
0.93**
0.85**
139.44
1,438.75
3.92-5.07
5.38-8.25
Trachypenaeus sp.
Day
Night
0-45
0-43
40
40
20.63
60.23
13.38
19.51
0.80**
0.73**
13,040.70
40,354.41
10.15-16.60
13.46-25.67
Portunus gibbesii
Night
0-114
40
24.65
5.92
0.78**
9,961.84
4.40-7.45
Lolliguncula brevis
Day
0-42
40
9.92
1.66
0.72**
292.57
1.14-2.19
**P< 0.01.
983
170
160
150
140
130
-J
120
£
<f
1 10
&
h-
100
S
<-N|
<N
PENAEUS SETIFERUS
120
I 10
100
90
K0 -
70
60 -
50
STELLIFER LANCEOLATUS
— i 1 1 i 1 i i ■
100 110 120 130 140 150 160 170
50 60 70 HO
— r—
90
1 00 110
— I —
120
x
O
z
u
-J
z
s
80
70
60 -
50 -
TRACHYPENAEUS SP.
- 1 —
50
60
50 -
40 ■
30
PORTUNUSGIBBESII
60
70
SO
30
— i —
40
- 1 —
50
- 1
60
MEAN LENGTH (MM) IN 4.3 M TRAWL
Figure 2.— Regression of mean length in 12.2 m trawl (Yi) on mean length in 4.3 m trawl (Xt) for comparative tows during November
1982-February 1983. Observations, regression line, and 95% confidence intervals are shown.
984
<
130 -
120 -
10 •
100 ■
90
80 -
70
60 -
SQUILLA EMPUSA
50 60 70
— ■ i 1 1 1 i 1 —
HO 90 100 110 120 1 30
X
o
u
z
w
130
120
I 10
100
90
SO
70
60
CYNOSCION NOTHUS
- 1 1 1 1 1 1 r
70 80 90 100 110 120 130
MEAN LENGTH (MM) IN 4.3 M TRAWL
Figure 2.— Continued.
985
2500 - TOTAL ORGANISMS
jiiiiii -
-J
<
H
S
1500 -
1000
500 -
PENAEUSSETIFERUS
40(1 -
?00 ■
200
100
20 40
m-i 1 1 1 1 1 1 1 —
60 X0 100 120 140 160 ISO 200
10 20 .?0 40 50 60
SQUILLA EMPUSA il)\Vi
SOI III \ I MPLSA (NIGHT I
4ll>
175
250
200
175
150 -
125 -
100
75
50 -
10 15
NUMBER PER TOW IN 4.3 M TRAWL
Figure 3.— Regression of catch per tow in 12.2 m trawl (Yt) on catch per tow in 4.3 m trawl (AT,) for comparative tows during November
986
1 200-
TRACHYPENA£US<l)A\ I
1 100-
1 000-
900-
soo-
•
700-
•
600-
500-
—
<
400-
300-
• jS^
•
1
200-
^r ^r i^S*
(N
ri
100-
Z
A*' i — i 1 r
1 1 —
1 i
1 200-1
1100
1000
900
xoo-
700
600
TRACHYPLNAEUS (NIGHT)
W 35 40 45
35 40 45
100-
LOLL1GUNCULA BREVIS (DAY)
40-
XO-
70-
60-
s S^
50-
/ • f S'
40-
• / / /
30-
20-
/ 3r / •
10 ■
•
1 1 i ■ i • i —
■ i
10 15 20
30 35 40
NUMBER PER TOW IN 4.3 M TRAWL
Figure 3.— Continued. — 1982-February 1983. Observations, regression line, and 95% confidence intervals are shown.
987
isms or P. setiferus. Significantly different residual
variances were found for S. empusa and Trachy-
penaeus sp. (Table 4).
The 12.2 m trawl caught more individuals and
more species than the 4.3 m trawl (Table 5). The
large trawl caught 30,000 organisms during the day
and 46,000 during the night. The small trawl caught
3,000 during the day and 3,800 during the night. The
large trawl caught 99 species during the day and
107 during the night, while the small trawl caught
63 species during the day and 82 during the night.
The trend of more species caught in the large trawl
was apparent for vertebrates both day and night and
invertebrates during the day. The same number of
invertebrate species were caught at night in both
trawls. Species caught exclusively in one trawl were
usually represented by fewer than 30 individuals
during the entire study.
Only 26 of 125 species were represented by a
mean catch ^5/tow in either trawl (Table 6). These
26 species comprised 95% of the total catch.
small trawl it was 0.03. The fishery manager must
decide if an increase in species diversity helps
manage a particular fishery and ultimately whether
it is cost effective to go after these "rare" in-
dividuals.
Catch in the large trawl may be higher than in the
small trawl because of higher efficiency. Kjelson and
Johnson (1978) reported higher catch efficiencies for
a 6.1 m trawl than for a 3.0 m or 4.6 m trawl. Loesch
et al. (1976) reported 5% efficiency for Leiostomus
xanthurus in a 4.0 m trawl while Kjelson and John-
son (1978) reported 32% for the same species in a
6.1 m trawl.
The relationship between trawl width and catch
may be asymptotic. This study showed the 12.2 m
trawl caught more organisms than the 4.3 m trawl.
Cody and Fuls (1985) found the same trend but
reported that the catch in the 12.2 m trawl was not
significantly less than the catch in the 13.7 m trawl.
Matthews (1982) found no difference in mean total
weight caught in 12.2 m and 13.7 m trawls. He did
Table 4.— Summary of ANCOVA for catch per tow of total organisms and selected species.
Calculated
Calculated
Calculated
Fsfor
Fsfor
Fsfor
Species
df
W0:°i = o2
df
«O01 = ft»
df
W0:a1 = °2
Total organisms
(38,38)
2.17 ns
(1,76)
0.01 ns
(1.77)
5.76 ns
Penaeus setiferus
(37,38)
2.03 ns
(1,75)
4.32 ns
(1,76)
0.16 ns
Squilla empusa
(37,38)
10.32 **
Trachypenaeus sp.
(38,38)
3.09 **
"P< 0.01.
Discussion
Catches in the large trawl were consistently
higher than in the small trawl. Chittenden and Van
Engel (1972) stated there must be some relationship
between catch and tow duration because of the
amount of bottom sampled, but they found that in-
creased tow duration (which increases area covered)
did not significantly increase the catch of blue crabs
in a 9.1 m trawl. However, they tested only a small
range of tow durations (5-15 min) and concluded that
variation in the trawl catches was a significant fac-
tor. Tow duration in this study was constant, so
higher catches were most likely a result of more area
being sampled by the larger net.
It also seems reasonable that a large trawl would
have a greater chance of encountering organisms
especially if they have patchy distributions such
as found with shrimp (Matthews 1982). The large
net caught more species than the small net in this
study. The highest mean catch per tow was 0.37 for
species found exclusively in the large trawl; for the
not, however, compare the total number or size of
organisms. Because of the inherent variation found
in sampling with trawls, the inability to detect differ-
ences in the 12.2 m and 13.7 m trawls would be
expected.
Implications of this may apply to the commercial
trawl fishery. Through the years shrimp fishermen
have been reducing the size of trawls and increas-
ing the number of trawls used in order to increase
catch efficiency (Christmas and Etzold 1977). These
changes may reflect the asymptotic relationship of
trawl width and at the same time help reduce un-
wanted by catch.
Cody and Fuls (1985) reported a regression coef-
ficient of 2.52 for the catch vs. catch relationship
for P. setiferus in daytime samples in contrast to
5.37 for this study. Only 13 data points over a much
wider range of Xi (0-136/tow vs. 0-55/tow) were
used by Cody and Fuls. When the ranges of X{
were made comparable the slopes of the two regres-
sions were not significantly different.
The use of small trawls and determination of rela-
988
Table 5.— Total number of organisms collected with 4.3 m and 12.2 m trawls towed simultaneously off the central Texas coast from
November 1982-February 1983. Blanks = no data.
Day
Night
Species
4.3 m
12.2 m
4.3 m
12.2 m
Vertebrates
Cynoscion nothus
257
8,781
190
8,981
Stellifer lanceolatus
80
1,110
333
4,559
Cynoscion arenarius
48
1,383
46
2,498
Peprilus burti
106
1,903
20
344
Leiostomus xanthurus
118
1,510
9
68
Arius felis
77
775
17
283
Symphurus plagiusa
40
297
60
470
Lagodon rhomboides
43
357
36
360
Syacium gunteri
29
400
29
235
Anchoa mitchilli
16
372
12
222
Larimus fasciatus
30
188
31
356
Menticirrhus americanus
9
164
23
315
Micropogonias undulatus
23
218
17
237
Trichiurus lepturus
6
309
3
167
Selene setapinnis
16
269
4
88
Sphoeroides parvus
17
162
16
178
Orthopristis chrysoptera
14
87
19
133
Peprilis alepidotus
8
91
4
77
Menticirrhus littoralis
8
66
2
100
Etropus crossotus
5
37
16
116
Prionotus salmonicolor
4
10
6
137
Astroscopus y-graecum
1
37
11
93
Brevoortia patronus
1
6
2
124
Prionotus tribulus
9
43
12
63
Chloroscombrus chrysurus
28
4
87
Hemicaranx amblyrhynchus
1
63
2
26
Citharichthys spilopterus
8
21
16
43
Halieutichthys aculeatus
6
10
8
62
Urophycis floridanus
5
27
6
38
Achirus lineatus
2
26
27
Dasyatis sabina
1
19
32
Synodus foetens
28
1
13
Ophidion welshi
1
7
4
25
Porichthys plectrodon
11
2
24
Trachurus lathami
28
2
Anchoa hepsetus
24
Saurida brasiliensis
16
3
Paralichthys lethostigma
12
6
Chaetodipterus faber
10
3
4
Opisthonema oglinum
15
2
Lutjanus campechanus
2
3
11
Bairdiella chrysoura
1
9
1
5
Chilomycterus schoepfi
9
5
Ogcocephalus parvus
3
4
6
Centropristis philadelphica
1
4
8
Monacanthus hispidus
4
3
5
Bollmannia communis
5
4
Rhinoptera bonasus
6
3
Paralichthys albigutta
1
5
3
TRIGLIDAE (Unidentified)
4
4
Lepophidium graellsi
1
7
Pomatomus saltatrix
1
1
6
Selene vomer
4
4
Gymnachirus texae
3
1
3
Polydactylus octonemus
4
1
Narcine brasiliensis
5
Eucinostomus gula
3
2
Serranus atrobranchus
2
2
Sygnathus scovelli
2
1
1
Ophidion gray!
3
Pogonias cromis
1
2
Mugil cephalus
2
Serraniculus pumilio
2
Ancylopsetta quadrocellata
2
Membras martinica
2
Day
Night
Species
4.3 m 12.2 m 4.3 m 12.2 m
Prionotus rubio
Sardinella aurita
Diplectrum bivittatum
Eucinostomus argenteus
Raja texana
Bregmaceros atlanticus
Ogcocephalus radiatus
GERREIDAE (Unidentified)
Bagre marinus
Lutjanus apodus
Prionotus ophryas
Total
Invertebrates
Trachypenaeus sp.
Penaeus setiferus
Portunus gibbesii
Squilla empusa
Lolliguncula brevis
Callinectes similis
Renilla mulleri
Stomolophus melaegris
Penaeus duorarum
Sicyonia dorsalis
Portunus spinimanus
Brissopsis alta
ACTINIARIA (order)
Arenaeus cribrarius
Astropecten antillensis
Luidia clathrata
Xiphopeneus kroyeri
Penaeus aztecus
Aurelia aurita
Libinia dubia
Millita quinquiesperforata
Persephona aquilonaris
Sequilla neglecta
Libinia emarginata
Ovalipes guadulpensis
Hepatus epheliticus
Persephona crinita
Dactylometra quinquecirrha
Luidia alternata
Polinices duplicatus
Loligo peali
Calappa sulcata
Sicyonia brevirostris
Phalium granulatum
Squilla chydaea
Thais haemostoma
Callinectes sapidus
Anadara ovalis
Albunea paretii
Dinocardium robustum
Synalpheus fritzmuelleri
Hepatus pudibundus
Mnemiopsis mccradyi
Architectonica nobilis
Busycon perversum
Calappa flammea
Portunus spinicarpus
Sinum perspectivum
REPTANTIA (suborder)
Total
Grand Total
2
1
1
992 18,995 984 20,699
297
347
113
115
304
73
157
165
7
6
181
31
110
33
11
7
16
9
1
9
6
5
4
3
1
2
1
2
4,798
2,352
876
758
902
447
379
486
54
19
16
58
42
15
54
21
109
70
52
19
21
2
3
7
9
2
2
4
10
1
7
5
467 1 1 ,522
594 4,180
561
390
25
109
218
24
34
36
42
35
62
60
30
61
9
33
20
5
3
4
6
12
2
6
1
1
4
2
1
1
1
4,332
2,173
515
1,013
369
294
298
280
263
36
133
139
21
61
5
44
6
28
1
9
16
17
6
11
4
12
3
6
1
2
6
1
3
1
1
1
1
2,017 11,604 2,867 25,814
3,009 30,599 3,851 46,513
989
Table 6.— Mean catch per tow (+ 1 SE) of dominant species1, November 1982-February
1983. Blank = no catch.
i
Day
Night
Species
1.3
m
12.2
m
4.3
m
12.2 m
Vertebrates
Cynoscion nothus
6
±
1.2
219
+
43.0
5
+
0.9
225
+ 33.6
Stellifer lanceolatus
2
±
0.7
28
±
12.0
8
±
2.6
114
+ 29.8
Cynoscion arenarius
1
+
0.3
34
+
7.7
1
+
0.2
62
± 14.5
Peprilus burti
3
+
1.0
47
+
16.1
0
±
0.3
9
± 2.9
Leiostomus xanthurus
3
±
1.9
38
±
27.9
0
+
0.1
2
+ 0.7
Arius felis
2
+
1.8
20
+
18.0
0
±
0.3
7
± 3.4
Symphurus plagiusa
1
±
0.3
7
+
2.1
2
±
0.3
12
± 2.0
Lagodon rhomboides
1
±
0.6
9
±
4.7
1
+
0.3
9
+ 3.2
Syacium gunteri
1
±
0.2
10
+
2.6
1
±
0.2
6
+ 1.6
Anchoa mitchilli
0
+
0.2
9
±
4.0
0
±
0.2
6
± 2.4
Larimus fasciatus
1
±
0.4
5
+
2.2
1
+
0.3
9
+ 3.7
Menticirrhus americanus
0
±
0.1
4
+
1.3
1
±
0.2
8
± 1.7
Micropogonias undulatus
1
±
0.2
5
+
1.4
0
+
0.2
6
+ 1.4
Trichiurus lepturus
0
±
0.1
8
±
2.1
0
+
0.0
4
± 0.9
Selene setapinnis
0
+
0.3
7
±
5.8
0
±
0.0
2
± 1.5
Invertebrates
Trachypenaeus sp.
7
+
1.8
120
±
30.1
11
±
1.7
228
± 45.6
Penaeus setiferus
9
±
2.0
59
+
11.9
15
+
3.1
104
+ 24.2
Portunus gibbesii
3
+
1.1
2
±
4.4
14
±
3.3
108
+ 25.2
Squilla empusa
3
±
1.0
19
+
5.0
10
+
1.7
54
+ 10.9
Lolliguncula brevis
8
±
1.7
23
+
3.8
1
±
0.2
13
± 1.9
Callinectes similis
2
±
0.8
11
+
4.6
3
±
0.6
25
± 6.0
Renilla mulleri
4
+
1.5
9
±
3.0
5
±
2.2
9
+ 3.3
Stomolophus melaegris
4
±
3.4
12
±
6.0
1
±
0.3
7
± 3.0
Penaeus duorarum
0
±
0.1
1
±
0.6
1
±
0.4
7
± 5.0
Sicyonia dorsalis
0
+
0.3
1
±
0.3
7
+ 2.0
Portunus spinimanus
0
+
0.1
0
+
0.2
1
±
0.6
7
+ 2.9
1Mean catch >5/tow in either net.
tionships between day and night catches in a fishery
independent assessment program can increase sam-
pling frequency and decrease the cost of sampling
by reducing processing time, manpower require-
ments, and variability caused by subsampling large
catches. Samples from the small trawl could be pro-
cessed in approximately 25% of the time required
for sample processing from the large trawl. The
small trawl required no subsampling. Management
agencies should consider these findings when plan-
ning long-term programs.
Acknowledgments
We would like to express our appreciation to each
member of the Gulf Research Program who so
conscientiously collected scheduled samples. Thanks
are extended to the Texas Parks and Wildlife
Department review committee and an unknown
reviewer for their valuable comments. Nancy
Ziegler prepared the manuscript. This study was
conducted with partial funding from the U.S.
Department of Commerce; National Oceanic and At-
mospheric Administration, National Marine Fish-
eries Service, under P.L. 88-309 (Project 2-385-
R).
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biological research. 2d ed. W. H. Freeman and Co., San
Francisco, 859 p.
Wathne, F.
1977. Performance of trawls used in resource assessment.
Mar. Fish. Rev. 39(6):16-23.
Watson, J. W., Jr.
1976. Electric shrimp trawl catch efficiency for Penaeus
duorarum and Penaeus aztecus. Trans. Am. Fish. Soc. 105:
135-148.
Watson, J. W., Jr., and N. Bane (editors).
1985. Proceedings of the SEAMAP shrimp and bottomfish
sampling gear workshop. Gulf States Mar. Fish. Comm.
No. 12, 80 p.
Terry J. Cody
Billy E. Fuls
Texas Parks and Wildlife Department
Coastal Fisheries Branch
4200 Smith School Road
Austin, TX 787U
Long Island to Chesapeake Bay, spawning occurs
in offshore coastal waters from October to Decem-
ber and from March to May. From North Carolina
to Florida, spawning occurs in offshore coastal
waters from October through March and this spawn-
ing population consists of fish that have migrated
from the north and contains all age groups (Nichol-
son 1978). The gulf menhaden, which is distributed
zonally, is restricted to the Gulf of Mexico and
ranges from Cape Sable, FL, to Vera Cruz, Mexico
(Reintjes 1969). Their maximum reported age is ap-
proximately 4 yr, and they may spawn for approx-
imately 2 yr (Lewis and Roithmayr 1981). They
spawn from October through March in nearshore
and offshore waters within the 110 m depth contour
(Christmas and Waller 1975). Both species use estu-
aries as nursery areas for more than half their first
year of life.
The major objectives of this study were to examine
and compare early life history characteristics of
these two menhadens and to investigate the effects
of temperature on developmental processes. Char-
acteristics examined were egg size, size at hatching,
yolk utilization rates, yolk volume at first feeding,
size and age at first feeding, and growth.
EARLY LIFE HISTORY OF ATLANTIC
MENHADEN, BREVOORTIA TYRANNUS, AND
GULF MENHADEN, B. PATRONUS
Atlantic menhaden, Brevoortia tyrannus, and gulf
menhaden, B. patronus, are allopatric, morphologi-
cally similar clupeids with contrasting distributional
patterns and reproductive traits. The Atlantic men-
haden has a meridional distribution and encounters
variable environmental conditions during its life-
time. It occurs along the eastern coast of North
America from Nova Scotia to Florida, and its dis-
tribution is stratified by age and size, with the older
and larger fish ranging farther north (Nicholson
1978). Atlantic menhaden are a relatively long-lived
clupeid. Their maximum reported age is approx-
imately 10 yr, and they may spawn for approximate-
ly 7 yr (Higham and Nicholson 1964; Nicholson
1975). The spatial and temporal spawning habits of
Atlantic menhaden are more complex than those of
its congener. In Long Island Sound and New Eng-
land waters, limited spawning occurs in inshore
waters during the summer and early fall. From
Methods
Atlantic menhaden were collected with a commer-
cial purse seine from the Newport River, NC, dur-
ing the summer. Fish were held in the laboratory
at ambient temperatures for approximately 4 mo
before spawning. Gulf menhaden were collected in
late September by cast net near Gulf Breeze, FL,
and transported to the laboratory by methods devel-
oped by Hettler (1983). They were held in the lab-
oratory at ambient temperatures for about 1 mo
before spawning. For each spawning, about 10 men-
haden were induced to spawn by methods described
by Hettler (1981, 1983). Eggs were spawned in
approximately 20 °C water during the night and col-
lected the following morning. All experiments ex-
cept those dealing specifically with growth were con-
ducted in 10 L rearing tanks; growth experiments
were conducted in 60 L rearing tanks. Tanks were
set in a temperature controlled water bath with two
40-W fluorescent lamps positioned 40 cm above each
tank, and the tanks were illuminated for 12 h daily.
Temperatures were controlled to approximately
±0.5°C. Salinities ranged from 28%>o to 32%o.
Rotifers, Brachionus plicatilis, were used as food
for about the first 10 d, and Artemia nauplii and
rotifers were used thereafter. Feeding levels were
not controlled, but, based on experience, we pro-
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
991
vided food in densities we felt would not limit
growth.
Growth in standard length (SL) from the time lar-
vae begin feeding to age 21 d at 20° C was modeled
by an exponential equation. All measurements were
made on eggs and larvae that were preserved in 5%
sodium acetate buffered Formalin1. Volumes (V) of
the elliptically shaped yolk mass were calculated
using the formula for a prolate spheroid
V = (n/6) lh2,
where I is the length and h is the height of the yolk
mass (Blaxter and Hempel 1963).
We were unable to treat the two species the same
in most experiments. The gulf menhaden was sub-
jected to a greater number of treatments than the
Atlantic menhaden. Experiments dealing with
starvation and yolk utilization rates were conducted
only on the gulf menhaden. In addition, the lack of
replications for some experiments limited the ap-
plication of statistical tests (e.g., ANOVA) and, as
a result the differences or similarities between the
two menhadens, should be considered tentative.
Results and Discussion
Based on a sample of eggs from the single spawn
of a group of approximately five females from each
species, Atlantic menhaden had significantly (P <
0.001) larger eggs (1.6 mm diameter, N = 20) than
gulf menhaden (1.3 mm diameter, N = 20). Egg
sizes for both these species that have been reported
(Houde and Fore 1973; Jones et al. 1978; Hettler
1984) support our observations that Atlantic men-
haden eggs are larger than gulf menhaden eggs.
Atlantic menhaden larvae measured at hatching also
were larger than gulf menhaden (Fig. 1) and sup-
ports Blaxter and Hunter's (1982) view that egg size
greatly influences the size of larvae at hatching.
Temperature did not affect the size at hatching
of gulf menhaden (Fig. 1), but the rate of yolk utiliza-
tion was affected by temperature and was roughly
2.5 times faster at the highest temperature (24 °C)
than at the lowest temperature (14°C) (Table 1). The
instantaneous rate of yolk utilization increased
linearly with increasing temperature (Fig. 2). The
volume of yolk at the onset of exogenous feeding
(first feeding) was approximately similar at all tem-
peratures (Table 1) and was not affected by temper-
ature (ANOVA, P = 0.13).
The size of gulf menhaden at first feeding was in-
dependent of temperature (Fig. 3) (ANOVA P =
0.15) and, although data are limited, the size of
Atlantic menhaden also was independent of tem-
perature. The age at first feeding, however, was
dependent on temperature (Fig. 3). An ANCOVA
(log transformed ages on temperature) revealed that
the regression slopes were similar (P = 0.37), in-
i-
<
E
E
O
z
ai
DW
s«
ZO
<Z
UjX
• Atlantic Menhaden
oQulf Menhaden
4.0
X
I
3.0
o n
- 1
■
5
i
5 s n
i i i I
14 16 18 20 22 24
TEMPERATURE °C
'Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
Figure 1.— The size at hatching of Atlantic gulf menhadens at dif-
ferent temperatures. Each point represents the mean of 10 fish.
Table 1 .—The effects of temperature on yolk utilization of gulf menhaden. For regression equations,
Y = loge preserved yolk volume (mm3) and X = age (d). The equations were derived from the means
of approximately 10 fish per sample. S is the number of samples; N is the number of larvae.
Mean volume of
Mean volume of
Tempera-
S
yolk at hatching
yolk at first
ture (°C)
No.
Regression
equation
rd
(mm3)
N
feeding (mm3)
N
14
15
V = -1.189
- 0.96446(x)
0.93
0.130482
10
0.000340
20
16
0.133397
10
0.000335
10
18
5
Y = -0.803
- 1.67066(x)
0.98
0.000211
10
20
10
V = - 1 .375
- 1.61365(x)
0.91
0.169317
10
0.000549
20
22
7
Y = - 1 .447
- 2.04386(x)
0.96
0.110202
10
0.000506
20
24
8
y = -1.509
- 2.22355(x)
0.95
0.123148
10
0.000289
19
992
o
>- ~
2
2
HI
<
CO
3
o
UJ
z
<
z
o
I-
<
N
< H
I- z>
CO
z
3.00
2.50
2.00
1.50
1.00-
C 0.50 -
0.00-
Gulf Menhaden
Y= 0.736+0. 12426(X)
ra = 0.95
_L
14 16 18 20 22 24
TEMPERATURE °C
Figure 2.— The effects of temperature on the instantaneous
rate of yolk utilization for gulf menhaden.
dicating a similar response to temperature by both
species. But the Y-intercepts differed significantly
(P = 0.02) indicating that, over the range of tem-
peratures tested, the Atlantic menhaden fed at a
significantly earlier age than gulf menhaden. For
both species the age at first feeding declined ex-
ponentially with increasing temperatures. Atlantic
menhaden were larger than the gulf menhaden at
first feeding (Fig. 3). At 20° C, Atlantic and gulf
menhaden growth rates were similar (ANCOVA, P
= 0.36), but Atlantic menhaden maintained a size
advantage during the early larval period (Table 2).
This difference was attributed to differential size
and age at first feeding.
The ability of early larvae to withstand the depri-
vation of food was influenced by temperature (Table
3). Although at 20 °C mortalities may be attributed
to causes other than starvation (compare control and
starved), at progressively higher temperatures lar-
vae are less able to withstand the deprivation of
food. For example, at 24°C, gulf menhaden must
find food within three days after the onset of first
E
E
I
I-
CD
O
Z
z
III
Q
1
HI
Q
DC
<
HI
1-
rn
UJ
CO
CM
z
rr
+i
<
LL
1-
H
co
<
z
<
Lit
2
o
z
CO
Q
>»
UJ
«
UJ
n
Ll_
*w
h-
UJ
fO
O
rr
<
LL
1-
<
5.5-
5.0-
4.5-
4.0
8
6
4
2
{Atlantic Menhaden
-
o Gulf Menhaden
-
t
- {
1
{
a
•
i
i
6
X
1
{
1
• Atlantic Menhaden
o Gulf Menhaden
/
Y=30.7e-°-11454
r2=0.99
_l L
Y=25.1e
/ r2 = 0.96
-0.0929(X)
14 16
18
20 22
24
TEMPERATURE °C
Figure 3.— The size and age when gulf and Atlantic menhadens begin feeding on exogenous food sources
at different temperatures. Each point represents a sample of about 10 fish. Replicate experiments were
only conducted for gulf menhaden and only at 14°, 20°, 22°, and 24°C.
993
Table 2.— Growth of larval gulf and Atlantic menhadens from time
of first feeding to age 21 d at 20°C.
W1
Growth parameters2
a b
r2
Estimated SL
(mm)
Species
First Age
feeding 21 d
Gulf
menhaden
Atlantic
menhaden
11
16
3.36
4.38
0.04640
0.04267
0.97
0.95
4.0 8.9
5.0 10.7
'Number of samples; about 10 fish per sample.
2SL (mm) = a x exp b (age in d).
tuating environment producing more reproductive
uncertainty (Murphy 1968; Stearns 1976). This in-
formation suggests to us that the subtle differences
we observed may indicate a fine tuning of reproduc-
tive strategies that allow these menhadens to per-
sist in their particular environments. A more rigor-
ous comparative study is required before we can
understand how menhaden life history character-
istics are adapted to their particular environments.
Such a study is presently underway by the senior
author.
Table 3.— The survival (%) of first-feeding gulf menhaden larvae
deprived of food (starved) in relation to temperature. The fed treat-
ment represents the control group.
Temper-
ature
(°C)
Treatment
N
Days past time of first feeding
1
2
3
4
5
6 7
18
Starved
25
100
100
100
100
92
32 0
Fed
25
100
100
100
100
96
92 92
20
Starved
25
92
76
72
48
8
4 0
Fed
25
88
84
84
84
72
68 68
22
Starved
20
100
100
80
75
0
Fed
20
100
100
100
100
100
24
Starved
25
56
40
40
4
0
Fed
25
96
96
96
96
96
feeding or high mortalities will occur; whereas at
18 °C they can survive without food for 5 d without
incurring high mortalities (Table 3). The gulf men-
haden's response to starvation in relation to tem-
perature is comparable to numerous temperate zone,
pelagic fish larvae (McGurk 1984).
In conclusion, although temperature is an impor-
tant factor in controlling the development of marine
fish larvae (Blaxter 1970), we observe that temper-
ature was not a determinant of size at hatching, size
at first feeding, and yolk volume remaining at first
feeding. These data suggest that age is not a good
correlate of these developmental events. On the
other hand, temperature had an effect on the rate
of yolk utilization, the time between hatching and
exogenous feeding, and the ability of larvae to with-
stand the deprivation of food.
Our observations, although limited by a lack of
rigorous statistical testing, suggest that, relative to
gulf menhaden, Atlantic menhaden produced larger
eggs, were larger at hatching, were larger and
younger at time of first feeding, and appeared to
maintain a larger size throughout the early larval
period. We tried to interpret these differences in the
context of their entire life history. Relative to gulf
menhaden, Atlantic menhaden exhibit life history
traits (later maturity, longer life, and more repro-
ductive years) that may be adapted to a more flue-
Acknowledgments
Sincere appreciation is extended to J. Govoni, D.
Peters, and two anonymous reviewers for their
critical review of the manuscript. W. Hettler and
C. Lewis provided technical support during various
phases of the study. This research was supported
by a contract from the Ocean Assessments Division,
National Ocean Service, National Oceanic and At-
mospheric Administration.
Literature Cited
Blaxter, J. H. S.
1970. Development: eggs and larvae. In W. S. Hoar and D.
J. Randall (editors), Fish physiology, Vol. 3, p. 178-252.
Acad. Press, Inc. N.Y.
Blaxter, J. H. S., and G. Hempel.
1963. The influence of egg size on herring larvae (Clupea
harengus L.). J. Cons., Cons. Int. Explor. Mer 28:211-240.
Blaxter, J. H. S., and J. R. Hunter.
1982. The biology of clupeoid fishes. Adv. Mar. Biol. 20:
1-223.
Christmas, J. Y., and R. S. Waller.
1975. Location and time of menhaden spawning in the Gulf
of Mexico. Gulf Coast Res. Lab., Ocean Springs, MS, 20 p.
Hettler, W. F.
1981. Spawning and rearing Atlantic menhaden. Prog. Fish-
Cult. 43:80-84.
1983. Transporting adult and larval gulf menhaden and tech-
niques for spawning in the laboratory. Prog. Fish-Cult.
45:45-48.
1984. Description of eggs, larvae, and early juveniles of gulf
menhaden, Brevoortia patronus, and comparisons with
Atlantic menhaden, B. tyrannus, and yellowfin menhaden,
B. smithi. Fish. Bull., U.S. 82:85-95.
HlGHAM, J. R., AND W. R. NICHOLSON.
1964. Sexual maturation and spawning of Atlantic menhaden.
U.S. Fish Wildl. Serv., Fish. Bull. 63:255-271.
Houde, E. D., and P. L. Fore.
1973. Guide to the identity of eggs and larvae of some Gulf
of Mexico clupeid fishes. Fla. Dep. Nat. Resour., Mar. Res.
Lab., Leafl. Ser. 4(23):1-14.
Jones, P. W., F. D. Martin, and J. D. Hardy, Jr.
1978. Development of fishes of the Mid- Atlantic Bight. Vol.
1, Acipensaridae through Ictaluridae. U.S. Fish. Wildl.
Serv., Biol. Serv. Program FWS/OBS-78/12, 314 p.
994
Lewis, R. M., and C. M. Roithmayr.
1981. Spawning and sexual maturity of gulf menhaden,
Brevoortia patronus. Fish. Bull., U.S. 78:947-951.
McGurk, W. D.
1984. Effects of delayed feeding and temperature on the age
of irreversible starvation and on the rates of growth and
mortality of Pacific herring larvae. Mar. Biol. 84:13-26.
Murphy, G. I.
1968. Pattern in life history and the environment. Am. Nat.
102:391-403.
Nicholson, W. R.
1975. Age and size composition of the Atlantic menhaden,
Brevoortia tyrannus, purse seine catch, 1963-71, with a brief
discussion of the fishery. U.S. Dep. Commer., NOAA Tech.
Rep. NMFS SSRF-684, 28 p.
1978. Movements and population structure of Atlantic men-
haden indicated by tag returns. Estuaries 1:141-150.
Reintjes, J.
1969. Synopsis of biological data on the Atlantic menhaden,
Brevoortia tyrannus. U.S. Fish Wildl. Serv., Circ. 320, 30
P-
Stearns, S. C.
1976. Life-history tactics: a review of the ideas. Q. Rev. Biol.
51:3-47.
Allyn B. Powell
Southeast Fisheries Center Beaufort Laboratory
National Marine Fisheries Service, NOAA
Beaufort, NC 28516 USA
Germano Phonlor
Fundacao Universidade do Rio Grande
Departamento de Oceanografia
Caixa postal k7k
96200 Rio Grande - RS, BRAZIL
SEASONALITY OF BLUE MUSSEL,
MYTILUS EDULIS L., LARVAE IN
THE DAMARISCOTTA RIVER ESTUARY,
MAINE, 1969-771
(Engle and Loosanoff 1944; Stubbings 1954; Baird
1966; Bohle 1971; Rasmussen 1973; Jorgensen 1981;
Kautsky 1982).
Seed (1975) summarized reproduction in Euro-
pean mussel populations and found that spawning
in M. edulis varies with latitude, occurring earlier
in warm waters and progressively later in cooler,
northern waters. However, Newell et al. (1982)
reported no latitudinal variation of spawning among
mussel populations along the northwestern Atlan-
tic coast. Such geographic variation has been attrib-
uted to the existence of physiological races (Stauber
1950; Loosanoff and Nomejko 1951). Newell et al.
(1982) and Fell and Belsamo (1985) also found that
mussel populations at the same latitude in Long
Island Sound spawn at different temperatures and
times of the year. They surmised that food avail-
ability, rather than temperature, dictates when
spawning occurs.
Factors which are important in the timing and
intensity of spawning can be determined by moni-
toring spawning activity. This may be achieved
directly, by examination of gonad development in
seasonally collected samples, or indirectly, by ob-
serving the presence or absence of M. edulis larvae
in plankton samples (Chipperfield 1953). While the
direct method is preferable, the indirect method
does allow one to use long-term plankton records.
These provide an estimate of the variation in both
the timing and intensity of spawning. Since the
source of the larvae is not certain, some caution
should be used in the interpretation of the results
(Seed 1975).
An 8-yr plankton record of Mytilus larval abun-
dance presents an unusual opportunity to observe
long-term variability in spawning and larval occur-
rence. Specifically, the data were examined with the
following goals:
The spawning of the blue mussel, Mytilus edulis L.,
has been the subject of many studies (see Bayne
1976 for partial review). In an early paper Field
(1922) reported that gametogenesis and spawning
were influenced by water temperature, though he
provided no data. Chipperfield (1953) found that
mussels spawn over a specific range of water tem-
perature (9.5°-12.5°C). In addition, Chipperfield
noted that the rate of temperature change prior to
spawning influences intensity. Other investigators
have found that mussels spawn over a specific tem-
perature range, which may vary among locales
Contribution No. 183, Ira C. Darling Center, University of
Maine, Orono, ME.
1) Determination of the initiation and the dura-
tion of the spawning season and degree of tem-
poral variation between years;
2) Determination of the variation in larval abun-
dances within and between seasons;
3) Examination of the possible correlation of en-
vironmental variables (temperature, phyto-
plankton abundance, degree days, calendar
date, and lunar cycles) with spawning activity.
Materials and Methods
The study site was the Damariscotta River estuary
(Fig. 1), a narrow embayment, 29 km long, which
receives a limited amount of freshwater. The estu-
FISHERY BULLETIN: VOL. 84, NO. 4, 1986.
995
arine portion has a MLW (mean low water) volume
of 123.4 x 106 m3, a tidal volume of 56.2 x 106 m3,
and a mean summer flushing time of 4-5 wk
DAMARISCOTTA
DAMARISCOTTA RIVER
LOCATION MAP
1 ,5 0 1
NAUTICAL MILES
1 .5 0 1 2
KILOMETERS
- 44" 00'
- 43* 55'
43* 50'
(McAlice 1977). The estuary is stratified near its
head but approaches a well-mixed condition further
seaward. Tides are semi-diurnal with a mean range
of 2.7 m and a tidal excursion of about 2.8 km (Lee
and McAlice 1979).
Monthly plankton samples were collected during
daylight at station D7 (Fig. 1) from October 1969
to June 1970 and then biweekly until September
1977. Plankton tows were 10-15 min oblique hauls
with #20 mesh (76 /im) nets of 0.5 m mouth diam-
eter equipped with centrally mounted flowmeters.
Maximum depths of tows were 10-15 m (4-5 m above
the bottom). Boat speed was 1-2 m s-1. Samples
were immediately fixed in 4% buffered Formalin2.
Laboratory subsampling followed the method
recommended by Frolander (1968). The concen-
trated plankton was diluted to a known volume,
thoroughly stirred, and a 1 mL aliquot removed with
a Stempel pipette. Initial counts on samples taken
from June 1974 to September 1977 did not distin-
guish among taxa of larval bivalves. We therefore
took an additional subsample, determined the per-
centage of Mytilus in 50 bivalve larvae, and multi-
plied this by the total veliger abundance to obtain
Mytilus densities for each sampling period.
Several key publications (Loosanoff et al. 1966;
Chanley and Andrews 1971; DeScweinitz and Lutz
1976; Lutz and Hidu 1979) containing photomicro-
graphs and descriptions were used to identify
Mytilus edulis larvae. The differentiation of Mytilus
edulis larvae from other mytilid larvae (Modiolus
modiolus and Geukensia demissa) at the straight
hinge stage was achieved by comparing the length
of the hinge line as well as total shell length and
height. The early and late umbo larvae of Geuken-
sia were easily distinguishable by their elongated
appearance; Mytilus larvae tended to be less
elongate, though pointed anteriorly (Chanley and
Andrews 1971). The differentiation of Modiolus
modiolus larvae and Mytilus edulis larvae was based
mainly on the characteristics described by
DeSchweinitz and Lutz (1976); hinge line lengths,
total shell length in the 95-105 ycm range, shell shape
of umbo stage larvae, presence of an eye spot in
specimens <270 yxn, and the presence of a functional
foot in larvae <295 \xm. Further positive identifica-
tion of late stage Mytilus larvae was achieved by
examining the hinge teeth of disarticulated valves
(Lutz and Hidu 1979).
Spawning dates were estimated by subtracting the
approximate age of the larvae from the sampling
69' 35'
69'30'
Figure 1.— Location map.
2Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.
996
date. Larval age was estimated using photomicro-
graphs of larvae of known age and size for com-
parison, available in Chanley and Andrews (1971).
The initial occurrence of larvae in each year was
dominated by early straight hinge larvae. The
spawning season was defined by larval abundances
>10 m~3. This level was chosen arbitrarily to
distinguish major spawning from occasional low lar-
val abundances (<10 m~3).
Environmental variables that were examined for
correlations with the initiation of spawning and lar-
val abundance included water temperature, phyto-
plankton abundance, degree days, calendar date,
and lunar cycles. Water temperatures were taken
concurrently with the plankton samples. Phyto-
plankton abundances from July 1974 to August 1977
were available for the Damariscotta River (McAlice
unpubl. data). Data from the neighboring Sheepscot
River estuary (McAlice and Denniston3) were sub-
stituted for the period October 1969 to June 1974.
The decision to use the Sheepscot data was based
on the highly significant Spearman's rank correla-
tion (Zar 1984) (r = 0.67, P < 0.001) between the
Damariscotta and Sheepscot phytoplankton abun-
dances from July 1974 to August 1977. Degree days
were calculated in the manner described by Thiesen
(1973). For each year, degree days were summed
from the time of peak larval abundance the previous
year to the initiation of spawning. Lunar cycle in-
formation was obtained from tide tables published
by NOAA (1969-76).
once initiated, probably continued throughout the
summer as indicated by the persistence of early
stage mussel larvae. Spawning appeared to cease
as temperatures fell to 9° -14° C in September and
October (Fig. 2), when only late stage larvae were
present. Maximal larval abundances were observed
in mid- to late June, shortly after spawning began.
At this time, straight hinge larvae, <6 d old, were
dominant. Maximum values for the period 1970-75
ranged from 787 larvae m~3 to 5,400 larvae m~3.
In 1976 and 1977, maximum abundances were an
order of magnitude larger (3.16 x 104 m~3 and
6.09 x 104 m-3, respectively). Following the peaks
in June, larval densities generally declined through
1 to 3 successively smaller peaks (Fig. 2).
Mussel larvae appeared well after phytoplankton
abundances had begun to increase from low winter
values to generally high summer values (Fig. 3). Lar-
vae usually disappeared before phytoplankton abun-
dances fell to typically low winter levels.
In addition to the larvae of Mytilus edulis, those
of Anomia simplex, Geukensia demissa, Modiolus
modiolus, and what was probably a complex of My a
arenaria, Hiatella arctica, and possibly Sphenia
sincera (Hanks and Packer 1985) larvae were also
identified. Amonia simplex occurred most commonly
from September through December, though never
in great numbers. The Mya-Hiatella-Sphenia group
was often very abundant, and occurred from early
May through September. Geukensia and Modiolus
were never common.
Results
Examination of the age and abundance of mussel
larvae from December 1969 to September 1977 in-
dicated that spawning began in late May or early
June when temperatures reached 10° -12.5°C (Fig.
2). The average date when spawning began was 4
June, with a standard deviation of approximately
7 d. The average number of degree days prior to
spawning was 2,853, with a standard deviation of
368. No significant relationship was found between
degree days and commencement of spawning or
degree days and maximum larval abundances.
Commencement of spawning may be related to the
time of spring tides (Table 1). In 7 of the 8 yr ex-
amined, spawning began within 5 d, before and
after, a spring tide. On four occasions spawning
commenced within 2 d of a spring tide. Spawning,
3McAlice, B. J., and F. D. Denniston. Dominance and diversity
of Sheepscot River estuary phytoplankton. Manuscr. in prep.
Ira C. Darling Center, University of Maine, Walpole, ME
04573.
Table 1 .—Estimated dates and temperatures of the initiation and
cessation of spawning for Mytilus edulis in the Damariscotta River
estuary, and dates of nearest spring tides, 1970-77.
Date of
Estimated date and (°C) when spawning „„,„,
spring
Year
began
ended tide
1970
2 June (10.0°-13.2°C) 2 Oct.
(14.6°-13.9°C) June 4
1971
8 June (10.2°-12.2°C) 18 Oct.
(14.3°-12.8°C) June 9
1972
16 June (10.5°-12.1°C) 20 Oct.
(13.1°-9.0°C) June 11
1973
12 June (10.0°-14.0°C) 10 Oct.
(12.7°-11.0°C) June 15
1974
12 June (10.7°-12.3°C) 8 Oct.
(12.4°-9.1°C) June 4
1975
27 May (10.3°-12.5°C) 24 Sept.
(16.9°-13.7°C) May 25
1976
24 May (10.1°-12.8°C) 22 Oct.
(14.6°-11.0°C) May 29
1977
2 June (9.3°-10.2°C)
— June 1
Discussion
A temperature threshold for spawning was in-
dicated by the appearance of Mytilus larvae when
water temperatures exceeded 10°-12.5°C and the
subsequent disappearance of larvae when tempera-
tures fell below 9° -14°C. A number of studies have
reported the initiation of spawning in Mytilus edulis
997
IO
1970
iij
o
z
<
a
z
O
<
B
4.0-
3.0-
2.0-
<
>
<
o
IO~
0.0-
J' • '0' ' |j" 'A1 ' 'j1 ■ b1 ' |J ' 'a1 ' 'J1 ' 'o1 ' p" 'a' ' 'j
1974
1975
1976
1977
Figure 2.— Abundance ofMytilus edulis larvae (solid line) and water temperature (broken line) at station D7: A)
1969-73; B) 1974-77.
at temperatures of 10°-13°C or higher while few
studies have reported spawning at lower tempera-
tures (Table 2), which also suggests a thermal
threshold for spawning. The significance of this
threshold may be linked to gametogenesis. Bayne
(1965) found that mussels with fully developed
gametes would not spawn when held at 5°C under
high food concentrations. However, if temperatures
were raised to 12°-14°C, gametes matured and
spawning ensued. Similarly, Sastry (1968) found
that in the bay scallop, Aequipecten irradians,
oogonia and spermatozoa formed at 15 °C and 20 °C,
but that temperatures higher than 20 °C were
necessary for oocytes to reach a fertilizable stage.
Therefore, the apparent correlation between a par-
ticular temperature and the initiation of spawning
may actually reflect the maturation of gametes
followed by induction of spawning by any of a num-
ber of stimuli. Given the predictable rise in temper-
ature each spring, this may explain the initiation of
spawning at approximately the same time each year.
Use of degree days to predict the time of spawn-
ing does not appear to be useful. This is due to a
very regular pattern of rising and falling water
temperatures each year. As a result, the sum of
degree days between spawning periods conveyed no
more information than did elapsed time. Newell et
al. (1982) arrived at a similar conclusion for mussel
populations in Long Island Sound. They found that
one Long Island Sound mussel population spawned
3 mo later than another, despite nearly identical
temperature conditions, difference in degree days
due solely to a difference in elapsed calendar days.
Bayne (1975), however, did find a relationship be-
tween rate of gametogenesis and degree days, but
not calendar days.
998
UJ
6.0-
w
UJ
o
o
5.0-
4.0-
3.0
[J ' 'A1 ' 7 ' 'o' ' P ' 'A' ' 'J1 ' 'o' ' |J' ' 'A1 ' 'j' ' '01 ' |J' ' 'A1 ' 'J1 ' 01 '
1970 1971 1972 1973
3.0 |0i i ,Ai i .j. , lQl i jji i iai i iji i i0. i |ji i iai i iji i b. . jji" i 'iai i iji i
1974 1975 1976 1977
Figure 3.— Abundance of phytoplankton in the lower Sheepscot River estuary: A) 1969-73; B) January
1974-June 1974 and at station D7, July 1974-August 1977.
Table 2.— Reported spawning temperatures and periods of Mytilus edulis.
Tempera-
tures
Major spawning
Location
(°C)
period
Reference
Europe
Norway
8
early May
Bohle 1971
Denmark
7-16
May
Jorgensen 1981
England
9.5-12.5
May
Chipperfield 1953
Sweden
12
mid-May-early June
Kautsky 1982
England
13
early May
Baird 1966
Denmark
13-14
May-June
Rasmussen 1973
United States
Damariscotta
10-13
late May-mid-June
This study
River, ME
Milford, CT
15-16
May
Engle and
Loosanoff 1944
Branford, CT
14-16
late May-early June
Fell and Balsimo 1985
Stony Brook, NY
11-15
late April-early June
Newell et al. 1982
Shinnecock, NY
16-22
August-October
Newell et al. 1982
Spawning in response to lunar cycles is also a
possibility. Korringa (1947) noted that the European
oyster, Ostrea edulis, spawns around the period of
spring tides and attributed this to increased hydro-
static pressure. Chipperfield (1953) also observed 0.
edulis at several sites in Great Britain shortly after
999
the occurrence of a spring tide. In our study, spawn-
ing began around the time of spring tides, but in-
duction of spawning by hydrostatic pressure has not
been reported in mussels. Alternatively, spawning
may be induced by other factors associated with
spring tides, such as increased temperature fluctua-
tions, air exposure, and water movement. Temper-
ature fluctuations have been shown to induce labor-
atory spawning in Mytilus edulis (Bayne 1976).
While a temperature threshold is suggested, time
of year may also be important as indicated by the
spawning periods in Table 2. Of the 10 studies ex-
amined, all but one reported the initiation of spawn-
ing from May to June. Aside from temperature, the
initiation of spawning may be influenced by another
cyclic phenomena such as photoperiod. Light and
photoperiod in particular have been shown to affect
the timing of reproduction in a number of marine
invertebrates (Segal 1970). While adult mussels are
sensitive to changes in light intensity (Bayne et al.
1976), the ability to detect changing photoperiod has
not been demonstrated. The results of this study
have been attributed to annual temperature cycles,
but until light response of mussels is more fully ex-
amined photoperiod cannot be ruled out.
Variations in larval abundance from year to year
do not appear to be linked to temperature, nor to
availability of food energy. Kautsky (1982) reported
that Baltic Sea mussel populations were limited to
one major spawning by reduced food availability dur-
ing the remainder of the year. Similarly, Thompson
(1979) attributed annual variation in reproductive
condition and fecundity of mussels along the coast
of Nova Scotia to annual variations in food supply.
Bayne (1975) noted that while poor nutrition does
not significantly alter the timing of gametogenesis,
it can result in resorption of gametes prior to spawn-
ing. Newell et al. (1982) suggested that the cycle of
food availability could affect both the nutrient
storage cycle and the timing of gametogenic events,
including spawning. In every year of our study the
spring augmentation of phytoplankton was well
under way by March or April, with densities >105
cells 1_1. Significant numbers of mussel larvae
were first detected between late May and early
June. Thus, it appears that food is not limiting to
either adult or larval mussel populations in our area.
Our phytoplankton data, however, do not include the
smaller naked nanoplankton which, together with
particulate organic matter, could account for more
than half of the available energy in the Damariscotta
River (Incze 1979). This fraction would be a better
index of food available to mussel larvae and should
be included in studies attempting to link abundance
or setting success of larvae to their food supply.
Onset of spawning in Damariscotta River mussel
populations is predictable from year to year. It oc-
curs when water temperature exceeds 10°-12.5°C,
and near the spring tide portion of the neap-spring
cycle. Food does not appear to be limiting to either
gametogenesis or the development of larvae.
Acknowledgments
We thank H. Hidu for stimulating discussions and
for criticizing an earlier draft of the manuscript. E.
S. Gardella and A. L. Heinig contributed greatly to
the sampling efforts. Greg Podniesinski was sup-
ported by UMO-UNH Sea Grant R/FD-99 awarded
to H. Hidu.
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Gulf of Maine. Veliger 27:320-330.
Incze, L. S.
1979. Relationships between environmental temperatures,
seston, and the growth and survival of Mytilus edulis, L.
in a north temperate estuary. M.S. Thesis, Univ. Maine,
Orono.
Jorgenson, C. B.
1981. Mortality, growth and grazing impact of a cohort of
bivalve larvae, Mytilus edulis. (L.). Ophelia 20:185-192.
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1982. Quantitative studies on gonad cycle, fecundity, repro-
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1947. Relations between the moon and periodicity in the
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Lee, W. Y., and B. J. McAlice.
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Loosanoff, V. L., H. C. Davis, and P. E. Chanley.
1966. Dimensions and shapes of larvae of some marine
bivalve mollusks. Malacologia 4:351-435.
Loosanoff, V. L., and C. A. Nomejko.
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Crassostrea virginica. Biol. Bull. (Woods Hole) 101:151-
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Lutz, R. A., and H. HlDU.
1979. Hinge morphogenesis in the shells of larval and early
post-larval mussels (Mytilus edulis and Modiolus modiolus
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1977. A preliminary oceanographic survey of the Damari-
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1982. Temporal variation in the reproductive cycle of Mytilus
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1969-1976. Tide Tables: East Coast of North and South
America, including Greenland. Tide Tables Natl. Ocean
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Rasmussen, E.
1973. Systematics and ecology of the Isefjord marine fauna
(Denmark) with a survey of the eelgrass (Zostera) vegeta-
tion and its communities. Ophelia 11:1-495.
Sastry, A. N.
1968. The relationships among food, temperature and gonad
development of the bay scallop, Aequipecten irradians
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1975. Reproduction in Mytilus (Mollusca-.Bivalvia) in Euro-
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1970. Light, animals, invertebrates. In O. Kinne (editor),
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1950. The problem of physiological species with special
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1954. The biology of the common mussel in relation to foul-
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Thompson, R. J.
1979. Fecundity and reproductive effort in the blue mussel
(Mytilus edulis), the sea urchin (Stronglyocentrotus droe-
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Board Can. 36:955-964.
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Greg S. Podniesinski
Department of Zoology
University of Maine, Orono, ME
Mailing address:
Ira C. Darling Center
University of Maine
Walpole, ME 04573
Bernard J. McAlice
Department of Botany and Plant Pathology
University of Maine
Orono, ME 04573
1001
INDEX
Fishery Bulletin Vol. 84, No. 1-4
"The abundance and distribution of the family Macrouridae
(Pisces: Gadiformes) in the Norfolk Canyon area," by
Robert W. Middleton and John A. Musick 35
"Abundance, size, and sex ratio of adult sea-run sea lam-
preys, Petromyzon marinus, in the Connecticut River," by
Kathleen Stier and Boyd Kynard 476
"Age and growth of the marine catfish, Netuma barba
(Siluriformes, Ariidae), in the estuary of the Patos Lagoon
(Brasil)," by Enir Girondi Reis 679
"Age dependent fecundity, number of spawnings per year,
sex ratio, and maturation stages in northern anchovy,
Engraulis mordax," by Richard H. Parrish, Donna L.
Mallicoate, and Richard A. Klingbeil 503
Aging studies
larval fish 91
sailfish, Atlantic 493
AHRENHOLZ, DEAN W.-see NELSON and
AHRENHOLZ
Albacore
chromosomal analysis 469
Ammodytes americanus—see Eel, sand
Ammodytes hexapterus—see Sand lance
Ampelisca agassizi—see Amphipods, gammaridean
Amphipods, benthic
parasites of 204, 605
"Anatomical trauma to sponge-coral reef fishes captured
by trawling and angling," by S. Gordon Rogers, Hiram T.
Langston, and Timothy E. Targett 697
Anchovy, northern
fecundity and spawning 503
drift in the California Current 585
life-stage-specific instantaneous mortality rates 395
spawning in San Francisco Bay 879
vulnerability to predation 859
"An approach to yield assessment for unexploited
resources with application to the deep slope fishes of the
Marianas," by Jeffrey J. Polovina and Stephen Ralston . . 759
Anglerfish, lophiid
early development 429
Angling
trauma to sponge-coral reef fishes 697
Anguilla rostrata—see Eel, American
"Annual production of eviscerated body weight, fat, and
gonads of Pacific herring, Clupea harengus pallasi, near
Auke Bay, southeastern Alaska," by Jay C. Quast .... 705
Anoplopoma fimbria— see Sablefish
Anthozoans
ecology of Ceriantharia from Cape Hatteras to Nova
Scotia 625
Arctica islandica—see Quahog, ocean
"Arrival of northern fur seals, Callorhinus ursinus, on St.
Paul Island, Alaska," by Michael A. Bigg 383
Ascarophis sp.
parasites in American lobster 197
"Aspects of the reproductive biology, spatial distribution,
growth, and mortality of the deepwater caridean shrimp,
Heterocarpus laevigatus, in Hawaii," by Murray D. Dailey
and Stephen Ralston 915
Atheresthes evermanni—see Flounder, Kamchatka
Atheresthes stomias—see Flounder, arrowtooth
ATKINSON, C. ALLEN, "Discrete-time difference model
for simulating interacting fish population dynamics" . . . 535
Backdown
dolphin-releasing procedure 27
Balaenoptera edeni—see Whale, Bryde
Balaenoptera physalus—see Whale, finback
BALTZ, DONALD M.-see MOYLE et al.
BARBER, RICHARD T.-see FORWARD et al.
BARLOW, J.-see MYRICK et al.
-see REILLY and BARLOW
Bass, black sea
anatomical trauma from angling 697
contributions to life history 723
Bass, striped
feeding below a hydroelectric dam 220
survival and growth 905
BAYER, RANGE D., "Seabirds near an Oregon estuarine
salmon hatchery in 1982 and during the 1983 El Nino" . . 279
BEACHAM, TERRY D., "Type, quantity, and size of food
of Pacific salmon (Oncorhynchus) in the Strait of Juan de
Fuca, British Columbia" 77
1003
BIANCHINI, MARCO L.-see SORENSEN et al.
BIGG, MICHAEL A., "Arrival of northern fur seals,
Callorhinus ursinus, on St. Paul Island, Alaska" 383
BIGG, MICHAEL A.-see PEREZ and BIGG
BODKIN, JAMES LEE, "Fish assemblages in Macrocystis
and Nereocystis kelp forests off central California" .... 799
BOEHM, PAUL D.-see STEIMLE et al.
BONNELL, MICHAEL L.-see DOHL et al.
Boston
Ex-vessel price in New England fishing industry .... 437
BOTSFORD, LOUIS W.-see SYKES and BOTSFORD
Bottomfish
affect of hypoxia on abundance and distribution 19
Brevoortia patronus—see Menhaden, gulf
Brevoortia tyrannus—see Menhaden, Atlantic
Briarosaccus callosus—see Rhizocephalan
BRUNO, RALPH A.-see STEIMLE et al.
BRUSHER, HAROLD A.-see FINUCANE et al.
BURCH, RAYMOND, K.-see UCHIYAMA et al.
Calanus pacificus
abundance, chemical composition, distribution, and
size 157
California Current 157
California Cooperative Oceanic Fisheries Investigation
northern anchovy drift studies 587
California Current
Calanus pacificus 157
northern anchovy 585
Callorhinus ursinus— see Seal, northern fur
CAREY, ANDREW G, JR.-see TESTER and CAREY
"Cartilage and bone development in scombroid fishes," by
Thomas Potthoff, Sharon Kelley, and Joaquin C. Javech . . 647
Catfish, sea
age and growth in Patos Lagoon, Brasil 679
Centrapristis striata— see Bass, black sea
Ceriantharia— see Anthozoans
"Cetacean high-use habitats of the northeast United States
continental shelf," by Robert D. Kenney and Howard E.
Winn 345
Cetaceans
high-use habitats 345
1004
sighted by CETAP aerial and POP surveys 349
CETAP
aerial surveys 345
"Chinook salmon, Oncorhynchus tshawytscha, spawn-
ing escapement based on multiple mark-recapture of
carcasses," by Stephen D. Sykes and Louis W. Bots-
ford 261
Chionoecetes tanneri—see Crab, spider
Chlorophyll
sea surface concentration in the tropical Pacific 687
"Chromosomal analysis of albacore, Thunnus alalunga,
and yellowfin, Thunnus albacares, and skipjack, Kat-
suwonus pelamis, tuna," by F. J. Ratty, Y. C. Song, and
R. M. Laurs 469
Ciliates
parasites of benthic amphipods 204
Clam, soft shell
description of poecilostomatoid copepods 227
occurrence of epizootic sarcoma in Chesapeake Bay . . 851
Clupea harengus pallasi—see Herring, Pacific
Cod
ex-vessel price in New England fishing industry .... 437
CODY, TERRY J., and BILLY E. FULS, "Comparison of
catches in 4.3 m and 12.2 m shrimp trawls in the Gulf of
Mexico" 981
Coelorinchus c. carminatus
abundance and distribution in Norfolk Canyon 37
COLLETTE, BRUCE B., "Resilience of the fish assem-
blage in New England tidepools" 200
COLLINS, L. ALAN-see FINUCANE et al.
"Community studies in seagrass meadows: A comparison
of two methods for sampling macroinvertebrates and
fishes," by Kenneth M. Leber and Holly S. Greening . . 443
"Comparison of catches in 4.3 m and 12.2 m shrimp trawls
in the Gulf of Mexico," by Terry J. Cody and Billy E.
Fuls 981
"Comparison of visceral fat and gonadal fat volumes of
yellowtail rockfish, Sebastesflavidus, during a normal year
and a year of El Nino conditions," by William H. Lenarz
and Tina Wyllie Echeverria 743
Connecticut River
spawning migration of sea lampreys 749
"Contributions to the life history of black sea bass, Cen-
tropristis striata, off the southeastern United States," by
Charles A. Wenner, William A. Roumillat, and C. Wayne
Waltz 723
COOPER, RICHARD A.-see SHEPARD et al.
"Copepodids and adults of Leptinogaster major (Williams,
1907), a poecilostomatoid copepod living in Mya arenaria
L. and other marine bivalve mollusks," by Arthur G.
Humes 227
Copepods
size and chemical composition 165
Copepods, poecilostomatoid
Leptinogaster major living in mollusks 227
taxonomic history 227
Coryphaena equiselis—see Dolphin, pompano
Coryphaena hippurus—see Dolphin (fish)
Coryphaenoides armatus
abundance and distribution in Norfolk Canyon 51
Coryphaenoides carapinus
abundance and distribution in Norfolk Canyon 51
Coryphaenoides rupestris
abundance and distribution in Norfolk Canyon 48
COX, JAMES L.-see WILLASON et al.
Crab, blue king
Rhizocephalan infection 177
Crab, golden king
distribution and reproductive biology in eastern Bering
Sea 571
Crab, king
comparison of blue and golden king crabs 327
Crab, spider
instar identification 973
life history 973
Culture studies
squid, market 771
CUMMINGS, WILLIAM C, PAUL 0. THOMPSON, and
SAMUEL J. HA, "Sounds from Bryde, Balaenoptera
edeni, and finback, B. physalus, whales in the Gulf of
California" 359
DAILEY, MURRAY D, and STEPHEN RALSTON,
"Aspects of the reproductive biology, spatial distribution,
growth, and mortality of the deepwater caridean shrimp,
Heterocarpus laevigatus, in Hawaii" 915
Dams, hydroelectric
striped bass feeding area 220
DANDONNEAU, YVES, "Monitoring the sea surface
chlorophyll concentration in the tropical Pacific: conse-
quences of the 1982-83 El Nino" 687
DANIELS, ROBERT A.-see MOYLE et al.
DEAN, JOHN M.-see PRINCE et al.
Delphinus delphis—see Dolphin, common
de MENDIOLA, BLANCA ROJAS-see FORWARD et al.
"Determining age of larval fish with the otolith increment
technique," by Cynthia Jones 91
"Development and evaluation of methodologies for assess-
ing and monitoring the abundance of widow rockfish,
Sebastes entomelas," by Mark E. Wilkins 287
Developmental studies
scombroid fishes 647
"Diel foraging activity of American eels, Anguilla rostrata
(LeSueur), in a Rhode Island estuary," by Peter W.
Sorensen, Marco L. Bianchini, and Howard E. Winn . . 746
"Diet of northern fur seals, Callorhinus ursinus, off
western North America," by Michael A. Perez and Michael
A. Bigg 957
"Differentiation of Prionotus carolinus and Prionotus
evolans eggs in Hereford Inlet estuary, southern New
Jersey, using immunodiffusion," by Walter J. Keirans,
Sidney S. Herman, and R. G. Malsberger 63
Dinoflagellates
swimming speed of Gymnodinium splendens 461
parasites of benthic amphipods 605
"Discrete-time difference model for simulating interacting
fish population dynamics," by C. Allen Atkinson 535
Disease
epizootic sarcoma in soft shell clams 851
Dissolved oxygen concentration
effect on shrimp and bottomfish in Louisiana coastal
waters 19
"Distribution and abundance of common dolphin, Del-
phinus delphis, in the Southern California Bight: a quan-
titative assessment based upon aerial transect data," by
Thomas P. Dohl, Michael L. Bonnell, and R. Glenn Ford . . 333
"Distribution and reproductive biology of the golden king
crab, Lithodes aequispina, in the eastern Bering Sea," by
David A. Somerton and Robert S. Otto 571
"The distribution of the humpback whale, Megaptera
novaeangliae, on Georges Bank and in the Gulf of Maine
in relation to densities of the sand eel, Ammodytes
americanus," by P. Michael Payne, John R. Nicolas,
Loretta O'Brien, and Kevin D. Powers 271
DITTY, JAMES G., "Ichthyoplankton in neritic waters of
the northern Gulf of Mexico off Louisiana: composition,
relative abundance, and seasonality" 935
DOHL, THOMAS P., MICHAEL L. BONNELL, and R.
GLENN FORD, "Distribution and abundance of common
dolphin, Delphinus delphis, in the Southern California
Bight: a quantitative assessment based upon aerial transect
data" 333
Dolphin, common
distribution and abundance in southern California . . . 333
1005
Dolphin (fish)
growth in Hawaiian waters by daily increments 186
stock structure in western central Atlantic 451
Dolphin, spotted
reproductive biology in eastern tropical Pacific 247
Dolphins
increase in population size 527
mortality
due to tuna purse seine fishery 27
in eastern tropical Pacific tuna fishery 559
"Early development of the Lophiid anglerfish, Lophius
gastrophysus," by Yasunobu Matsuura and Nelson Takumi
Yoneda 429
EARLY, GREG-see SELZER et al.
"Early life history of Atlantic menhaden, Brevoortia tyran-
nus, and gulf menhaden, B. patronus" by Allyn B. Powell
and Germano Phonlor 991
ECHEVERRIA, TINA WYLLIE-see LENARZ and
ECHEVERRIA
Echo integration
assessing widow rockfish abundance 287
"An ecological survey and comparison of bottom fish
resource assessments (submersible versus handline fishing)
at Johnston Atoll," by Stephen Ralston, Reginald M.
Gooding, and Gerald M. Ludwig 141
Ecology
anthozoans 625
bottom fish resource assessment at Johnston Atoll . . 141
community studies in seagrass meadows 443
"Ecology of Ceriantharia (Coelenterata, Anthozoa) of the
northwest Atlantic from Cape Hatteras to Nova Scotia,"
by Andrew N. Shepard, Roger B. Theroux, Richard A.
Cooper, and Joseph R. Uzmann 625
Economic studies
spiny lobster 69, 74
Ecosystems
fish population dynamic simulations 535
Eel, American
diel foraging activity 746
Eel, sand
relationship to humpback whale 271
"Effects of exposure and confinement on spiny lobsters,
Panulirus argus, used as attractants in the Florida trap
fishery," by John H. Hunt, William G. Lyons, and Frank
S. Kennedy, Jr 69
"Effects of temperature on swimming speed of the
dinoflagellate, Gymnodinium splendens," by Richard B.
Forward, Jr., Blanca Rojas de Mendiola, and Richard T.
Barber 460
1006
El Nino
chlorophyll concentration in tropical Pacific 687
correlations of seabirds and salmon smolts 279
fat volume of yellowtail rockfish 743
Engraulis mordax—see Anchovy, northern
Euphausia pacifica 161
Euphausiids
distribution and abundance in California Current .... 161
invertebrate prey of Pacific salmon 77
"Ex-vessel price linkages in the New England fishing in-
dustry," by Dale Squires 437
FARLEY, C. A., S. V. OTTO, and C. L. REINISCH, "New
occurrence of epizootic sarcoma in Chesapeake Bay soft
shell clams, Mya armaria 851
FAVUZZI, JC N-see WILLASON et al.
"Fecundity of northern shrimp, Pandalus borealis,
(Crustacea, Decapoda) in areas of the Northwest Atlantic,"
by D. G. Parsons and G. E. Tucker 549
"Fecundity of the Pacific hake, Merluccius productus,
spawning in Canadian waters," by J. C. Mason 209
FINUCANE, JOHN H., L. ALAN COLLINS, HAROLD
A. BRUSHER, and CARL H. SALOMAN, "Reproductive
biology of king mackerel, Scomberomorus cavalla, from the
southeastern United States" 841
FIORELLI, PATRICIA M.-see SELZER et al.
"First record of the longfin mako, Isurus paucus, in the
Gulf of Mexico," by Kristie Killam and Glenn Parsons. . 748
Fish.
assemblages in kelp forests 799
resilience in New England tidepools 200
"Fish assemblages in Macrocystis and Nereocystis kelp
forests off central California," by James Lee Bodkin . . 799
Fish population studies
food consumption estimates 827
simulating population dynamics 535
Fishery
crab, golden king 571
hypoxia in Louisiana coastal waters 19
management 697
menhaden, gulf 311
rockfish, commercial 409
spiny lobster, Florida 69
tuna purse seine and dolphin mortality 27
tuna, yellowfin 247, 559
Fishes
community studies in seagrass meadows 443
distribution and abundance in Suisan Marsh 105
Fishes, reef
trauma from trawling and angling 697
Fishing
ex-vessel price in New England fishing industries . . . 437
multispecies intensive fishing experiment 423
shrimp
caridean 927
submersible versus handline 141
Fistulicola plicatus—see Tapeworm
Flounder
ex-vessel price linkages in New England 437
Flounder, arrowtooth
food habits in eastern Bering Sea 615
genetic confirmation of specific distinction 222
Flounder, Kamchatka
food habits in eastern Bering Sea 615
genetic confirmation 222
Flounder, yellowtail
statistical methods for estimating abundance 519
FOLKVORD, ARILD, and JOHN R. HUNTER, "Size-
specific vulnerability of northern anchovy, Engraulis mor-
dax, larvae to predation by fishes" 859
Food habits
bass, striped 220
fish consumption estimates 615
flounder 615, 827
hake, Pacific 947
salmon, Pacific 77
seal, northern fur 957
"Food habits and diet overlap of two congeneric species,
Atheresthes stomias and Atheresthes evermanni, in the
eastern Bering Sea," by M. S. Yang and P. A. Livingston. . 615
FORD, R. GLENN-see DOHL et al.
FORWARD, RICHARD B., JR., BLANCA de MENDIOLA,
and RICHARD T. BARBER, "Effects of temperature on
swimming speed of the dinoflagellate, Gymnodinium splen-
dens" 460
FROST, KATHRYN J., and LLOYD F. LOWRY, "Sizes of
walleye pollock, Theragra chalcogramma, consumed by
marine mammals in the Bering Sea" 192
FULS, BILLY E.-see CODY and FULS
Gammaridean amphipods 204
"Genetic confirmation of specific distinction of arrowtooth
flounder, Atheresthes stomias, and Kamchatka flounder,
A. evermanni" by Carol L. Ranck, Fred M. Utter, George
B. Milner, and Gary B. Smith 222
Genetic studies
chromosomal analysis of tuna 469
specific distinction of flounder 222
Georges Bank
distribution of humpback whales 271
GIBSON, DARCY L.-see GRAHAM et al.
Gloucester
ex-vessel price in New England fishing industry .... 437
GOLDBERG, STEPHEN R.-see WEBER and
GOLDBERG
GOODING, REGINALD M.-see RALSTON et al.
GRAHAM, JEFFREY B., RICHARD H. ROSENBLATT,
and DARCY L. GIBSON, "Morphology and possible swim-
ming mode of a yellowfin tuna, Thunnus albacares, lack-
ing one pectoral fin" 463
GREENING, HOLLY S.-see LEBER and GREENING
Groupers
unexploited resources in the Marianas 759
GROVER, JILL J., and BORI L. OLLA, "Morphological
evidence for starvation and prey size selection of sea-
caught larval sablefish, Anoplopoma fimbria" 484
"Growth, behavior, and sexual maturation of the market
squid, Loligo opalescens, cultured through the life cycle,"
by W. T. Yang, R. F. Hixon, P. E. Turk, M. E. Krejci, W.
H. Hulet, and R. T. Hanlon 771
"Growth of dolphins, Coryphaena hippurus, and C.
equiselis, in Hawaiian waters as determined by daily in-
crements on otoliths," by James H. Uchiyama, Raymond
K. Burch, and Syd A. Kraul, Jr 186
Growth rates
anchovy, northern 503
bass, black sea 723
bass, striped 905
catfish, sea 679
dolphin fishes in Hawaiian waters 186
herring, Pacific 705
shrimp, caridean 915
squid, market 771
Gulf of California
sounds of Bryde and finback whales 359
Gulf of Maine
distribution of humpback whales 271
Gulf of Mexico
first record of longfin mako 748
ichthyoplankton 935
Gymnodinium splendens—see Dinoflagellate
HA, SAMUEL J. -see CUMMINGS et al.
Habitat studies
cetaceans of the northeast United States .
Haddock
ex-vessel price in New England fishing industry
345
437
1007
Hake, Pacific
fecundity in Canadian waters 209
stomach contents and food consumption 947
HANLON, R. T.-see YANG et al.
HARRIS, R. E., JR.-see VAN ENGEL et al.
Hatcheries
growth and survival of striped bass 905
HAWKES, CLAYTON R, THEODORE R. MEYERS, and
THOMAS C. SHIRLEY, "Length-weight relationships of
blue, Paralithodes platypus, and golden, Lithodes
aequispina, king crabs parasitized by the rhizocephalan,
Briarosaccus callosus Boschma" 327
HERBOLD, BRUCE-see MOYLE et al.
HERMAN, SIDNEY S.-see KEIRANS et al.
Herring, Pacific
annual production 705
Heterocarpus laevigatas— see Shrimp, caridean
Heterostichus rostratus—see Kelpfish, giant
Histology
starvation induced mortality 1
HIXON, R. F.-see YANG et al.
HOGANS, W. E., and P. C. F. HURLEY, "Variations in the
morphology of Fistulicola plicatus Rudolphi (1802)
(Cestoda: Pseudophyllidea) from the swordfish, Xiphias
gladius L., in the northwest Atlantic Ocean" 754
HOHN, A. A. -see MYRICK et al.
Homarus americanus—see Lobster, American
HOUDE, EDWARD D, and LAWRENCE LUBBERS III,
"Survival and growth of striped bass, Morone saxatilis,
and Morone hybrid larvae: laboratory and pond enclosure
experiments 905
HULET, W H.-see YANG et al.
HUMES, ARTHUR G., "Copepodids and adults of Lep-
tinogaster major (Williams, 1907), a poecilostomatoid
copepod living in Mya arenaria L. and other marine bivalve
mollusks" 227
HUNT, JOHN H., WILLIAM G. LYONS, and FRANK S.
KENNEDY, JR., "Effects of exposure and confinement on
spiny lobsters, Panulirus argus, used as attractants in the
Florida trap fishery" 69
HUNTE, WAYNE-see OXENFORD and HUNTE
HUNTER, J. ROE, BEVERLY J. MACEWICZ, and JOHN
R. SIBERT, "The spawning frequency of skipjack tuna,
Katsuwonus pelamis, from the South Pacific" 895
HUNTER, JOHN R.-see FOLKVORD and HUNTER
1008
HURLEY, P. C. F.-see HOGANS and HURLEY
Hybrids, bass striped
survival and growth 905
"Hypoxia in Louisiana coastal waters during 1983: implica-
tions for fisheries," by Maurice L. Renaud 19
"Ichthyoplankton in neritic waters of the northern Gulf of
Mexico off Louisiana: composition, relative abundance, and
seasonality," by James G. Ditty 935
Immunodiffusion
differentiation of Prionotus eggs 63
"An improved otter surface sampler," by J. C. Mason and
A. C. Phillips 480
"Incidental dolphin mortality in the eastern tropical Pacific
tuna fishery, 1973 through 1978," by Bruce E. Wahlen . . 559
"Incidental mortality of dolphins in the eastern tropical
Pacific, 1959-72," by N. C. H. Lo and T. D. Smith .... 27
"Increased food and energy consumption of lactating
northern fur seals, Callorhinus ursinus," by Michael A.
Perez and Elizabeth E. Mooney 371
"Instar identification and life history aspects of juvenile
deepwater spider crabs, Chionoecetes tanneri Rathbun,"
by Patricia A. Tester and Andrew G. Carey, Jr 973
"An intensive fishing experiment for the caridean shrimp,
Heterocarpus laevigatas, at Alamagan Island in the
Mariana Archipelago," by Stephen Ralston 927
Istiophorus platypterus—see Sailfish, Atlantic
Isurus paucus—see Shark, longfin mako
JAVECH, JOAQUIN C.-see POTTHOFF et al.
JOHNSON, P. T, R. A. MacINTOSH, and D. A. SOMER-
TON, "Rhizocephalan infection in blue king crabs,
Paralithodes platypus, from Olga Bay, Kodiak Island,
Alaska" 177
JOHNSON, PHYLLIS T., "Parasites of benthic amphi-
pods: ciliates" 204
JOHNSON, PHYLLIS T., "Parasites of benthic amphi-
pods: dinoflagellates (Duboscquodinida: Syndinidae) . . . 605
Johnston Atoll
resource assessment 141
Jolly-Seber
spawning escapement of chinook salmon 261
JONES, CYNTHIA, "Determining age of larval fish with
the otolith increment technique" 91
Katsuwonus pelamis— see Tuna, skipjack
KEIRANS, WALTER J., SIDNEY S. HERMAN, and R.
G. MALSBERGER, "Differentiation of Prionotus
carolinus and Prionotus evolans eggs in Hereford Inlet
estuary, southern New Jersey, using immunodiffusion" . . 63
KELLEY, SHARON-see POTTHOFF et al.
Kelp, bull
fish assemblages in kelp forests 799
Kelp forests
fish assemblages 799
Kelp, giant
fish assemblages in kelp forests 799
Kelpfish, giant
life history and larval development 809
KENNEDY, FRANK S., JR.-see HUNT et al.
KENNEY, ROBERT D, and HOWARD E. WINN, "Ceta-
cean high-use habitats of the northeast United States con-
tinental shelf" ■ 345
KILLAM, KRISTIE, and GLENN PARSONS, "First
record of the longfin mako, Isurus paucus, in the Gulf of
Mexico" 748
KLINGBEIL, RICHARD A.-see PARRISH et al.
KRAUL, SYD A., JR.-see UCHIYAMA et al.
KREJCI, M. E.-see YANG et al.
KRYGIER, E. E, and W G PEARCY, "The role of
estuarine and offshore nursery areas for young English
sole, Parophrys vetulus Girard, of Oregon" 119
KYNARD, BOYD-see STIER and KYNARD
-see WARNER and KYNARD
Lampreys, sea
abundance, size, and sex ratio 476
movement in the Connecticut River 749
LANGSTON, HIRAM T.-see ROGERS et al.
Larvae
anchovy, northern
in the California Current 585
instantaneous mortality rates 395
spawning and predation in San Francisco Bay 879
vulnerability of 859
anglerfish, lophiid
early development and comparison with other lophiid
species 429
bass, striped
survival and growth 905
fish
age determination 91
kelpfish, giant 809
mackerel, jack 1
mussels, blue
spawning and seasonality 995
sablefish
starvation and prey size selection 484
scombroid
cartilage and bone development 647
LAURS, R. M.-see RATTY et al.
LEBER, KENNETH M., and HOLLY S. GREENING,
"Community studies in seagrass meadows: A comparison
of two methods for sampling macroinvertebrates and
fishes" 443
LEE, DENNIS W.-see PRINCE et al.
LENARZ, WILLIAM H., and TINA WYLLIE ECHE-
VERRIA, "Comparison of visceral fat and gonadal fat
volumes of yellowtail rockfish, Sebastesflavidus, during a
normal year and a year of El Nino conditions" 743
"Length-weight relationships of blue, Paralithodes platy-
pus, and golden, Lithodes aequispina, king crabs para-
sitized by the rhizocephalan, Briarosaccus callosus
Boschma," by Clayton R. Hawkes, Theodore R. Meyers,
and Thomas C. Shirley 327
Leptinogaster major— see Copepod, poecilostomatoid
Leslie model
dolphin population studies 527
fish population studies 535
variable catchability version 423
"Life history and larval development of the giant kelpfish,
Heterostichus rostratus Girard, 1854," by Carol A.
Stepien 809
Life history studies
bass, black sea 723
crab, spider 973
kelpfish, giant 809
menhaden, Atlantic and gulf 991
Limanda ferruginea—see Flounder, yellowtail
Line intercept survey
assessing widow rockfish abundance 287
Line transect survey
assessing widow rockfish abundance 287
Literature review
daily deposition of otolith increments 91
Lithodes aequispina— see Crab, golden king
LIVINGSTON, P. A.-see YANG and LIVINGSTON
LO, NANCY C. H., "Modeling life-stage-specific instan-
taneous mortality rates, an application to northern
anchovy, Engraulis mordax, eggs and larvae" 395
LO, N. C. H, and T D SMITH, "Incidental mortality of
dolphins in the eastern tropical Pacific, 1959-72" 27
Lobster, American
occurrence of parasites 197
1009
Lobster, spiny
in Florida trap fishery 69
Loligo opalescens—see Squid, market
"Longevity and age validation of a tag-recaptured Atlan-
tic sailfish, Istiophoms platypterus, using dorsal spines and
otoliths," by Eric D. Prince, Dennis W. Lee, Charles A.
Wilson, and John M. Dean 493
Lophius gastrophysus—see Anglerfish, lophiid
Louisiana
hypoxia in coastal waters 19
LOWRY, LLOYD F.-see FROST and LOWRY
LUBBERS, LAWRENCE Ill-see HOUDE and
LUBBERS
LUDWIG, GERALD M.-see RALSTON et al.
LYONS, WILLIAM G.-see HUNT et al.
MACEWICZ, BEVERLY J.-see HUNTER et al.
MacINTOSH, R. A.-see JOHNSON et al.
Mackerel, jack
histological analysis 2
morphological analysis 2
offshore starvation 1
reproductive biology 841
starvation-induced mortality 1
Macrocytis pyrifera—see Kelp, giant
Macroinvertebrates
community studies in seagrass meadows 443
Macrouridae
abundance and distribution in Norfolk Canyon 35
Makalii— see Submersible
Mako, longfin— see Shark, longfin mako
MALLICOATE, DONNA L.-see PARRISH et al.
MALSBERGER, R. G.-see KEIRANS et al.
Manly-Parr
model for spawning escapement of chinook salmon . . 261
Mariana Archipelago
fishing experiment for caridean shrimp 927
Marine mammals
sizes of walleye pollock consumed 192
MASON, J. C, "Fecundity of the Pacific hake, Merluccius
productus, spawning in Canadian waters" 209
MASON, J. C, and A. C. PHILLIPS, "An improved otter
surface sampler" 480
1010
MATSUURA, YASUNOBU, and NELSON TAKUMI
YONEDA, "Early development of the lophiid anglerfish,
Lophius gastrophysus" 429
McALICE, BERNARD, J.-see PODNIESINSKI and
McALICE
McGOWAN, MICHAEL F., "Northern anchovy, Engraulis
mordax, spawning in San Francisco Bay, California,
1978-79, relative to hydrography and zooplankton prey of
adults and larvae" 879
Megaptera novaeangliae—see Whale, humpback
Menhaden, Atlantic
early life history 991
Menhaden, gulf
early life history 991
population and fishery characteristics 311
Merluccius productus— see Hake, Pacific
MERRINER, JOHN V.-see SMITH, JOSEPH W
"Methodological problems in sampling commercial rockfish
landings," by A. R. Sen 409
MEYERS, THEODORE R.-see HAWKES et al.
Micropogonius undulatus—see Croaker, Atlantic
MIDDLETON, ROBERT W., and JOHN A. MUSICK,
"The abundance and distribution of the family Macrouridae
(Pisces: Gadiformes) in the Norfolk Canyon area" 35
MILNER, GEORGE B.-see RANCK et al.
"A model of the drift of northern anchovy, Engraulis mor-
dax, larvae in the California Current," by James H. Power. . 585
"Modeling life-stage-specific instantaneous mortality rates,
an application to northern anchovy, Engraulis mordax,
eggs and larvae," by Nancy C. H. Lo 395
Models
estimating food consumption of fish populations 827
Leslie 423
life-stage-specific instantaneous mortality rates 395
Manly-Parr 261
"Monitoring the sea surface chlorophyll concentration in
the tropical Pacific: consequences of the 1982-83 El Nino,"
by Yves Dandonneau 687
MOONEY, ELIZABETH E.-see PEREZ and MOONEY
Morone saxatilis—see Bass, striped
"Morphological evidence for starvation and prey size selec-
tion of sea-caught larval sablefish, Anoplopoma fimbria,"
by Jill J. Grover and Bori L. Olla 484
"Morphology and possible swimming mode of a yellowfin
tuna, Thunnus albacares, lacking one pectoral fin," by
Jeffrey B. Graham, Richard H. Rosenblatt, and Darcy L.
Gibson 463
"Movement of sea-run sea lampreys, Petromyzon marinus,
during the spawning migration in the Connecticut River,"
by Kathleen Stier and Boyd Kynard 749
MOYLE, PETER B., ROBERT A. DANIELS, BRUCE
HERBOLD, and DONALD M. BALTZ, "Patterns in
distribution and abundance of a noncoevolved assemblage
of estuarine fishes in California" 105
MUSICK, JOHN A.-see MIDDLETON and MUSICK
Mussel, blue
larvae in Damariscotta River estuary, Maine 995
Mya arenaria—see Clam, soft shell
MYRICK, A. C, JR., A. A. HOHN, J. BARLOW, and P. A.
SLOAN, "Reproductive biology of female spotted dolphins,
Stenella attenuata, from the eastern tropical Pacific" . . 247
Mytilus edulis—see Mussel, blue
NELSON, WALTER R, and DEAN W AHRENHOLZ,
"Population and fishery characteristics of gulf menhaden,
Brevoortia patronus" 311
Nematoscelis difficilis 157
Nereocystis leutkeana—see Kelp, bull
Netuma barba—see Catfish, sea
Neuston sampler
an improved otter surface sampler 480
New Bedford
ex-vessel price in New England fishing industry .... 437
New England
ex-vessel price in New England fishing industry .... 437
"New occurrence of epizootic sarcoma in Chesapeake Bay
soft shell clams, Mya arenaria," by C. A. Farley, S. V.
Otto, and C. L. Reinisch 851
Nezumia aequalis
abundance and distribution in Norfolk Canyon 35
Nezumia bairdii
abundance and distribution in Norfolk Canyon 35
NICHOLAS, JOHN R.-see PAYNE et al.
"Northern anchovy, Engraulis mordax, spawning in San
Francisco Bay, California, 1978-79, relative to hydrography
and zooplankton prey of adults and larvae," by Michael F.
McGowan 879
Nursery studies
estuary studies 119
"Observations on the reproductive biology of the cownose
ray, Rhinoptera bonasus in Chesapeake Bay," by Joseph
W. Smith and John V. Merriner 871
O'BRIEN, LORETTA-see PAYNE et al.
"Occurrence of some parasites and a commensal in the
American lobster, Homarus americanus, from the Mid-
Atlantic Bight," by W. A. Van Engel, R. E. Harris, Jr.,
and D. E. Zwerner 197
OLLA, BORI L.-see GROVER and OLLA
Oncorhynchus gorbuscha—see Salmon, pink
Oncorhynchus kisutch—see Salmon, coho
Oncorhynchus nerka—see Salmon, sockeye
Oncorhynchus tshawytscha—see Salmon, chinook
Oregon
nursery areas for English sole 119
"Organic and trace metal levels in ocean quahog, Arctica
islandica Linne, from the northwestern Atlantic," by
Frank W. Steimle, Paul D. Boehm, Vincent S. Zdanowicz,
and Ralph A. Bruno 133
Otoliths
age validation in Atlantic sailfish 493
catfish, sea 679
disposition rates 91
dolphin fishes in Hawaiian waters 186
increment technique for aging larval fishes 493
Otter surface sampler 480
OTTO, ROBERT S.-see SOMERTON and OTTO
OTTO, S. V.-see FARLEY et al.
OXENFORD, HAZEL A., and WAYNE HUNTE, "A pre-
liminary investigation of the stock structure of the dolphin,
Coryphaena hippurus, in the western central Atlantic" . . 451
Pacific eastern tropical
reproductive biology of the spotted dolphin 247
Pandalus borealis—see Shrimp, northern
Panulirus argus—see Lobster, spiny
Paralithodes platypus— see Crab, king
Parasite studies
American lobster 197
benthic amphipods infected with dinoflagellates 605
rhizocephalan infection in king crab 327
swordfish tapeworm 754
"Parasites of benthic amphipods: ciliates," by Phyllis T.
Johnson 204
"Parasites of benthic amphipods: dinoflagellates (Dubosc-
quodinida: Syndinidae)," by Phyllis T. Johnson 605
Parathemisto (hyperiid amphipod)
food items of Pacific salmon 77
1011
Parophrys vetulus—see Sole, English
PARRISH, RICHARD H., DONNA L. MALLICOATE, and
RICHARD A. KLINGBEIL, "Age dependent fecundity,
number of spawnings per year, sex ratio, and maturation
stages in northern anchovy, Engraulis mordax" 503
PARSONS, D. G., and G. E. TUCKER, "Fecundity of north-
ern shrimp, Pandalus borealis, (Crustacea, Decapoda) in
areas of the Northwest Atlantic" 549
PARSONS, GLENN-see KILLAM and PARSONS
"Patchiness and nutritional condition of zooplankton in the
California Current," by Stewart W. Willason, John
Favuzzi, and James L. Cox 157
"Patterns in distribution and abundance of a noncoevolved
assemblage of estuarine fishes in California," by Peter B.
Moyle, Robert A. Daniels, Bruce Herbold, and Donald M.
Baltz 105
PAULY, DANIEL, "A simple method for estimating the
food consumption of fish populations from growth data and
food conversion experiments" 827
PAYNE, P. MICHAEL, JOHN R. NICOLAS, LORETTA
O'BRIEN, and KEVIN D. POWERS, "The distribution of
the humpback whale, Megaptera novaeangliae, on Georges
Bank and in the Gulf of Maine in relation to densities of
the sand eel, Ammodytes americanus" 271
PAYNE, P. MICHAEL-see SELZER et al.
PCB's
organic and trace metals in ocean quahog 133
PEARCY, W. G.-see KRYGIER and PEARCY
Penaeus aztecus—see Shrimp, brown
Penaeus setiferus—see Shrimp, white
PENNINGTON, MICHAEL, "Some statistical techniques
for estimating abundance indices from trawl surveys" . . 519
PEREZ, MICHAEL A., and MICHAEL A. BIGG, "Diet
of northern fur seals, Callorhinus ursinus, off western
North America" 957
PEREZ, MICHAEL A., and ELIZABETH E. MOONEY,
"Increased food and energy consumption of lactating
northern fur seals, Callorhinus ursinus" 371
Petromyzon marinus—see Lampreys, sea
PHILLIPS, A. C.-see MASON and PHILLIPS
Phoca vitulina concolor—see Seal, harbor
PHONLOR, GERMANO-see POWELL and PHONLOR
Phytoplankton
zooplankton biomass and nutritional parameters 157
PIKITCH, ELLEN K.-see REXSTAD and PIKITCH
1012
Plankton
identification of Prionotus 63
PODNIESINSKI, GREG S., and BERNARD J. McALICE,
"Seasonality of blue mussel, Mytilus edulis L., larvae in
the Damariscotta River estuary, Maine, 1969-77" 995
Pollock
ex-vessel price in New England fishing industry .... 437
Pollock, walleye
sizes consumed by marine mammals in the Bering
Sea 192
Pollution
benthic animals as indicator species 133
POLOVINA, JEFFREY J., "A variable catchability ver-
sion of the Leslie model with application to an intensive
fishing experiment on a multispecies stock" 423
POLOVINA, JEFFREY J., and STEPHEN RALSTON,
"An approach to yield assessment for unexploited
resources with application to the deep slope fishes of the
Marianas" 759
POP surveys
cetacean high-use habitats 345
"Population and fishery characteristics of gulf menhaden,
Brevoortia patronus," by Walter R. Nelson and Dean W.
Ahrenholz 311
Population sampling devices
shrimp trawls 981
Population studies
bass, black sea 723
dolphin 527
fish 535
menhaden, gulf 311
sardine 540
POTTHOFF, THOMAS, SHARON KELLEY, and JOA-
QUIN C JAVECH, "Cartilage and bone development in
scombroid fishes" 647
POWELL, ALLYN B„ and GERMANO PHONLOR,
"Early life history of Atlantic menhaden, Brevoortia tyran-
nus, and gulf menhaden, B. patronus" 991
POWER, JAMES H., "A model of the drift of northern
anchovy, Engraulis mordax, larvae in the California
Current" 585
POWERS, KEVIN D.-see PAYNE et al.
Predation
of northern anchovy 859
"A preliminary investigation of the stock structure of
the dolphin, Coryphaena hippurus, in the western
central Atlantic," by Hazel A. Oxenford and Wayne
Hunte 451
PRESCOTT, ROBERT-see SELZER et al.
PRINCE, ERIC D., DENNIS W. LEE, CHARLES A.
WILSON, and JOHN M. DEAN, "Longevity and age
validation of a tag-recaptured Atlantic sailfish, Istiophorus
platypterus, using dorsal spines and otoliths" 493
Prionotus carolinus—see Searobin, northern
Prionotus evolans—see Searobin, striped
Quahog, ocean
organic and trace metal levels
133
QUAST, JAY C, "Annual production of eviscerated body
weight, fat, and gonads by Pacific herring, Clupea haren-
gus pallasi, near Auke Bay, southeastern Alaska" .... 705
RALSTON, STEPHEN-see DAILEY and RALSTON
-see POLOVINA and RALSTON
RALSTON, STEPHEN, "An intensive fishing experiment
for the caridean shrimp, Heterocarpus laevigatus, at
Alamagan Island in the Marina Archipelago" 927
RALSTON, STEPHEN, REGINALD M. GOODING, and
GERALD M. LUDWIG, "An ecological survey and com-
parison of bottom fish resource assessments (submersible
versus handline fishing) at Johnston Atoll" 141
RANCK, CAROL L., FRED M. UTTER, GEORGE B.
MILNER, and GARY B. SMITH, "Genetic confirmation
of specific distinction of arrowtooth flounder, Atheresthes
stomias, and Kamchatka flounder, A. evermanni" 222
"Rates of increase in dolphin population size," by Stephen
B. Reilly and Jay Barlow 527
RATTY, F. J., Y. C. SONG, and R. M. LAURS,
"Chromosomal analysis of albacore, Thunnus alalwnga,
and yellowfin, Thunnus albacares, and skipjack, Katsu-
wonus pelamis, tuna" 469
Ray, cownose
reproductive biology 871
Red tide
effects on Gymnodinium splendens swimming
speed 460
REINISCH, C. L.-see FARLEY et al.
REILLY, STEPHEN B., and JAY BARLOW, "Rates of
increase in dolphin population size" 527
REIS, ENIR GIRONDI, "Age and growth of the marine
catfish, Netuma barba (Siluriformes, Ariidae), in the
estuary of the Patos Lagoon (Brasil)" 679
RENAUD, MAURICE L., "Hypoxia in Louisiana coastal
waters during 1983: implications for fisheries" 19
"Reproductive biology of female spotted dolphins,
Stenella attenuata, from the eastern tropical Pacific,"
by A. C. Myrick, Jr., A. A. Hohn, J. Barlow, and P. A.
Sloan 247
"Reproductive biology of king mackerel, Scomberomorus
cavalla, from the southeastern United States," by John H.
Finucane, L. Alan Collins, Harold A. Brusher, and Carl H.
Saloman 841
Reproductive studies
anchovy, northern 503, 879
bass, black sea 723
crab, golden king 571
dolphin, spotted 247
mackerel, king 841
mussel, blue 995
ray, cownose 871
shrimp, caridean 915
squid, market 771
tuna, skipjack 895
"Resilience of the fish assemblage in New England
tidepools," by Bruce B. Collette 200
Resource assessment techniques
hydroacoustic echo integration 287
line intercept survey 287
line transect survey 287
abundance of widow rockfish 287
REXSTAD, ERIC A, and ELLEN K. PIKITCH, "Stomach
contents and food consumption estimates of Pacific hake,
Merluccius productus" 947
Rhinoptera loonasus—see Ray, cownose
"Rhizocephalan infection in blue king crabs, Paralithodes
platypus, from Olga Bay, Kodiak Island, Alaska," by P.
T. Johnson, R. A. Macintosh, and D. A. Somerton 177
Rhizocephalans
length-weight relationships of king crab 327
Rockfish
problems in sampling commercial landings 409
Rockfish, widow
behavior studies 287
methodologies for assessing abundance 287
Rockfish, yellowtail
fat volume comparisons 743
ROGERS, S. GORDON, HIRAM T LANGSTON, and
TIMOTHY E. TARGETT, "Anatomical trauma to sponge-
coral reef fishes captured by trawling and angling" . . . 697
"The role of estuarine and offshore nursery areas for young
English sole, Parophrys vetulus Girard, of Oregon," by E.
E. Krygier and W. G. Pearcy 119
ROSENBLATT, RICHARD H.-see GRAHAM et al.
ROUMILLAT, WILLIAM A.-see WENNER et al.
Sablefish, larval
starvation
prey size selection
484
484
1013
Sailfish, Atlantic
longevity and age validation 493
Salmon, chinook
methods used to estimate spawning escapement 261
Salmon, Pacific
food habits in the Strait of Juan de Fuca 77
Salmon, smolts
correlation with seabirds 279
SALOMAN, CARL H.-see FINUCANE et al.
Samplers
improved otter surface sampler 480
Sarcoma
occurrence in soft shell clams 851
Sardine
population collapse 535
population studies 535
"Scavenger feeding by subadult striped bass, Morone sax-
atilis, below a low-head hydroelectric dam," by John
Warner and Boyd Kynard 220
Scomberomorus cavallasee Mackerel, king
Scombroid fish
cartilage and bone development 647
Sea surface studies
monitoring chlorophyll concentration in the tropical
Pacific 687
Seabirds
correlations with salmon smolts 279
"Seabirds near an Oregon estuarine salmon hatchery in
1982 and during the 1983 El Nino," by Range D. Bayer . . 279
Seagrass meadows
community studies 443
comparison of two sampling methods 443
Seal, harbor
in southern New England 217
Seal, northern fur
arrival times and numbers on St. Paul Island, Alaska. . 383
diet 957
food and energy consumption of lactating females . . . 371
Searobin, northern
differentiation of Prionotus eggs 63
Searobin, striped
differentiation of Prionotus eggs 63
"Seasonality of blue mussel, Mytilus edulis L., larvae in
the Damariscotta River estuary, Maine, 1969-77," by Greg
S. Podniesinski and Bernard J. McAlice 995
Sebastes entomelas—see Rockfish, widow
1014
Sebastes flavidus— see Rockfish, yellowtail
SELZER, LAWRENCE, A, GREG EARLY, PATRICIA M.
FIORELLI, P. MICHAEL PAYNE, and ROBERT
PRESCOTT, "Stranded animals as indicators of prey
utilization by harbor seals, Phoca vitulina concolor, in
southern New England" 217
SEN, A. R., "Methodological problems in sampling com-
mercial rockfish landings" 409
"The sex ratio and gonad indices of swordfish, Xiphias
gladius, caught off the coast of Southern California in
1978," by Earl C. Weber and Stephen R. Goldberg ... 185
Shark, longfin mako
first record in the Gulf of Mexico 748
SHEPARD, ANDREW N„ ROGER B. THEROUX,
RICHARD A. COOPER, and JOSEPH R. UZMANN,
"Ecology of Ceriantharia (Coelenterata, Anthozoa) of the
northwest Atlantic from Cape Hatteras to Nova Scotia" . . 625
SHIRLEY, THOMAS C.-see HAWKES et al.
Shrimp
affect of hypoxia on abundance and distribution 19
Shrimp, caridean
an intensive fishing experiment 927
reproduction, distribution, and growth 915
Shrimp, northern
fecundity studies in northwest Atlantic 549
Shrimp, penaid
population sampling 981
Shrimp, pink— see Shrimp, northern
SIBERT, JOHN R.-see HUNTER et al.
"A simple method for estimating the food consumption of
fish populations from growth data and food conversion ex-
periments," by Daniel Pauly 827
"Sizes of walleye pollock, Theragra chalcogramma, con-
sumed by marine mammals in the Bering Sea," by Kathryn
J. Frost and Lloyd F. Lowry 192
"Size-specific vulnerability of northern anchovy, Engraulis
mordax, larvae to predation by fishes," by Arild Folkvord
and John R. Hunter 859
SLOAN, P. A. -see MYRICK et al.
SMITH, GARY B.-see RANCK et al.
SMITH, JOSEPH, W., and JOHN V. MERRINER, "Obser-
vations on the reproductive biology of the cownose ray,
Rhinoptera bonasus, in Chesapeake Bay" 87
SMITH, T. D.-see LO and SMITH
Snappers
yield assessment in the Marianas 759
Sole, English
estuarine and offshore nursery areas 119
SOMERTON, D. A.-see JOHNSON et al.
SOMERTON, DAVID A., and ROBERT S. OTTO, "Distri-
bution and reproductive biology of the golden king crab,
Lithodes aequispina, in the eastern Bering Sea" 571
"Some statistical techniques for estimating abundance in-
dices from trawl surveys," by Michael Pennington .... 519
SONG, Y. C.-see RATTY et al.
SORENSEN, PETER W., MARCO L. BIANCHINI, and
HOWARD E. WINN, "Diel foraging activity of American
eels, Anguilla rostrata (LeSueur), in a Rhode Island
estuary" 746
"Sounds from Bryde, Balaenoptera edeni, and finback, B.
physalus, whales in the Gulf of California," by William C.
Cummings, Paul 0. Thompson, and Samuel J. Ha 359
Southern California Bight
distribution and abundance of common dolphin 333
Squid, market
growth, behavior, and sexual maturation 771
SQUIRES, DALE, "Ex-vessel price linkages in the New
England fishing industry" 437
"The spawning frequency of skipjack tuna, Katsuwonus
pelamis, from the South Pacific," by J. Roe Hunter,
Beverly J. Macewicz, and John R. Sibert 895
"Starvation-induced mortality of young sea-caught jack
mackerel, Trachurus symmetricus, determined with
histological and morphological methods," by Gail H.
Theilacker 1
Statistical methods
estimating abundance 519
STEIMLE, FRANK W, PAUL D BOEHM, VINCENT S.
ZDANOWICZ, and RALPH A. BRUNO, "Organic and
trace metal levels in ocean quahog, Arctica islandica
Linne, from the northwestern Atlantic" 133
Stenella attenuata—see Dolphin, spotted
STEPIEN, CAROL A., "Life history and larval develop-
ment of the giant kelpfish, Heterostichus rostratus Girard,
1854" 809
STIER, KATHLEEN, and BOYD KYNARD, "Abundance,
size, and sex ratio of adult sea-run sea lampreys,
Petromyzon marinus, in the Connecticut River" 476
STIER, KATHLEEN, and BOYD KYNARD, "Movement
of sea-run sea lampreys, Petromyzon marinus, during the
spawning migration in the Connecticut River" 749
"Stomach contents and food consumption estimates of
Pacific hake, Merluccius productus," by Eric A. Rexstad
and Ellen K. Pikitch 947
"Stranded animals as indicators of prey utilization by
harbor seals, Phoca vitulina concolor, in southern New
England," by Lawrence A. Selzer, Greg Early, Patricia M.
Fiorelli, P. Michael Payne, and Robert Prescott 217
Submersibles
resource assessment at Johnston Atoll 141
"Survival and growth of striped bass, Morone saxatilis,
and Morone hybrid larvae: laboratory and pond enclosure
experiments," by Edward D. Houde and Lawrence
Lubbers III 905
Swordfish
sex ratio and gonad indices 185
morphology of Fistulicola plicatus 754
SYKES, STEPHEN D., and LOUIS W BOTSFORD,
"Chinook salmon, Oncorhynchus tshawytscha, spawning
escapement based on multiple mark-recapture of
carcasses" 261
TARGETT, TIMOTHY E.-see ROGERS et al.
Taxonomy
arrowtooth and Kamchatka flounders 222
TESTER, PATRICIA A., and ANDREW G. CAREY, JR.,
"Instar identification and life history aspects of juve-
nile deepwater spider crabs, Chionoecetes tanneri
Rathbun" 973
THEILACKER, GAIL H., "Starvation-induced mortality
of young sea-caught jack mackerel, Trachurus sym-
metricus, determined with histological and morphological
methods" 1
Theragra chalcogramma—see Pollock, walleye
THEROUX, ROGER B.-see SHEPARD et al.
THOMPSON, PAUL O.-see CUMMINGS et al.
Thunnus alalunga—see Albacore
Thunnus albacares—see Tuna, yellowfin
Tidepools
fish assemblages in New England 200
Townsend Cromwell
resource assessment at Johnston Atoll 141
Trachurus symmetricus— see Mackerel, jack
Trawls, shrimp
population sampling devices 981
Trawl surveys
statistical methods for estimating abundance 519
Trawling
anatomical trauma to sponge-coral reef fishes 697
TUCKER, G. E.-see PARSONS and TUCKER
1015
Tuna, skipjack
chromosomal analysis 469
spawning frequency 895
Tuna, yellowfin
chromosomal analysis 469
incidental dolphin mortality 559
morphology and swimming mode 463
TURK, P. E.-see YANG et al.
"Type, quantity, and size of food of Pacific salmon
(Oncorhynchus) in the Strait of Juan de Fuca, British
Columbia," by Terry D. Beacham 77
UCHIYAMA, JAMES H., RAYMOND K. BURCH, and
SYD A. KRAUL, JR., "Growth of dolphins, Coryphaena
hippurus and C. equiselis, in Hawaiian waters as deter-
mined by daily increments on otoliths"
Underwater sounds
Bryde and finback whales
186
359
UTTER, FRED M.-see RANCK et al.
UZMANN, JOSEPH R.-see SHEPARD et al.
WEBER, EARL C., and STEPHEN R. GOLDBERG,
"The sex ratio and gonad indices of swordfish, Xiphias
gladius, caught off the coast of Southern California in
1978" 185
WENNER, CHARLES A., WILLIAM A. ROUMILLAT,
and C. WAYNE WALTZ, "Contributions to the life history
of black sea bass, Centropristis striata, off the south-
eastern United States" 723
Whales, Bryde
underwater sounds in the Gulf of California 359
Whales, finback
underwater sounds in the Gulf of California 359
Whales, humpback
distribution in relation to sand eels 271
WILKINS, MARK E., "Development and evaluation of
methodologies for assessing and monitoring the abundance
of widow rockfish, Sebastes entomelas" 287
WILLASON, STEWART W, JOHN FAVUZZI, and
JAMES L. COX, "Patchiness and nutritional condition of
zooplankton in the California Current" 157
WILSON, CHARLES, A.-see PRINCE et al.
VAN ENGEL, W A., R. E. HARRIS, JR., and D. E.
ZWERNER, "Occurrence of some parasites and a com-
mensal in the American lobster, Homarus americanus,
from the Mid-Atlantic Bight" 197
"A variable catchability version of the Leslie model with
application to an intensive fishing experiment on a
multispecies stock," by Jeffrey J. Polovina 423
"Variations in the morphology of Fistulicola plicatus
Rudolphi (1802) (Cestoda: Pseudophyllidea) from the
swordfish, Xiphias gladius L., in the northwest Atlantic
Ocean," by W. E. Hogans and P. C. F. Hurley 754
WAHLEN, BRUCE E., "Incidental dolphin mortality in
the eastern tropical Pacific tuna fishery, 1973 through
1978" 559
WALTZ, C. WAYNE-see WENNER et al.
WARNER, JOHN, and BOYD KYNARD, "Scavenger
feeding by subadult striped bass, Morone saxatilis, below
a low-head hydroelectric dam" 220
WINN, HOWARD E.-see KENNEY and WINN
-see SORENSEN et al.
Xiphias gladius— see Swordfish
YANG, M. S., and P. A. LIVINGSTON, "Food habits and
diet overlap of two congeneric species, Atheresthes stomias
and Atheresthes evermanni, in the eastern Bering
Sea" 615
YONEDA, NELSON TAKUMI-see MATSUURA and
YONEDA
ZDANOWICZ, VINCENT S.-see STEIMLE et al.
Zooplankton
California Current
157
ZWERNER, D E.-see VAN ENGEL et al.
1016
NOTICES
NOAA Technical Reports NMFS published during first 6 months of 1986.
39. Survey of fish protective facilities at water withdrawl sites on the Snake
and Columbia Rivers. By George A. Swan, Tommy G. Withrow, and Donn
L. Park. April 1986, iii + 34 p., 26 figs., 6 tables.
Some NOAA publications are available by purchase from the Superintendent of Documents, U.S. Govern-
ment Printing Office, Washington, DC 20402.
Gulf of Mexico Ichthyoplankton Samples
The Gulf States Marine Fisheries Commission wishes to announce the availability of Gulf
of Mexico ichthyoplankton samples for loan to qualified researchers. Samples have been and
are continuing to be collected for SEAMAP (Southeast Area Monitoring and Assessment
Program), a multi-year international federal/state/university program of the GSMFC. Neuston
and bongo nets were employed for specimen collection in a one degree latitude/longitude
grid over the entire Gulf from 26 °N northward and sorted and preliminarily identified by
the Plankton Sorting and Identification Center, Szczecin, Poland. At present samples from
1982 (7057 lots, 93 families), 1983 (8351 lots, 106 families) and material from one summer
cruise in 1984 (4155 lots, 75 families) are available for loan. Lots of unsorted fish eggs are
also available from these years. Most samples are sorted to the family level, although many
have identification to generic or species level. Additional 1984 samples are expected to become
available by the end of 1986. Specimens are available for loan on a 6-month renewable basis.
Researchers interested in obtaining additional information can contact either SEAMAP
Ichthyoplankton Curator, Florida Department of Natural Resources, Bureau of Marine
Research, St. Petersburg, FL 33701, or SEAMAP Coordinator, Gulf States Marine Fisheries
Commission, P.O. Box 726, Ocean Springs, MS 39564.
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$,. Onteryts— Contim
REXSTAD, ERIC A., and ELLEN K. PUCITCH. Stomach contents and food consump-
tion estimates of Pacific hak< us productus 947
PEREZ, MICHAEL A and MV i ' iEL' A. BIGG. Diet of northern fur seals, CaUorhinvs
ursinus, off western D >'rica 957
TESTER, PATRICIA A NTPREW G. CAREY, JR. Instar identification and life
history aspects of ju\ deepvater spider crabs, Chionoecetes tanneri Rathbun . . . 973
jar Jfij Notes
CODY TERRY i E. FULS. Comparison of catches in 4.3 m and 12.2 m shrimp
trawls in th< M 'xico 981
POWELL, AT B. 4 GERMANO PHONLOR. Early life history of Atlantic men-
haden, Bre . ' ' innnus, and gulf menhaden, B. patronus 991
PODNL G s-> antl BERNARD J. McALICE. Seasonality of blue mussel,
arvae in the Damariscotta River estuary, Maine, 1969-77 995
1003
1017
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